Next Article in Journal
Humoral and Cellular Defense Mechanisms in Rebel Workers of Apis mellifera
Next Article in Special Issue
The Oleaginous Yeast Metschnikowia pulcherrima Displays Killer Activity against Avian-Derived Pathogenic Bacteria
Previous Article in Journal
Novel Algicides against Bloom-Forming Cyanobacteria from Allelochemicals: Design, Synthesis, Bioassay, and 3D-QSAR Study
Previous Article in Special Issue
Antibiotic Resistance of Staphylococci from Bulk-Tank Milk of Sheep Flocks: Prevalence, Patterns, Association with Biofilm Formation, Effects on Milk Quality, and Risk Factors
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Biology
Volume 10
Issue 11
10.3390/biology10111144
biology-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Systematic Review

Emerging Status of Multidrug-Resistant Bacteria and Fungi in the Arabian Peninsula

by
J. Francis Borgio
1,2,*,
Alia Saeed Rasdan
1,†,
Bayan Sonbol
1,†,
Galyah Alhamid
1,†,
Noor B. Almandil
3 and
Sayed AbdulAzeez
2
1
Department of Epidemic Diseases Research, Institute for Research and Medical Consultations (IRMC), Imam Abdulrahman Bin Faisal University, Dammam 31441, Saudi Arabia
2
Department of Genetic Research, Institute for Research and Medical Consultations (IRMC), Imam Abdulrahman Bin Faisal University, Dammam 31441, Saudi Arabia
3
Department of Clinical Pharmacy Research, Institute for Research and Medical Consultations (IRMC), Imam Abdulrahman Bin Faisal University, Dammam 31441, Saudi Arabia
*
Author to whom correspondence should be addressed.
†
Equally contributed.
Biology 2021, 10(11), 1144; https://doi.org/10.3390/biology10111144
Submission received: 12 October 2021 / Revised: 31 October 2021 / Accepted: 4 November 2021 / Published: 6 November 2021
(This article belongs to the Special Issue Microbial Diversity and Microbial Resistance)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

The incidence and developing status of multidrug-resistant bacteria and fungi, as well as their related mortality, is reviewed by a systematic published literature search from nine countries in the Arabian Peninsula. In order to analyse the emerging status and mortality, a total of 382 research articles were selected from a comprehensive screening of 1705 papers. More than 850 deaths reported since 2010 in the Arabian Peninsula due to the infection of multidrug-resistant bacteria and fungi. Multidrug-resistant bacteria Acinetobacter baumannii, Mycobacterium tuberculosis, Staphylococcus aureus, and fungi Candida auris are the most prevalent and causing high deaths. To control these infections and associated deaths in the Arabian Peninsula, continuous preventive measures, accurate methods for early diagnosis of infection, active surveillance, constant monitoring, developing vaccines, eradicating multidrug resistance modulators, and data sharing among countries are required.

Abstract

We aimed to identify the prevalence and emerging status of multidrug-resistant bacteria and fungi and their associated mortality in nine countries in the Arabian Peninsula. Original research articles and case studies regarding multidrug-resistant bacteria and fungi in the Arabian Peninsula, published during the last 10 years, were retrieved from PubMed and Scopus. A total of 382 studies were included as per the inclusion and exclusion criteria, as well as the PRISMA guidelines, from a thorough screening of 1705 articles, in order to analyse the emerging status and mortality. The emerging nature of >120 multidrug-resistant (MDR) bacteria and fungi in the Arabian Peninsula is a serious concern that requires continuous monitoring and immediate preventive measures. More than 50% (n = 453) of multidrug-resistant, microbe-associated mortality (n = 871) in the Arabian Peninsula was due to MDR Acinetobacter baumannii, Mycobacterium tuberculosis and Staphylococcus aureus infection. Overall, a 16.51% mortality was reported among MDR-infected patients in the Arabian Peninsula from the 382 articles of this registered systematic review. MDR A. baumannii (5600 isolates) prevailed in all the nine countries of the Arabian Peninsula and was one of the fastest emerging MDR bacteria with the highest mortality (n = 210). A total of 13,087 Mycobacterium tuberculosis isolates were reported in the region. Candida auris (580 strains) is the most prevalent among the MDR fungal pathogen in the Arabian Peninsula, having caused 54 mortalities. Active surveillance, constant monitoring, the development of a candidate vaccine, an early diagnosis of MDR infection, the elimination of multidrug resistance modulators and uninterrupted preventive measures with enhanced data sharing are mandatory to control MDR infection and associated diseases of the Arabian Peninsula. Accurate and rapid detection methods are needed to differentiate MDR strain from other strains of the species. This review summarises the logical relation, prevalence, emerging status and associated mortality of MDR microbes in the Arabian Peninsula.

1. Purpose and Methods

This systematic review of the emerging status of multidrug-resistant (MDR) bacteria and fungi in the Arabian Peninsula was designed to answer the following questions:
  • Is there a common MDR organism (MDRO) reported in the Arabian Peninsula?
  • Are there any MDR bacteria and fungi that have emerged in the Arabian Peninsula in the last 10 years?
  • What are the logical relationships between sets of MDR bacteria and fungi in countries of the Arabian Peninsula?
  • How many in-depth studies have been conducted on the molecular nature of drug-resistant micro-organisms prevalent in the Arabian Peninsula?
  • What are the novel antimicrobial strategies developed in the study region?
  • Is there a high mortality reported due to MDR micro-organisms in the Arabian Peninsula?
  • To what extent have nanomaterials and nanoparticles been exploited against MDR micro-organisms in the Arabian Peninsula?
This review aims to identify the prevalence and emerging status of multidrug-resistant bacteria and fungi and their associated mortality in nine countries of the Arabian Peninsula: Saudi Arabia, Bahrain, Kuwait, Oman, Qatar, the United Arab Emirates, Jordan, Iraq and Yemen. Published data from the past 10 years were retrieved from PubMed, Scopus and Google Scholar from 2 March 2021 to 8 March 2021. This review was registered with PROSPERO (CRD42021246777). The participants or populations selected from the Arabian Peninsula were Saudi Arabia, Bahrain, Kuwait, Oman, Qatar, the United Arab Emirates, Jordan, Iraq, and Yemen.
Inclusion criteria:
  • Articles reporting the multidrug-resistant bacteria in the Arabian Peninsula.
  • Articles reporting multidrug-resistant fungi in the Arabian Peninsula.
  • Research articles published since 2010 regarding multidrug-resistant micro-organisms in the Arabian Peninsula.
  • Full-text articles.
Exclusion criteria:
  • Articles discussing the use of multidrug-resistant bacteria and fungi to screen the antimicrobials in the Arabian Peninsula.
  • Articles reporting the multidrug-resistant micro-organisms from other than the Arabian Peninsula.
  • Review articles reporting the multidrug-resistant micro-organisms from the Arabian Peninsula.
Original research articles and case studies of multidrug-resistant bacteria and fungi in the Arabian Peninsula and their associated mortality were considered as articles of interest. A total of 1705 articles (published after 2010) from Scopus and PubMed were thoroughly screened for eligibility, as per the inclusion and exclusion criteria. A total of 382 studies were eligible for inclusion as per PRISMA 2009 (Figure 1; Supplementary Table S1). There were three papers reporting MDR micro-organisms from multiple countries: Article 1 [1]—Bahrain, Saudi Arabia and United Arab Emirates; Article 2 [2]—Saudi Arabia, United Arab Emirates, Oman, Qatar, Bahrain, and Kuwait and Article 3 [3]—Saudi Arabia, Kuwait, Oman and United Arab Emirates.
The most urgent public and animal health problems are increasingly caused by multidrug-resistant (MDR) micro-organisms. This problem is widely shown in bacteria that defy ultimate antibiotics and portend an untreatable future. The Arabian Peninsula has several challenges that stimulate the emergence and spread of multidrug-resistant bacteria. Dealing with these challenges requires the of multiple sectors to successfully control the spread and emergence of antimicrobial resistance. The present review summarises the logical relationship between emerging multidrug resistance organisms and associated mortality in the Arabian Peninsula.

2. Logical Relation between Sets of Multidrug-Resistant (MDR) Microbes

Eighty different species of multidrug-resistant bacteria and fungi were reported in the Arabian Peninsula (Figure 2). MDR Acinetobacter baumannii prevailed in all the nine countries of the Arabian Peninsula and was the most prevalent MDR microbe (Table 1), and was able to survive in hot dry summers and mild wet winters. After A. baumannii, Escherichia coli was the next most prevalent MDR microbe, reported in eight countries of the Arabian Peninsula; it was not reported in Yemen.
MDR Candida auris is a globally emerging fungal pathogen, for which diagnoses and treatments are challenging. The incidence of C. auris in clinical specimens from Kuwait, Saudi Arabia, and United Arab Emirates was reported in 11 articles; 580 strains (Table 1 and Table 2) responsible for 54 deaths (Figure 3, Table 3 and Table 4). A total of 13087 Mycobacterium tuberculosis isolates were reported in the region (Table 5).

2.1. Saudi Arabia

Due to its large area and population, the Kingdom of Saudi Arabia has the most significant number of scientific studies on the subject of MDR organisms among the countries of the Arabian Peninsula. Therefore, it has several obstacles that might promote the emergence and transmissiom of MDR micro-organisms. Eventually, a total of 79 unique MDR microbes were reported (Figure 2). The difficulties of this were overcome due to the successful efforts of different sectors to restrict the growth and establishment of MDR micro-organisms in the country. The active monitoring of the onset and spread of MDR micro-organisms is very important. Many relevant articles were published in research and case studies from Saudi Arabia on MDR bacteria and fungi. The inclusion criteria were applied carefully to all the search results (for articles published after 2010) from Scopus and PubMed. A total of 198 studies, as per PRISMA 2009, were eligible for inclusion (Figure 1; Supplementary Table S1). Three publications reported MDR micro-organisms in more than one country of the Arabian Peninsula: the report by Sonnevend and colleagues [1] in Bahrain, Saudi Arabia and United Arab Emirates; a study by Zowawi and colleagues [2] in Saudi Arabia, United Arab Emirates, Oman, Qatar, Bahrain, and Kuwait and a report by Sonnevend and colleagues [3] in Saudi Arabia, Kuwait, Oman and United Arab Emirates. These reports were considered separately for individual counties and also considered as only three studies in general (Figure 1). One hundred and ninety-eight studies reported various MDR organisms in Saudi Arabia, (Table 2), where there were considerably more MDR organisms compared to the other countries in the Arabian Peninsula.
Saudi Arabia had the highest number of MDR strains reported compared to other countries (Supplementary Table S2): 10972 Escherichia coli, 9829 Mycobacterium tuberculosis, 4092 Klebsiella pneumonia, 3787 Acinetobacter baumannii, 2594 Pseudomonas aeruginosa, 2014 Acinetobacter, 986 Staphylococcus aureus, 927 Klebsiella spp., 812 Enterobacter, 722 Proteus vulgaris, 715 Enterobacteriaceae, 695 Methicillin-resistant Staphylococcus aureus (MRSA) and 553 Enterococcus. Recently, the emergence of 18 Clostridioides difficile and 19 Candida auris were reported [24,317]. Between 2010 and 2021, the top five research papers reported MDR micro-organisms in Saudi Arabia. The first report included A. baumannii 59 isolates from human samples: urine, blood culture [147], respiratory specimens, skin and soft tissue specimens, blood, sterile body fluids [146,224] Biofilm-Formation in Clonally Unrelated Multidrug-Resistant Acinetobacter baumannii Isolates), wound swabs, rectal swabs, and sputum [326]. The second report included 51 E. coli isolates from human and animal samples, the isolates from human samples originated from tissue swabs [327] (the genomic diversity and antimicrobial resistance genes in multidrug-resistant CTX-M-positive isolates of Escherichia coli at a healthcare facility in Jeddah), urine, wound pus, vaginal swabs, blood culture, stools and ear swabs [87]. The isolates from animal samples originated from: chicken [60], camel [77], and minced meat samples [72]. The third report included 36 K. pneumonia isolates from human samples: blood, urine, wound swabs, sputum [40], rectal swabs and suction swabs [216]. The fourth report included 36 P. aeruginosa isolates from human samples: respiratory, urine, surgical, blood culture, genital swabs, eye swabs, ear swabs, burns [234], skin tissue, intra-abdominal fluid, bone tissue [26], wound swabs, sputum, and tracheal swabs [228]. The fifth report included 31 M. tuberculosis isolates from human samples: sputum, tissues and biopsies, abscesses, abdominal fluids, breast fluid, cerebrospinal fluid, urine, knee fluid and synovial fluid [117], wound swabs, ENT swabs, blood, tracheal swabs [130] (Supplementary Table S3).
Saudi Arabia had the highest mortality rate, with 365 patients who died due to MDR microbes (Figure 3A). The top three MDR organisms with the highest mortality rates were A. baumannii, M. tuberculosis and P. aeruginosa. Six MDR organisms were related to mortality: S. epidermidis, A. baumannii, M. tuberculosis, C. auris, P. aeruginosa and Enterobacteriaceae (Table 4). Thus, there were 365 MDR strains associated with death. M. tuberculosis caused the highest level of mortality [27]. The impact of the migrant workers from other countries cannot be understated; in 2017, a Filipino resident of Saudi Arabia was diagnosed with MDR Mycobacterium leprae. The etiologic agent was discovered using metagenomic sequencing a biopsy sample of the patient’s skin [324]. In one of the studies, 105 adult patients admitted to the intensive care unit (ICU) at Aseer Central Hospital in 2014 and 2015 were reviewed retrospectively. The species of Acinetobacter were isolated using specific phenotypes and verified by the automated system, Vitek 2. Of the 105 stains, genus Acinetobacter accounted for A. baumannii 49, A. baumannii complex 19, A. baumannii/haemolyticus 32, A. haemolyticus 4, A. lwoffii 1 [144]. There are well-established studies on electron microscopic structures, which reported both dead and alive multidrug-resistant micro-organisms in Saudi Arabia, using confocal laser scanning micrography [328].

2.2. Bahrain

The Kingdom of Bahrain had the lowest number of research articles, in contrast to the rest of the Arabian Peninsula’s countries, due to its small area and population. The papers in this review, published between 2010 and 2021 and retrieved from PubMed and Scopus, were thoroughly screened for their eligibility, as per the inclusion and exclusion criteria. Only three studies published on MDR bacteria were included in the final qualitative analysis, as per PRISMA 2009 (Figure 1; Supplementary Table S1). Two studies reported MDR micro-organisms in multiple countries: a study by Sonnevend and colleagues [1] in Bahrain, Saudi Arabia, and the United Arab Emirates; and a study by Zowawi and colleagues [2] in Saudi Arabia, United Arab Emirates, Oman, Qatar, Bahrain, and Kuwait (Figure 1). Two unique MDR microbes were reported: Acinetobacter baumannii and Escherichia coli (Figure 2). Compared to the other countries mentioned in this review, Bahrain had the lowest reported MDR strain (n = 11): eight A. baumannii and three E. coli (Supplementary Table S2). Three E. coli isolates from human specimens were obtained, including urine and tissue swabs [1], and eight A. baumannii isolates, from which human samples of blood, sputum, swab, and urine were collected [2] (Supplementary Table S3). Unlike the mortality rates of the other countries, Bahrain reported no MDR microbial infection-associated deaths (Figure 3A). In one of the scientific articles, researchers screened for the mcr-1 gene of colistin resistant Enterobacteriaceae in Bahrain; the mcr-1 strains were positive and their antibiotic resistance was determined. The mcr-1 gene was found in two E. coli isolates [1]. In the study by Thani, on a urinary tract infection (UTI) cefotaxime resistant E. coli strain, a new DNA fragment was discovered. The DNA sequence was found to be linked to the pathogenicity island III536 locus. Researchers used the Single Genome Specific Primer-PCR (SGSP-PCR) to study the genomic state of the newly identified locus, which was discovered to obtain the antibiotic resistance gene blaCTX m [110]. Bahrain was included in the research on the molecular epidemiology and resistance mechanisms of carbapenem-resistant acinophilic bacteria (CRAB) for the Arabian Peninsula countries; eight A. baumannii isolates were identified in Bahrain hospitals, and OXA-51 was found in all of the isolates. Antibiotic resistance genes were detected using PCR, and clonality was determined using repetitive sequence-based PCR (rep-PCR). The majority (84%) of the isolates in this investigation were related to health exposure. The increased awareness of multidrug-resistant organisms in the Gulf Cooperation Council (GCC) states has significant implications for improving infection control procedures, developing antimicrobial stewardship programs and highlighting the importance of regional active monitoring systems [2].

2.3. Kuwait

The studies, published between 2010 and 2021, from selected databases were evaluated for eligibility, as per the inclusion and exclusion criteria, according to PRISMA 2009. Thirty-eight papers on multidrug-resistant (MDR) micro-organisms were included in the final qualitative analysis (Figure 1; Supplementary Table S1). A total of 22 unique MDR micro-organisms were identified from Kuwait (Figure 2), including the studies that reported MDR micro-organisms in various countries (Figure 1) [2,3]. There were seven publications that reported >100 MDR strains such as: 7138 methicillin-resistant Staphylococcus aureus (MRSA), 1176 Mycobacterium tuberculosis, 561 Candida auris, 410 Acinetobacter baumannii, 302 Staphylococcus aureus, 222 Klebsiella pneumonia and 149 Enterobacteriaceae (Supplementary Table S2). Notably, five studies in Kuwait from 2010 to 2021 revealed MDR micro-organisms. The first study revealed 11 M. tuberculosis, from human samples such as, sputum, pus, tissue biopsy, lymph node and endotracheal secretion, and cerebrospinal [112] samples. The second study found eight isolates of A. baumannii acquired from human urine [198] and swab specimens, sputum, blood [2]. The third study discovered six C. auris human isolates from axilla, groin, anterior nares, vascularline exit sites, the oropharynx, respiratory and urinary tract. The isolates were also taken from environmental samples: rooms, units occupied by all the infected C. auris, colonised patients, medical devices, linen, walls, floors, furniture, doorknobs, bed railings, bedside drawers, toilet faucets, and flush handles [9]. The fourth study observed five isolates of Enterobacteriaceae obtained from blood, urine, wound, and tissue swabs [259]. Finally, the fifth study anlysed four E. coli isolates of human samples derived from blood culture, urine, wounds, and central venous pressure [10]. After Saudi Arabia, Qatar, Jordan, and Iraq, Kuwait has the fifth highest mortality rate, with a total number of 78 non-survivors associated with MDR microbial infection (Figure 3A). Seven articles reported MDR microbial infection associated with mortality. The highest mortality in Kuwait was related to the MDR organism, C. auris, with 37 non-survivor patients, whereas C. auris were the most prominent MDRO in terms of the number of deaths (Table 3).
Healthcare-related pneumonia caused by MDR pathogens poses a significant treatment challenge. The frequency of antibiotic medication leads to inefficient antimicrobial therapy. Jamal and colleagues reported unique MDR organisms: two isolates of Haemophilus influenzae, two isolates of Legionella pneumophila, and one isolate of Moraxella catarrhalis. Critically ill patients with clinically diagnosed respiratory tract infections, hospitalised at Mubarak Al Kabeer Hospital between January and April 2013, were selected for their study. Recently, a rapid-multiplex, PCR-based Unyvero pneumonia application (UPA) assay that aids in early decision making became accessible. The respiratory samples from patients with nosocomial pneumonia included the sputum, bronchoalveolar lavage fluid, and endotracheal secretions [12]. From January to December 2016, a study conducted by Hamza and colleagues revealed a novel pathogen of an MDR micro-organism. All adult patients who had the specified GI procedures, used to estimate surgical site infection (SSI) rates among gastrointestinal surgeries in all Kuwait governmental hospitals, were examined in this study. Eventually, a single isolate of Aeromonas hydrophila was obtained from small bowel (SB) surgery [329].

2.4. Oman

After removing duplications, peer reviewed articles, and non-relevant countries of interest, a total of 42 articles were screened. Thirty-three studies were excluded from further analyses and nine articles fulfilled the inclusion criteria from the published data for MDR organisms from Oman in PubMed (n = 43) and Scopus (n = 36). Seventeen different species of multi-drug-resistant organisms were reported in Oman (Figure 2). Escherichia coli was the most recorded MDRO; this organism was identified five times in the studies (Table 2). Although several MDRO were recorded in this country, the following organisms were reported as the lowest among the collected studies: Pseudomonas aeruginosa, Staphylococcus aureus, Stenotrophomonas maltophilia Citrobacter freundii, Enterobacter asburiae, Enterobacter hormaechei, and Enterobacter ludwigii, Serratia marcescens and Pantoea dispersa. The total number of MDRO strains reported in Oman were as follows: 520 Klebsiella pneumoniae, 224 Acinetobacter baumannii, 78 Escherichia coli, 35 Staphylococcus aureus, 27 Pseudomonas aeruginosa, 25 Stenotrophomonas maltophilia, 8 Enterobacter cloacae, 2 Enterococcus faecium, and 1 Citrobacter freundii, (Supplement Table S2).
In the Oman region, E. coli was the most abundant MDRO, as reported by several studies. The study by Al-Kharousi focused on the microbial features of fresh fruit and vegetables at the market stage, evaluating the impact of antibiotic-resistant enterobacteria transmission. More specifically, this study focused on one of the resistance mechanisms in Enterobacteriaceae that could produce AmpC β-lactamase in cefoxitin-resistant isolates. Fourteen isolates displayed a multi-drug resistance for different classes of enterobacteria. From these different classes, E. coli isolates gained resistance to several types of antibiotics compared to other classes; they displayed the resistance to five antibiotics such as ampicillin, chloramphenicol, kanamycin, nalidixic acid, and tetracycline. Six E. coli isolates were collected from lettuce samples that gained a resistance to multiple antibiotics. Some isolates were phenotypically positive for producing the ampC β-lactamase [257]. Another study focused on the epidemiology of multi-drug-resistant organisms via the site of infection and types of bacteria at Sultan Qaboos University Hospital. Although several MDRO were identified, E. coli was the second most abundant among the isolates. The number of isolates was 60 for E. coli with extended spectrum β-lactamases and 5 for E. coli with a carbapenem resistance, respectively, among the samples from different infection sites, such as the bloodstream, urinary tract, and surgical infection [330]. A study focused on the colistin-resistant Enterobacteriaceae in several countries of the Arabian Peninsula, more specifically, studying the presence of the mcr-1 gene in this class. Four E. coli isolates were MDROs had an mcr-1-positive strain. The E. coli strains such as ST648, ST224, ST68, and ST131 belonged to other countries; none of these strains were from Oman [1]. The focus on identifying Arabian Enterobacteriaceae in the Arabian Peninsula region revealed the presence of strains with New Delhi metallo-beta lactamase (NDM)-7. Four stains showed a multi-drug resistance to NDM-7 E. coli; only one (E. coli ST4107) strain was from Oman Hospital, isolated from a patient’s endotracheal secretion. The blaNDM7 was identified on IncX3-type plasmids. In this study, an association was found between identifying the IncX3 type plasmids and spreading the rare NDM-7 variant in the region [101]. The defined mortality data associated with MDRO was not declared in studies from the last ten years [331,332]. This could be a major limitation of the statistical mortality data from the region; further studies are needed to discover the mortality data, which can be correlated with MDRO. Although several MDROs recorded in Oman were found in other regions in the Arabian Peninsula, few organisms were only found in the Oman region: Pantoea dispersa, Bukholderia cepacian, Enterobacter Hormaechei, and Enterobacter ludwigii (Table 1). Therefore, these MDROs were considered unique to the Oman region since they were able to survive in this region; specific studies are needed to find their prevalence and associated physiology.

2.5. Qatar

The searching process for the published data of MDRO from Qatar for the last decade resulted in a similar number of research results for both PubMed and Scopus; 54 and 52 studies were found in PubMed and Scopus, respectively. After removing duplicates, peer reviewed articles, and non-relevant countries of interest, a total of 52 articles were screened. Thirty-five were excluded from further analyses. Seventeen articles were screened for full-test article eligibility by screening the title and the abstract (Supplementary Table S1). Twenty-seven different species of multidrug-resistant organisms were reported in Qatar (Figure 2). Escherichia coli was the most recorded MDRO and was identified six times (Table 2). Among the collected studies, there were several MDRO recorded in Qatar; nevertheless, the following organisms were recorded as the lowest: Mycobacterium tuberculosis, Staphylococcus aureus, Streptococcus pneumoniae, Stenotrophomonas maltophilia, Enterobacter cloacae, Salmonella typhi, Vibrio vulnificu, Campylobacter spp., Nocardia crassostreae, Staphylococcus epidermidis, Staphylococcus haemolyticus, Staphylococcus hominis, Enterococcus gallinarum, Chryseobacterium indologenes, Acinetobacter spp., Enterobacter spp., Klebsiella spp., Salmonella spp., Bacteroid spp., Coagulase negative Staphylococci, Streptococci spp., and Enterococcus spp. These organisms were reported once as MDR (Table 2). A total of five MDRO above 100 strains were reported in Qatar: 426 Acinetobacter baumannii, 223 Escherichia coli, 223 Mycobacterium tuberculosis, 178 Pseudomonas aeruginosa, and 134 Streptococcus pneumoniae. Furthermore, six MDR organisms were reported: 73 Campylobacter jejuni, 34 Staphylococcus aureus, 26 Staphylococcus epidermidis, 24 Klebsiella pneumoniae, 23 Vibrio vulnificus and 13 Nocardia crassostreae (Supplementary Table S2).
Overall, Escherichia coli was the most abundant MDRO in Qatar. From the studies in Qatar, six research articles reported Escherichia coli (Table 2), which had the highest reported MDRO in Qatar. Hasan and colleagues studied the case of a patient infected with cytomegalovirus-associated, hemophagocytic lymphohistiocytosis that gained antimicrobial resistance. The patient colonised the multidrug-resistant MDR to Enterococcus faecium, Escherichia coli, and Klebsiella pneumoniae. As a result of the severe multidrug resistance, several infections such as respiratory, urine, and bloodstream infections, developed, causing a threat associated with the HLH patients and obtained MDR organisms. The study reported E. coli type ST410, which was isolated from blood. No specific strain numbers were declared for E. coli in this study. Using a whole-genome sequence, there were different sequence types between the vancomycin-resistant Enterococcus isolates from the urine and blood cultures of patients and the previously colonised patients. These authors found that the resistance mechanisms were acquired in the colonizing strains [333].
In another study, the bacterial infection and resistance patterns of pediatric oncology patients after chemotherapy treatment were analysed for MDRO in the bloodstream; 116 strains of Gram-positive and Gram-negative bacteria were isolated. E. coli was the third most common Gram-negative isolate with seven MDR isolates. Two patients died due to the infection of MDRO Stenotrophomonas maltophilia and E. coli. Unfortunately, no specific strain numbers and names were provided, hence they do not appear in the mortality table (Table 3) [55]. The study by Garcell et al. [78] focused on studying the etiology of surgical site infection in a community hospital in Qatar for a period of three years. Samples were collected and patients with contaminated wounds had the highest number of isolates. Most of the isolates in the surgical site were E. coli and Klebsiella spp.; 12 E. coli beta-lactamase (ESBL) isolates were collected from the infection in the surgical site [78]. The epidemiology of bacteremia at Hamad General Hospital isolated 167 g-positive, and 285 g-negative bacteria over a period of one year. The samples were collected from patients’ blood. Several MDRO were found; nevertheless, E. coli was the most common bloodstream isolate; 97 E. coli were isolated. The intravenous catheterisation blood stream infection was found to be the most common source of bacteraemia. In comparison with the other types of etiologic bacteria, the MDR E. coli ESBL caused the highest number of deaths, and accounted for 14 out of 102 mortalities [7]. Regarding the antibiotic resistance of E. coli in Qatar from food-producing animals, 90 E. coli isolates were reported from poultry farms and tested with several antibiotics. Uncooked food or unsanitary hygiene practices can accelerate the transmission of MDR to humans [75]. Having a statistical mortality on MDR microbial infection in the Arabian Peninsula is important for identifying the mortality caused by the MDRO. Qatar had the second highest number (n = 187) of mortalities compared to the other countries in the Arabian Peninsula, (Figure 3A). In Qatar, four studies reported information on mortalities. Several MDR organisms were recorded as the cause of a patient’s death. Acinetobacter baumannii was recorded as a pathogen associated with mortality in several studies (Table 3). The study by Al Samawi et al. recorded the higest number of deaths caused by Acinetobacter baumannii. The total number of non-survivors was 65 out of 239 patients, and 372 strains were isolated from adult patients samples. The respiratory tract was the most prominant site of A. baumannii infection [6]. (Table 3). Another study reported the same organism and its association with the deaths of 15 patients out of 48. A total of 48 MDR A. baumannii strains were isolated from the patients [4] (Table 3). Another study reported 102 deaths due to the MDR organisms, of which 34 were females. Multiple MDR pathogens caused the death of patients; nevertheless, ESBL and MSSA had the highest-recorded mortality [7] (Table 3). Although several MDRO recorded in Qatar were found in other parts of the Arabian Peninsula, Campylobacter spp., Nacardia crassostreae, Chryseobacteriu indologenes, Acinetobacter spp., Bacteroid spp., coagulase negative staphylococci, and Enterococcus spp. were considered unique to Qatar.

2.6. United Arab Emirates

The search terms related to multidrug resistance resulted in 71 studies from PubMed and 38 studies from Scopus. After removing duplicates, peer reviewed articles, and non-relevant countries of interest, a total of 70 articles were screened. Fifty-one studies were excluded from further analyses and 19 articles were screened for eligibility as full-text articles by screening the abstract. Four full-text articles were eliminated because patients were not from the country of interest. A total of fifteen full-text articles were included in this study (Supplementary Table S1).
Twelve different species of multidrug-resistant organisms were reported in the UAE (Figure 2). Escherichia coli was the most abundant MDRO in the UAE and was reported in six studies (Table 2). Although several MDRO were recorded in this country, the following organisms were reported as the lowest among the collected studies: Pseudomonas aeruginosa, Enterobacter cloacae, Candida auris, Citrobacter freundii, Staphylococcus epidermidis, and Salmonella typhi (Table 2). The total strain numbers of MDROs reported in the UAE were: 1116 Mycobacterium tuberculosis, 73 Enterobacteriaceae, 61 Escherichia coli, 55 Klebsiella pneumoniae, 31 Pseudomonas aeruginosa, 16 Acinetobacter baumannii, 6 methicillin-resistant Staphylococcus aureus, and 1 Stenotrophomonas maltophilia (Supplementary Table S2).
E. coli was the most abundant MDRO in UAE, and the highest reported by several articles. The study by Sonnevend et al. focused on the presence of the mcr-1 gene in colistin resistance to E. coli from several countries in the Arabian Peninsula. Four E. coli strains were isolated in this study; only one strain was from UAE, named ABC149 with the sequence type ST131. This sample was isolated from patients’ blood samples. In the Arabian Peninsula, several multi-resistance isolates contained the mcr-1 gene, which could increase mcr-1-carrying strains in these regions [1]. The impacts of ceftolozane–tazobactam and ceftazidime-avibactam against multidrug-resistant isolates such as Escherichia coli, Klebsiella pneumoniae, and Pseudomonas aeruginosa were studied, and included 60 CRE E. coli from different patient samples such as sputum, blood, urine, tissue, and body fluid samples. The study suggested that ceftolozane–tazobactam and ceftazidime–avibactam could treat most of the infections caused by MDROs [45]. Another study focused on the pattern of uropathogenic resistance to antibiotic prophylaxis in patients infected in the urinary tract. E. coli was the most grown organism with prophylaxis. The number of E. coli isolates was 26, and the majority of them were isolated from urine [97]. The activity of hymenochirin-1B against multidrug-resistant bacteria and immunomodulatory properties were studied [182] such as the E. coli strains, ABC 54 and ABC 85, collected from urine and tracheal aspirate. The study revealed a potential drug development, combined with hymenochirin-1B, against several Gram-positive and Gram-negative bacteria, with low cytotoxicity in humans. The characteristics of E. coli in several counties in the peninsula region revealed the presence of the New Delhi Metallo-beta-lactamase (NDM)-7, four stains showed a multi-drug resistance of NDM-7 E. coli, including two strains (ABC133 and ABC218) from the UAE region of patient’s sputum and wound secretion samples. The blaNDM7 was identified on IncX3 type plasmids and an association was found between IncX3 type plasmids and the transmission of the rare NDM-7 variant in the Middle East [101]. Mortality data were not declared in the studies; which is one of the limitations of such data. Further studies are needed to find the mortality data, which can be correlated with the MDRO. All twelve of the different species of multidrug-resistant organisms reported in the UAE were also reported in other countries in the Arabian Peninsula (Table 1). These organisms were able to survive in other parts of the Arabian Peninsula with hot dry summers and mild wet winters.

2.7. Jordan

The screening of multidrug-resistant micro-organisms from Jordan through the databases PubMed, Scopus, and Google Scholar revealed 136, 92 and 22,400 published articles related to multidrug resistance, respectively. After filtering out review papers and limiting the search results timeline to 2010–2021, thirty-seven articles were screened and six papers were excluded, since their samples were reported from ATCC standard cultures rather than human samples, resulting in a total of 31 full-text articles for final consideration. Jordan reported 11 distinct, multidrug-resistant bacterial species; Escherichia coli was the dominant species with 886 isolates in total, and Acinetobacter had the lowest number of strains reported, with 19 [33]. Out of all countries in the Arabian Peninsula, Jordan is the only country that reported Propionibacterium acnes as a unique multidrug-resistant bacterium. Research articles reported a variety of strains that were isolated from humans, hospital environments, or other sources where meat products and green vegetables could be present [334]. Some articles reported a large number of bacterial strains isolated from the aforementioned sources. For instance: 269 E. coli strains were isolated from broiler chickens [85], another study reported 287 Salmonella enterica isolates from beef cattle [100], while 544 Streptococcus pneumoniae isolates were obtained from humans [268].
E. coli were the dominant MDR bacteria in 11 research studies. One study isolated 142 E. coli ST131 strains from infants’ faecal samples, of which the majority were ESBL producers. The antimicrobial susceptibility of these strains was tested using the disc diffusion technique [64]. Similarly, Haddadin et al. found 19 and 25 MDR E. coli strains from 70 strains isolated from green vegetables and 68 isolated from infants’ faeces, respectively, after testing them for antibiotic susceptibility. In addition, they found a genetic similarity between the strains isolated from plants and infants, implying the possibility of the circulation of these pathogens between both sources [80]. O1, O2, O25, and O78 avian E. coli serotypes were characterised in a study after their isolation from broiler chickens, in order to study their antimicrobial resistance and the associated risk factors [85]. Another study investigated the cause of urinary tract infections among patients in Jordan. They isolated 262 E. coli strains from urine samples, of which 150 were MDR with a high association with the ST131 clone [96]. In addition, for the purpose of studying the colonisation of E. coli in the intestines, 288 stool samples were collected from infants. From these isolates, 52 were MDR and ESBL producers [104].
It was crucial to include mortality data in this review to observe the number of deaths caused solely by MDR micro-organisms and the root cause of their ability to cause a high mortality in the Arabian Peninsula (Table 4). Regarding mortality data collected from Jordan, several bacterial species contributed to these numbers. Specifically, Almomani et al. reported the deaths of 50 patients (24 males and 26 females) out of 119 patients suffering from pneumoniae caused by using ventilators infected with Acinetobacter baumannii in ICUs. This article reported the highest number of mortalities in Jordan [34] (Table 4). MDR Acinetobacter sepsis cases in neonates were also studied to determine the effect of Colistin; this organism caused two deaths out of twenty-one neonates, averaging 0.6 years of age [33]. Furthermore, there were 457 wound infection cases at a Jordanian hospital that included 395 males and 62 females with a median age of 27 years. These infections were caused by several MDR micro-organisms, including Staphylococcus aureus, E. coli, Klebsiella pneumoniae, Pseudomonas, Enterobacter, Acinetobacter, and Proteus and 37 deaths were reported [32].

2.8. Iraq

The number of final research articles from Iraq (n = 75) was generally higher than those reported from other countries in the Arabian Peninsula, with the exception of Saudi Arabia (n = 198), in PubMed and Scopus, and Google Scholar (Supplementary Table S1) for the keywords “multidrug-resistant”, and “multidrug resistance”. After excluding irrelevant articles, review articles, and limiting the timeline to 2010–2021, 75 research articles were eventually obtained for further analysis. A. baumannii was the dominant species in Iraq, followed by E. coli, with 10 research reports among the 28 different bacterial species reported, including four Staphylococcus species and three Klebsiella species. However, the largest number of strains were from Providencia spp.; 1213 isolates were reported from only two studies [49,261]. Several varieties of bacterial strains were reported from Iraq; these included 1063 S. aureus isolated from humans [15], 142 E. coli isolated from chickens [37], and 1209 Providencia spp. from various sources such as humans, soil, chickens, and wastewater [49]. Iraq is the only country in the Arabian Peninsula that reported the multidrug-resistant Vibrio cholerae, making it unique to this region [316].
A total of 12 research articles reported A. baumannii MDR strains. Metallo ג-lactamases producing A. baumannii caused a nosocomial infection in clinical samples from patients’ sputum, blood, urine, and burn wound swabs, in addition to samples from the environment; 124 strains were acquired from Baghdad hospitals to study their multidrug resistance [189]. A study conducted by Muslim et al. to determine the lectin-producing ability among 51 A. baumannii isolates from a hospital environment and patient samples of the sputum, blood, wounds and urine, revealed 17 lectin producers [183]. In addition, a study isolated 96 A. baumannii from clinical samples of wound and burn infections tested against 16 antimicrobial drugs using the disc diffusion technique, and 84 were found to be MDR [174]. Another article reported carbapenem resistance in 44 A. baumannii isolates from 182 patients who suffered wound infections, samples included swabs from joints, bones, and connective tissues [162]. In addition, the virulence factors of 30 A. baumannii strains from patients with blood infections were determined, implying their ability to cause persistent infections due to harboring plcN and lasB genes [177]. Even though, in general, there were many reports from Iraq, only one article reported mortality data compared to the other countries in the Arabian Peninsula. In 2012, Babakir-Mina et al. reported that, out of 654 burn patients, 98 died due to infections caused by S. aureus, while 556 survived (Table 3). These burn patients were mainly females (381) with a median age of 18 years. The nosocomial infection-causing agent was the methicillin-resistant S. aureus (MRSA), with a total of 1063 isolates from the burn swabs [15]. This study alone does not reflect the total mortality caused by MDR micro-organisms in Iraq. More research must be conducted in order to determine the dominant micro-organisms and the root cause of mortality from such organisms.

2.9. Yemen

Yemen had much fewer search results in PubMed, Scopus, and Google Scholar when the keywords, “multidrug-resistant”, and “multidrug resistance” were used. For instance, there were 19 results from PubMed, 38 from Scopus, and 2269 from Google Scholar; articles from Google Scholar were not included. Many search results showed articles reporting parasitic infections in some regions in Yemen and their multidrug resistances, but these were also not included, in addition to irrelevant and older articles published before 2010. Eventually, only six articles were included from the databases PubMed and Scopus for a final analysis. Yemen reported only four distinct bacterial species dominated by Mycobacterium tuberculosis, with 240 strains from four research articles. The remaining three articles reported A. baumannii, Pseudomonas aeruginosa, and S. aureus. All the bacterial isolates in these articles were from human sources, including 120 strains of M. tuberculosis [115], 60 of S. aureus [270], and 65 of P. aeruginosa [237]. As mentioned, the number of reports from Yemen were generally fewer compared to the other countries studied; three research articles mentioned the isolation of M. tuberculosis from patients residing in tuberculosis (TB) centers in Yemen. For instance, MDR M. tuberculosis were isolated from 115 patients’ sputum samples to evaluate the associated risk factors [17]. In a similar study was conducted by the same author, in which MDR M. tuberculosis involving 135 patients was explored to evaluate health-related risk factors [16]. Furthermore, sputum samples were collected from 170 patients in the National TB Institute of Sana’a and 118 M. tuberculosis isolates were identified [115]. Two articles, both written by Jaber et al., reported mortality data in Yemen [16,17]. The first study reported 14 deaths out of 115 tuberculosis patients (65 males and 50 females), with a median age of 45 years, while being treated in TB centers. All of the isolated M. tuberculosis were resistant to at least two drugs. The other study also reported the isolation of M. tuberculosis from sputum samples. This micro-organism caused 14 deaths out of 80 patients (48 males and 32 females) who were also in TB centers [16]. Mortality data were limited to patients treated in TB centers, extensively focusing on MDR M. tuberculosis per se. More extensive mortality studies must be conducted to investigate the prominent MDR micro-organisms causing substantial death cases in the Arabian Peninsula in general, particularly in Yemen.

3. Methods Used to Detect Multidrug-Resistant Organisms

Various detection methods are used to identify MDR organisms: the disc diffusion method [300,330], Kirby and Bauer method [335], microdilution process [161], PCR with specific primers [336], real-time PCR tests with temperature melting analysis [49], MDR-TB detection [125], E-test for antimicrobial resistance [4,148], automated identification and susceptibility system [330], Growth Indicator Tube system [337] automated Phoenix method [221], matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF MS) [4], GeneXpert assay [338], AcrAB–TolC efflux pump system [36], multiplex PCR for confirming isolates [300,317], multilocus sequence typing [300], sequences of 18S rRNA gene and ITS region for MDR fungi [24], 16S rRNA gene sequencing [317], toxin genes multiplex PCR [317], multiplex real-time quantitative PCR [339], DNA Microarray Detection [84] and whole-genome sequencing [21].
The resistance of antibiotics was established for the A. baumannii isolates 506, 510 and 936 isolated in 2006, 2009 and 2012, respectively. In 2012, 12 unique XDRAB strains were extracted from critical patients with ventilator-associated pneumonia (VAP) using the microdilution process [161]. Minimum Inhibitory Concentration (MICs) were indicated by E-test. A CHROMagar Acinetobacter medium was used to diagnose susceptible and multi-drug-resistant A. baumannii (MDRAB) strain. The updated Hodge test (MHT) and multiplex PCR were used to examine carbapenemase-resistant A. baumannii. The E-test process was used to carry out a synergy test. A recent 3-year evaluation study determined a reduction in the antibiotic resistance in Gram-negative bacteria by the Saudi National Action Plan using commercially available identification cards (VITEK 2 ID-GNB cards) and MDR detection (AST-No. 12 cards) [340]. They found that the rates of antibiotic resistance, extended-spectrum beta-lactamase, and multidrug resistance were reduced over time, indicating that the Saudi National Action Plan was effective. Yassin et al., [299] reported the advent of Candida species resistance and suggested an antifungal sensitivity procedure performed prior to deciding on a treatment regimen. Updated techniques such as sequencing the 18S rRNA gene and ITS region in MDR fungi, 16S rRNA gene sequencing in bacteria, and toxin genes multiplex PCR were also adopted by laboratories in Saudi [24,317]. Whole-genome-sequencing-based MDR identifications were also reported [21]. Improved tools are needed for the diagnosis of MDRO [341,342].
Candida auris is an emerging fungal pathogen with multidrug resistance, causing nosocomial infections and invasive deaths [336]. A trustworthy diagnostic approach, such as using the 18S rRNA gene and ITS region against MDR fungi, is urgently needed [24]. C. auris is often mistaken for numerous other yeast species by phenotypic identification platforms [336]. In this work, PCR and real-time PCR tests were used for identifying C. auris and related species: Candida duobushaemulonii, Candida haemulonii and Candida lusitaniae. Targeted rDNA nucleotide region sequences, C. auris-specific, primers-based PCR or real-time PCR experiments followed by electrophoresis or temperature melting analysis, respectively, were performed using a panel of 140 clinical fungus isolates [336]. The findings of the tests completely corroborated the findings of the DNA sequencing. These genetic techniques address the current phenotypical shortcomings in the identification of C. auris and its associated species. The present MDR-TB outbreak is the result of decades of neglecting significant infectious diseases, a lack of national prevention program services, slow case identification, and inadequate treatment in high-burden countries [113]. The clinical results were vastly enhanced by optimizing care regimes along with the quick detection of DST in first- and second-line medications. The prognosis of MDR-TB was further strengthened by the recent advancements in MDR-TB detection and an intensive empirical management of patients with multiple medications during the initial period of treatment. However, laboratory funding, which is essential for the effective diagnosis of patients with MDR-TB, was largely insufficient. The rapid and cost-effective cultivation of DST systems of M. tuberculosis strains must be strengthened.
A pilot study from Hamad Medical Corporation (HMC), supported carbapenem resistance in randomly selected clinical isolates of multidrug-resistant Acinetobacter baumannii [4]. The research results were used to analyse carbapenemasal in all of the isolated MDR A. baumannii through molecular techniques. Matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry verified the identification of MDR isolates, which was verified and validated by E-test antibiotic tolerance. Real-time PCR was used to explore the molecular nature of carbapenemases (blaOXA-23, blaOXA-24, blaOXA-58, blaNDM). The phylogenetic study on the partial sequence of CsuE and blaOXA-51 genes confirmed the epidemiological relationship between the isolates. The 48 isolates were resistant to most antibiotics, including meropenem, imipenems, ciprofloxacin, levofloxacin, amicacin, gentamicin, and most β-lactam; yet they were susceptible to colistin. The MDR A. baumannii production of OXA-23 carbapenemase in Qatar was described in detail by Rolain [4]. The effect of a 1 and 2 h exposure to low-frequency magnetic fields (0.3 and 0.42 mT) on Pseudomonas aeruginosa resulted in a reduced resistance and increased drug susceptibility [225]. This increase was often linked to the temperature of the environment and the duration of the exposure. Antibiotic resistance in Iraq was conferred on Escherichia coli by the AcrAB–TolC efflux pump system [36], which contributed to poor patient results.
Another study examined 177 chicken samples using the ISO 10272-2006 procedure to isolate Campylobacter spp. A multiplex PCR was used for the confirmation and labelling of the isolates [300]. The disc diffusion method was used to assess the isolates’ antimicrobial resistance, and multilocus sequence typing was used to genotype the isolates. There were three distinct sequence types in ten C. coli isolates, but seven different sequence types in ten C. jejuni isolates. Many of the isolates tested were resistant to ciprofloxacin but not to imipenem, and they were multidrug-resistant to five or more antimicrobials. A retrospective analysis of MDRO data from January to December 2012 used the disc diffusion method to verify antibiotic susceptibility analysis, and an automated identification and susceptibility system was used to recognise and analyse species [330]. Increasing patterns in the prevalence rates of MDRO patients and MDRO isolates were discovered during the study [330]. The study by Al Shamahy et al. examined septic-resistant organisms in the neonatal unit at Al-Thawra Hospital, Sana’a, Yemen and offered an empirical treatment approach [335]. One hundred and fifty-eight neonates, aged 0 to 28 days, were recruited in the study. Blood samples were collected from each neonate, then the samples were cultivated, and, subsequently, antimicrobial susceptibility testing was performed using the Kirby and Bauer method [335].

4. Antimicrobial Resistance Profiles Used for Treating Multidrug-Resistant Organisms

Combining low-frequency magnetic fields with a wide range of antibiotics helped to reduce P. aeruginosa tolerance [225]. The physical parameters of LF-MF, such as strength and exposure duration, influenced the reduction in bacterial resistance and provided a potentially noninvasive and fast treatment option for burn victims [225]. Peptide B1 had a broad-spectrum behaviour against the strains examined in the study by Tell et al. [343]. The concentrations used to destroy microbial cells ranged from 10 to 20 M. B1 had a lower toxicity against mammalian cells and a lower probability of causing hemolysis [343]. Domperidone is an important ArcB inhibitor, a well-known and secure over-the-counter antiemetic [36]. Domperidone reversed the antibiotic tolerance of levofloxacin and ciprofloxacin in MDR E. coli stains and was more effective than the recognised efflux pomp-inhibitor reserpine. It was also able to improve every impact on the sensitive strains of antibiotics. This finding suggests that a combination of antibiotics and domperidone may be utilised to handle multi-drug-resistant E. coli bacteria in the clinic [36]. Multidrug-resistant pneumonia in the health sector offers an important treatment challenge [12]. A Unyvero Pneumonia Application (UPA) quick PCR multiplex test helps to make prompt decisions. UPA was assessed for its successful detection in nosocomial pneumonia of the etiologic pathogen and for resistance indicators. This test also investigated the impact on acute nosocomial pneumonia. The appropriate specimens were treated by UPA according to the manufacturer’s methods, along with conventional cultivation techniques. The results indicated that a multiplex PCR-based test was capable of reliably diagnosing the etiological agents of NP and MDR, as well as resistance indicators. This could allow doctors to make early antibiotic modifications [12]. The analysis of E. faecalis genomes was performed by means of multilocus sequence typing. ST179 and ST16 were the most common STs in clonal complex 16 in Saudi patients (CC16). MDR isolates were approximately 96% (n = 149). There was nearly no coverage of the antibiotics quinupristin/dalfopristine, clindamycin, and erythromycin, but there were elevated levels of streptomycin, gentamycin and ciprophloxacin, which were observed to be under-optimal. Low vancomycin, linezolid and ampicillin resistance were found and suggested for treating E. faecalis infection [292]. Alqasim [57] discovered the frequency of β-lactamases produced by E. coli. They analysed the transportation of these isolates by suspicious antibiotic patterns at phenotypic and genotypic levels. A total of 100 E. coli urine isolates were collected at a tertiary health facility in Riyadh from January 2018 to March 2018. All antimicrobial isolates were tested for susceptibility. The synthesis of ESBL was separated in phenotypic and genotypic phases by double disc synergy testing and a polymerase chain response. A variety of ESBL variations were identified using DNA sequencing. Of the 100 E. coli isolates, 67 were associated with the phenotype of MDR. All isolates were tolerant to all the antibiotics that were used, which were all vulnerable to imipenemia. There were 33 phenotypic and genotypical isolates of ESBLs the in 100 isolates of E. coli. For all ESBL-positive E. coli isolates, CTX m was an ESBL (31/33 isolates; 93.94 percent). In all CTX m carriage isolates, the CTX-M-15 variant was included. The multiple ESBL carriage of 15–33 isolates (45.45%) was detected, with 11 (33.30%) ESBL isolates, compared to four isolates (12.12%) with three ESBLs. A vast range of forefront antibiotics were found by our study, which were frequently utilised for the treatment of UTI patients with a high antimicrobial toleration of E. coli that generated ESBL. Among the E. coli urinary isolates, the most common CTX m variants also had a high incidence of ESBL channels. This is a serious concern and needs to be investigated further to find better treatment options.
M. morganii isolates were highly resistant to many antibacterial agents and classified as MDR bacteria from Bahrain [315], all of which had ESBL. The antibiotics, meropenem and imipenem, were very effective against the M morganii isolates. In Jordan, 31 percent of S. aureus were multidrug-resistant (MDR) among the S. aureus isolates from wound samples [247]; however, they were vulnerable to chloramphenicol, linezolid, nitrofurantoin, rifampicin, and teicoplanin (>80%). In Qatar, a pulsed-field gel electrophoresis analysis of P. aeruginosa isolates from cystic fibrosis patients indicated a strong degree of resemblance, indicating a unique adaptation of these clones to cystic fibrosis-affected lungs. The non-cystic fibrosis, hospitalised cluster had a distinct clonal root with localised clustering and potential hospital-acquired P. aeruginosa infections [221]. A. baumannii isolates from Al-Thawra University hospital in Yemen were immune to almost all antibiotics examined, with a high minimum inhibitory concentrations of imipenem, amikacin, and ciprofloxacin [168]. All three A. baumannii strains were positive for the modified Hodge test, and no inhibition was observed on the activity of β-lactamases. The naturally occurring blaOXA-51-like gene, and the carbapenemase-encoding blaOXA-23-like gene, were observed in all three isolates and detected with 16S rRNA methylase armA gene. A search for aminuglycoside enzymes (AMEs)-producing genes identified the presence of acetyltransferase aac (6-Ib) in one A. baumannii isolate. Fluoroquinolone resistance-associated GyrA genes with one Ser83Leu variation were observed in all of the isolates. A multilocus sequence typing demonstrated that all the isolates were sequence type 2 [168]. A case study in pediatric patients from Saudi Arabia with combined immunodeficiency syndrome, reported treating pneumonia caused by multidrug-resistant P. aeruginosa using ceftolozane/tazobactam, which was recommended only for adult patients (>18 years) [241]. Peptide (AamAP1-Lysine) antibiotic (chloramphenicol, levofloxacin, rifampicin, ampicillin and erythromycin) combinations proved a strong synergistic activity, causing a 64-fold reduction in multidrug-resistant bacteria [344]. Colistin was effective and safe for treating MDR Acinetobacter neonatal sepsis in neonatal units in Amman, Jordan [33].

5. Mining Natural and Novel Antimicrobials against MDR

The antibacterial activities against the most common multidrug resistance micro-organisms associated with skin infections, were assayed using aqueous and ethanol extracts from five native medicinal plants, most of which showed an antibacterial and antifungal activity, with the highest activity found in the aqueous extract of Arum discoridis [345]. The experiments that characterised and measured the effect of honey on P. aeruginosa quorum sensing networks revealed that low concentrations of honey decreased the expression of exotoxin A (ETA), las and rhl glucons, as well as the corresponding virulence factors through the interruption of the quorum sensing system [346,347]. Edible plants (Gundelie tournefortii L. and Pimpinella anisum L.) and the propolis of Apis mellifera [348] were also considered as options for inhibiting the growth of MDR in combination with antibiotics [69]. Lavender essential oil used against carbapenemase-producing K. pneumonia [349], extracts of Lawsania inermiss, Portulaca oleracea used against Candida albicans [350], and Trachyspermum ammi extracts mediated the green production of metal-nanoparticles against MDR Listeria monocytogenes and Serratia marcescens [351] and were reported as suitable for the identification of novel antimicrobial agents against selective MDROs.
Ultrashort antimicrobial peptides (novel pentapeptide, UP-5) had a strong to moderate efficacy against MDRO, with a low toxicity when used in conjunction with traditional antimicrobials [352]. Alyteserin-2a, a cationic α-helical peptide recovered from the skin secretions of Alytes obstetricans, showed an efficient activity against multidrug-resistant Acinetobacter baumannii and Stenothrophomonas maltophilia [172]. Cuminaldehyde, a key antibacterial ingredient of Calligonum comosum essential oil, was reported to have an antibacterial activity against MDROs in a study from the United Arab Emirates [353]. Actinomycetes, specifically Streptomyces, Nocardiopsis sp., and MK MSt033 were discovered to have an antimicrobial activity against a variety of MDROs [354]. Many peptides were tested against MDR Acinetobacter baumannii [355,356,357]. Terminalia chebula, Terminalia bellirica, and Phyllanthus emblica plants, traditionally used for treating microbial infections were tested against MDR bacteria and fungi [358].
Buffalo milk lactoperoxidase against S. enterica and L. monocytogenes [359]; colistin against MDR Acinetobacter [33]; lactic acid bacteria from raw camel milk [360]; peptides, including hybrid peptides and ultrashort peptides [343,344,352]; ultrashort antimicrobial peptide nanoparticles [356]; Isatin-benzoazine molecular hybrids [361]; chemical derivatives [362,363,364,365]; extracts of Matricaria aurea [366]; extracts of Nepeta deflersiana [223]; Saudi scorpion venoms [367]; artemisinin extract [368]; biocidal polymers [369]; microtubule depolymerizing agents [370]; ozonated water [250]; and marine Streptomyces sp [371] against MDRO were all tested in the study region. Nanomaterials, nanoparticles and nanoformulations [351,356,358,372,373], as well as silver nanomaterials derived from marine Streptomyces [374] were also tested against the growth of multidrug-resistant micro-organisms. Further studies are needed to understand the molecular mechanisms and future possibilities of identifying pharmaceutically active compounds with potential medicinal applications.

6. Conclusions and Future Perspectives

The active surveillance and constant preventive efforts to control MDR infections and associated diseases can improve healthcare facilities and the socio-economic status of patients [375]. Specifically, MDR E. coli is predominantly associated with urinary tract infections in pregnancy [54,61,102]. The emergence of multi drug-resistant Candida albicans is prevalent among pregnant and non-pregnant women with vaginitis [299]. Listeria monocytogenes from patients with spontaneous abortions [310] and multidrug-resistant clinical Enterococcus faecalis from pregnant women [292] highlight the need for more precautions and constant monitoring, with the appropriate identification of MDR and susceptibility tests prior to medication. The development of a candidate vaccine and the early diagnosis of MDR infection shall be a better option for protection against MDR infection. The most prevalent multidrug-resistant Escherichia coli, Mycobacterium tuberculosis, Acinetobacter baumannii, Klebsiella pneumoniae, Pseudomonas aeruginosa, Staphylococcus aureus, Acinetobacter, Enterobacteriaceae, Providencia spp., Streptococcus pneumoniae, methicillin-resistant Staphylococcus aureus (MRSA), Klebsiella spp., Enterobacter, Proteus vulgaris, Candida auris and Enterococcus in the Arabian Peninsula must be diagnosed accurately and rapidly using advanced molecular techniques by developing region-specific diagnostic tools. The control of infections by using specificity detecting systems is an important protection method against MDRO. One study develops a direct detecting system for Candida auris by using a novel multiplex real-time quantitative PCR that has a high degree of specificity in detecting different species-level of Candida [339]. However, in healthcare settings, more detection methods are needed to detect MDRO strains within the species in clinical samples; allowing a reduction in the evolving MDRO pathogenic species. The Arabian Peninsula is rich in religious traditions. Notably, every year, more than 10,000,000 pilgrims visit Saudi Arabia to perform the Umrah and Hajj. Multidrug-resistant Streptococcus pneumoniae [376], Acinetobacter baumannii, Escherichia coli [377], Salmonella enterica [308], and Mycobacterium tuberculosis [378] is observed among the pilgrims; however, it is relatively very low compared to the total number of pilgrims, which indicates the successful surveillance and management of these micro-organisms. International guidelines and recommendations can be implemented for the management and complete prevention of MDRO, such as guidelines for MDRO regarding mass gathering events. Networking MDRO research strategies are mandatory among the countries of the Arabian Peninsula to fight against the risk of MDRO infection and death. This research can enhance the sharing of information, overcome the limited data availability, and identify molecular and physiological mechanisms behind multidrug resistance. MDR co-infection with SARS-CoV-2 among COVID-19 patients shall also be considered to reduce the disease burden [379,380]. This review uncovered the huge requirement for developing novel, safe, and sustainable antimicrobials from natural and other resources to fight against MDRO. Food process parameters and the overuse of antimicrobials require active surveillance to reduce resistance modulators. The present cumulative observations will be informative for effective planning, designing preventive strategies, and prioritizing research goals to achieve MDRO-free zones.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/biology10111144/s1, Table S1: Country wise data for the number of articles from various database, Supplementary Table S2: Number of multi drug resistant strains reported from countries of Arabian Peninsula, Supplementary Table S3: Source of isolates and Number of MDR microbial strains reported from Arabian Peninsula.

Author Contributions

J.F.B., A.S.R., B.S., G.A., N.B.A. and S.A. conceived and designed the research; A.S.R., B.S. and G.A. performed the literature search and screening; J.F.B., N.B.A. and S.A. validated the final articles; J.F.B., A.S.R., B.S. and G.A. analysed and wrote the paper with the contributions of N.B.A. and S.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are available upon reasonable request from the corresponding author.

Acknowledgments

The authors thank the Dean, Institute for Research and Medical Consultations (IRMC), Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia for her continuous support and encouragement. We thank The Deanship of Library Affairs from the Imam Abdulrahman Bin Faisal University for their support.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Sonnevend, Á.; Ghazawi, A.; Alqahtani, M.; Shibl, A.; Jamal, W.; Hashmey, R.; Pal, T. Plasmid-Mediated Colistin Resistance in Escherichia coli from the Arabian Peninsula. Int. J. Infect. Dis. 2016, 50, 85–90. [Google Scholar] [CrossRef] [Green Version]
  2. Zowawi, H.M.; Sartor, A.L.; Sidjabat, H.E.; Balkhy, H.H.; Walsh, T.R.; Al Johani, S.M.; AlJindan, R.Y.; Alfaresi, M.; Ibrahim, E.; Al-Jardani, A.; et al. Molecular Epidemiology of Carbapenem-Resistant Acinetobacter Baumannii Isolates in the Gulf Cooperation Council States: Dominance of OXA-23-Type Producers. J. Clin. Microbiol. 2015, 53, 896–903. [Google Scholar] [CrossRef] [Green Version]
  3. Sonnevend, Á.; Ghazawi, A.A.; Hashmey, R.; Jamal, W.; Rotimi, V.O.; Shibl, A.M.; Al-Jardani, A.; Al-Abri, S.S.; Tariq, W.U.Z.; Weber, S.; et al. Characterization of Carbapenem-Resistant Enterobacteriaceae with High Rate of Autochthonous Transmission in the Arabian Peninsula. PLoS ONE 2015, 10, e0131372. [Google Scholar] [CrossRef]
  4. Rolain, J.-M.; Loucif, L.; Al-Maslamani, M.; Elmagboul, E.; Al-Ansari, N.; Taj-Aldeen, S.; Shaukat, A.; Ahmedullah, H.; Hamed, M. Emergence of Multidrug-Resistant Acinetobacter Baumannii Producing OXA-23 Carbapenemase in Qatar. New Microbes New Infect. 2016, 11, 47–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Khan, F.Y.; Abukhattab, M.; AbuKamar, M.; Anand, D. Adult K Lebsiella Pneumoniae Meningitis in Qatar: Clinical Pattern of Ten Cases. Asian Pac. J. Trop. Biomed. 2014, 4, 669–672. [Google Scholar] [CrossRef] [Green Version]
  6. Al Samawi, M.S.; Khan, F.Y.; Eldeeb, Y.; Almaslamani, M.; Alkhal, A.; Alsoub, H.; Ghadban, W.; Howady, F.; Hashim, S. Acinetobacter Infections among Adult Patients in Qatar: A 2-Year Hospital-Based Study. Can. J. Infect. Dis. Med. Microbiol. 2016, 2016, 6873689. [Google Scholar] [CrossRef] [Green Version]
  7. Khan, F.Y.; Elshafie, S.S.; Almaslamani, M.; Abu-Khattab, M.; El Hiday, A.H.; Errayes, M.; Almaslamani, E. Epidemiology of Bacteraemia in Hamad General Hospital, Qatar: A One Year Hospital-Based Study. Travel Med. Infect. Dis. 2010, 8, 377–387. [Google Scholar] [CrossRef] [PubMed]
  8. John Albert, M.; Bulach, D.; Alfouzan, W.; Izumiya, H.; Carter, G.; Alobaid, K.; Alatar, F.; Sheikh, A.R.; Poirel, L. Non-Typhoidal Salmonella Blood Stream Infection in Kuwait: Clinical and Microbiological Characteristics. PLoS Negl. Trop. Dis. 2019, 13, e0007293. [Google Scholar] [CrossRef]
  9. Alfouzan, W.; Ahmad, S.; Dhar, R.; Asadzadeh, M.; Almerdasi, N.; Abdo, N.M.; Joseph, L.; de Groot, T.; Alali, W.Q.; Khan, Z.; et al. Molecular Epidemiology of Candida Auris Outbreak in a Major Secondary-Care Hospital in Kuwait. J. Fungi 2020, 6, 307. [Google Scholar] [CrossRef] [PubMed]
  10. Jamal, W.; Rotimi, V.O.; Albert, M.J.; Khodakhast, F.; Nordmann, P.; Poirel, L. High Prevalence of VIM-4 and NDM-1 Metallo-β-Lactamase among Carbapenem-Resistant Enterobacteriaceae. J. Med. Microbiol. 2013, 62, 1239–1244. [Google Scholar] [CrossRef] [Green Version]
  11. Khan, Z.; Ahmad, S.; Al-Sweih, N.; Joseph, L.; Alfouzan, W.; Asadzadeh, M. Increasing Prevalence, Molecular Characterization and Antifungal Drug Susceptibility of Serial Candida Auris Isolates in Kuwait. PLoS ONE 2018, 13, e0195743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Jamal, W.; Al Roomi, E.; AbdulAziz, L.R.; Rotimi, V.O. Evaluation of Curetis Unyvero, a Multiplex PCR-Based Testing System, for Rapid Detection of Bacteria and Antibiotic Resistance and Impact of the Assay on Management of Severe Nosocomial Pneumonia. J. Clin. Microbiol. 2014, 52, 2487–2492. [Google Scholar] [CrossRef] [Green Version]
  13. Jamal, W.Y.; Albert, M.J.; Khodakhast, F.; Poirel, L.; Rotimi, V.O. Emergence of New Sequence Type OXA-48 Carbapenemase-Producing Enterobacteriaceae in Kuwait. Microb. Drug Resist. 2015, 21, 329–334. [Google Scholar] [CrossRef]
  14. Ibrahim, M.M.; Abuelmatty, A.M.; Mohamed, G.H.; Nasr, M.A.; Hussein, A.K.; Ebaed, M.E.D.; Sarhan, H.A. Best Tigecycline Dosing for Treatment of Infections Caused by Multidrug-Resistant Pathogens in Critically Ill Patients with Different Body Weights. Drug Des. Dev. Ther. 2018, 12, 4171–4179. [Google Scholar] [CrossRef] [Green Version]
  15. Babakir-Mina, M.; Othman, N.; Najmuldeen, H.H.; Noori, C.K.; Fatah, C.F.; Perno, C.-F.; Ciotti, M. Antibiotic Susceptibility of Vancomyin and Nitrofurantoin in Staphylococcus Aureus Isolated from Burnt Patients in Sulaimaniyah, Iraqi Kurdistan. New Microbiol. 2012, 35, 439–446. [Google Scholar]
  16. Jaber, A.A.S.; Ibrahim, B. Evaluation of Risk Factors Associated with Drug-Resistant Tuberculosis in Yemen: Data from Centres with High Drug Resistance. BMC Infect. Dis. 2019, 19, 464. [Google Scholar] [CrossRef] [PubMed]
  17. Jaber, A.A.S.; Ibrahim, B. Health-Related Quality of Life of Patients with Multidrug-Resistant Tuberculosis in Yemen: Prospective Study. Health Qual. Life Outcomes 2019, 17, 142. [Google Scholar] [CrossRef]
  18. Abd El Hafez, M.; Khalaf, N.G.; El Ahmady, M.; Abd El Aziz, A.; Hashim, A.E.G. An Outbreak of Methicillin Resistant Staphylococcus EpidermiDis. among Neonates in a Hospital in Saudi Arabia. J. Infect. Dev. Ctries 2011, 5, 692–699. [Google Scholar] [CrossRef] [Green Version]
  19. Al Mayahi, Z.; Kamel, S.; Amer, H.; Beatty, M. Outbreak of Colistin-Resistant Organisms at a Tertiary Hospital in Riyadh, Saudi Arabia, 2016. Pan Afr. Med. J. 2019, 34, 162. [Google Scholar] [CrossRef]
  20. Khan, U.; Huerga, H.; Khan, A.J.; Mitnick, C.D.; Hewison, C.; Varaine, F.; Bastard, M.; Rich, M.; Franke, M.F.; Atwood, S.; et al. The EndTB Observational Study Protocol: Treatment of MDR-TB with Bedaquiline or Delamanid Containing Regimens. BMC Infect. Dis. 2019, 19, 733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  21. Al-Ghafli, H.; Kohl, T.A.; Merker, M.; Varghese, B.; Halees, A.; Niemann, S.; Al-Hajoj, S. Drug-Resistance Profiling and Transmission Dynamics of Multidrug-Resistant Mycobacterium Tuberculosis in Saudi Arabia Revealed by Whole Genome Sequencing. Infect. Drug Resist. 2018, 11, 2219–2229. [Google Scholar] [CrossRef] [Green Version]
  22. Al-Jindan, R.; Al-Eraky, D. Two Cases of the Emerging Candida Auris in a University Hospital from Saudi Arabia. Saudi J. Med. Med. Sci. 2021, 9, 71. [Google Scholar] [CrossRef]
  23. Alhussain, F.A.; Yenugadhati, N.; Al Eidan, F.A.; Al Johani, S.; Badri, M. Risk Factors, Antimicrobial Susceptibility Pattern and Patient Outcomes of Pseudomonas Aeruginosa Infection: A Matched Case-Control Study. J. Infect. Public Health 2021, 14, 152–157. [Google Scholar] [CrossRef]
  24. AlJindan, R.; AlEraky, D.M.; Mahmoud, N.; Abdalhamid, B.; Almustafa, M.; AbdulAzeez, S.; Borgio, J.F. Drug Resistance-Associated Mutations in ERG11 of Multidrug-Resistant Candida Auris in a Tertiary Care Hospital of Eastern Saudi Arabia. J. Fungi 2020, 7, 18. [Google Scholar] [CrossRef]
  25. Almaghrabi, R.S.; Albalawi, R.; Mutabagani, M.; Atienza, E.; Aljumaah, S.; Gade, L.; Forsberg, K.; Litvintseva, A.; Althawadi, S. Molecular Characterisation and Clinical Outcomes of Candida Auris Infection: Single-centre Experience in Saudi Arabia. Mycoses 2020, 63, 452–460. [Google Scholar] [CrossRef] [PubMed]
  26. Bosaeed, M.; Ahmad, A.; Alali, A.; Mahmoud, E.; Alswidan, L.; Alsaedy, A.; Aljuhani, S.; Alalwan, B.; Alshamrani, M.; Alothman, A. Experience With Ceftolozane-Tazobactam for the Treatment of Serious Pseudomonas Aeruginosa Infections in Saudi Tertiary Care Center. Infect. Dis. 2020, 13, 117863372090597. [Google Scholar] [CrossRef]
  27. Aljadani, R.; Ahmed, A.E.; AL-Jahdali, H. Tuberculosis Mortality and Associated Factors at King Abdulaziz Medical City Hospital. BMC Infect. Dis. 2019, 19, 427. [Google Scholar] [CrossRef] [PubMed]
  28. Almangour, T.A.; Alenazi, B.; Ghonem, L.; Alhifany, A.A.; Aldakheel, B.A.; Alruwaili, A. Inhaled Colistin for the Treatment of Nosocomial Pneumonia Due to Multidrug-Resistant Gram-Negative Bacteria: A Real-Life Experience in Tertiary Care Hospitals in Saudi Arabia. Saudi Pharm. J. 2020, 28, 1009–1013. [Google Scholar] [CrossRef] [PubMed]
  29. Abdalhamid, B.; Almaghrabi, R.; Althawadi, S.; Omrani, A. First Report of Candida Auris Infections from Saudi Arabia. J. Infect. Public Health 2018, 11, 598–599. [Google Scholar] [CrossRef]
  30. Alraddadi, B.M.; Saeedi, M.; Qutub, M.; Alshukairi, A.; Hassanien, A.; Wali, G. Efficacy of Ceftazidime-Avibactam in the Treatment of Infections Due to Carbapenem-Resistant Enterobacteriaceae. BMC Infect. Dis. 2019, 19, 772. [Google Scholar] [CrossRef] [Green Version]
  31. Balkhy, H.; El-Saed, A.; Maghraby, R.; Khan, R.; Rishu, A.; Al-Dorzi, H.; Arabi, Y. Drug-Resistant Ventilator Associated Pneumonia in a Tertiary Care Hospital in Saudi Arabia. Ann. Thorac. Med. 2014, 9, 104. [Google Scholar] [CrossRef]
  32. Älgå, A.; Wong, S.; Shoaib, M.; Lundgren, K.; Giske, C.G.; von Schreeb, J.; Malmstedt, J. Infection with High Proportion of Multidrug-Resistant Bacteria in Conflict-Related Injuries is Associated with Poor Outcomes and Excess Resource Consumption: A Cohort Study of Syrian Patients Treated in Jordan. BMC Infect. Dis. 2018, 18, 233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Al-lawama, M.; Aljbour, H.; Tanash, A.; Badran, E. Intravenous Colistin in the Treatment of Multidrug-Resistant Acinetobacter in Neonates. Ann. Clin. Microbiol. Antimicrob. 2016, 15, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Almomani, B.A.; McCullough, A.; Gharaibeh, R.; Samrah, S.; Mahasneh, F. Incidence and Predictors of 14-Day Mortality in Multidrug-Resistant Acinetobacter Baumannii in Ventilator-Associated Pneumonia. J. Infect. Dev. Ctries 2015, 9, 1323–1330. [Google Scholar] [CrossRef] [Green Version]
  35. Abd El Ghany, M.; Sharaf, H.; Al-agamy, M.H.; Shibl, A.; Hill-Cawthorne, G.A.; Hong, P.-Y. Genomic Characterization of NDM-1 and 5, and OXA-181 Carbapenemases in Uropathogenic Escherichia coli Isolates from Riyadh, Saudi Arabia. PLoS ONE 2018, 13, e0201613. [Google Scholar] [CrossRef] [PubMed]
  36. Abdel-Halim, H.; Al Dajani, A.; Abdelhalim, A.; Abdelmalek, S. The Search of Potential Inhibitors of the AcrAB–TolC System of Multidrug-Resistant Escherichia coli: An in Silico Approach. Appl. Microbiol. Biotechnol. 2019, 103, 6309–6318. [Google Scholar] [CrossRef]
  37. Abed, A.R.; Khudhair, A.M.; Hussein, I.M. Effects of Misuse of Antibiotics on the Resistance of Escherichia coli Isolated from the Intestines of Broiler Chickens. Int. J. Drug Deliv. Technol. 2020, 10, 190–194. [Google Scholar] [CrossRef]
  38. Ahmad, S.; Al-Mutairi, N.M.; Mokaddas, E. Variations in the Occurrence of Specific RpoB Mutations in Rifampicin- Resistant Mycobacterium Tuberculosis Isolates from Patients of Different Ethnic Groups in Kuwait. Indian J. Med. Res. 2012, 135, 756–762. [Google Scholar]
  39. Ahmad Hamad, P.; Khadija, K.M. Prevalence of blaTEM, blaSHV, and blaCTX-M Genes among ESBL-Producing Klebsiella pneumoniae and Escherichia coli Isolated from Thalassemia Patients in Erbil, Iraq. Mediterr. J. Hematol. Infect. Dis. 2019, 11, e2019041. [Google Scholar] [CrossRef] [Green Version]
  40. Ahmed, M.U.; Farooq, R.; Hawashim, N.A.; Ahmed, M.; Yiannakou, N.; Sayeed, F.; Sayed, A.R.; Lutfullah, S. Sensitive, Resistant and Multi-Drug Resistant Acinetobacter Baumanii at Saudi Arabia Hospital Eastern Region. Pak. J. Pharm. Sci. 2015, 28, 825–832. [Google Scholar]
  41. Al Johani, S.M.; Akhter, J.; Balkhy, H.; El-Saed, A.; Younan, M.; Memish, Z. Prevalence of Antimicrobial Resistance among Gram-Negative Isolates in an Adult Intensive Care Unit at a Tertiary Care Center in Saudi Arabia. Ann. Saudi Med. 2010, 30, 364–369. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Al Wutayd, O.; Al Nafeesah, A.; Adam, I.; Babikir, I. The Antibiotic Susceptibility Patterns of Uropathogens Isolated in Qassim, Saudi Arabia. J. Infect. Dev. Ctries 2018, 12, 946–952. [Google Scholar] [CrossRef] [PubMed]
  43. Alaa, A.R.; Solhan, M.A.; Lalan, R.M.; Hiwa, L.I.; Mhamad, N.R.; Niga, K.M.; Awat, J.N.; Salar, A.I.; Brwa, H.Q.; Daryan, K.K.H.; et al. The antibiotic resistance pattern and molecular characterization of blactx and blatem genes of e. Coli isolated from different hosts based on the rate of antibiotic consumption in Sulaymaniyah/Iraq. Appl. Ecol. Environ. Res. 2020, 18, 6025–6040. [Google Scholar] [CrossRef]
  44. Alanazi, M.Q.; Alqahtani, F.Y.; Aleanizy, F.S. An Evaluation of E. coli in Urinary Tract Infection in Emergency Department at KAMC in Riyadh, Saudi Arabia: Retrospective Study. Ann. Clin. Microbiol. Antimicrob. 2018, 17, 3. [Google Scholar] [CrossRef] [PubMed]
  45. Alatoom, A.; Elsayed, H.; Lawlor, K.; AbdelWareth, L.; El-Lababidi, R.; Cardona, L.; Mooty, M.; Bonilla, M.-F.; Nusair, A.; Mirza, I. Comparison of Antimicrobial Activity between Ceftolozane–Tazobactam and Ceftazidime–Avibactam against Multidrug-Resistant Isolates of Escherichia coli, Klebsiella Pneumoniae, and Pseudomonas Aeruginosa. Int. J. Infect. Dis. 2017, 62, 39–43. [Google Scholar] [CrossRef] [Green Version]
  46. Alavudeen, S.S.; Vigneshwaran, E.; Asiri, S.A.A.; Alahmari, M.H.A.; Mohammed, M.A.; Algahtani, T.; Khan, N.A. Distribution of Multi-Resistant Bacterial Isolates from Clinical Specimens in a Hospital Environment of Kingdom of Saudi Arabia. J. Young Pharm. 2017, 9, 347–351. [Google Scholar] [CrossRef] [Green Version]
  47. Al-Ayed, M.S.Z.; Asaad, A.M.; Qureshi, M.A.; Attia, H.G.; AlMarrani, A.H. Antibacterial Activity of Salvadora Persica L. (Miswak) Extracts against Multidrug Resistant Bacterial Clinical Isolates. Evid.-Based Complementary Altern. Med. 2016, 2016, 7083964. [Google Scholar] [CrossRef] [Green Version]
  48. Albukhari, T.A.M.; Nafady-Hego, H.; Elgendy, H.; Abd Elmoneim, H.M.; Nafady, A.; Alzahrani, A.M. Analysis of Bacterial and Fungal Infections after Cytoreduction Surgery and Hyperthermic Intraperitoneal Chemotherapy: An Observational Single-Centre Study. Int. J. Microbiol. 2019, 2019, 6351874. [Google Scholar] [CrossRef] [Green Version]
  49. Al-Guranie, D.R.; Al-Mayahie, S.M. Prevalence of E. coli ST131 among Uropathogenic E. coli Isolates from Iraqi Patients in Wasit Province, Iraq. Int. J. Microbiol. 2020, 2020, 8840561. [Google Scholar] [CrossRef]
  50. Ali, F.A.; Hussen, B.M.; Zaki, S.M. Molecular detection of blactx-m gene among pseudomonas aeruginosa strains isolated from different clinical samples in erbil city. Ann. Trop. Med. Public Health 2020, 23, 231. [Google Scholar] [CrossRef]
  51. Aljanaby, A.A.J. Antibacterial Activity of an Aqueous Extracts of Alkanna Tinctoria Roots against Drug Resistant Aerobic Pathogenic Bacteria Isolated from Patients with Burns Infections. Russ. Open Med. J. 2018, 7, e0104. [Google Scholar] [CrossRef] [Green Version]
  52. Aljanaby, A.A.J.; Tuwaij, N.S.S.; Al-khilkhali, H.J.B. Antimicrobial Susceptibility Patterns of Klebsiella Pneumoniae Isolated from Older Smokers and Non-Smokers of Inpatients in Intensive Care Unit Infected with Chronic Pneumonia in AL-Najaf Hospital, Iraq. J. Pharm. Sci. 2018, 10, 6. [Google Scholar]
  53. Alm’amoori, K.; Hadi, Z.; Almohana, A. Molecular Investigation of Plasmid–Mediated Quinolone Resistant Genes among Aminoglycoside-Resistant Uropathogenic Escherichia coli Isolates from Babylon Hospitals, Iraq. Indian J. Forensic Med. Toxicol. 2020, 14, 493–498. [Google Scholar]
  54. Al-Mayahie, S.M. Phenotypic and Genotypic Comparison of ESBL Production by Vaginal Escherichia coli Isolates from Pregnant and Non-Pregnant Women. Ann. Clin. Microbiol. Antimicrob. 2013, 12, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Al-Mulla, N.; Elshafie, S.S.; Janahi, M.; Al-Nasser, A.; Chandra, P.; Taj-Aldeen, S.J. Bacterial Bloodstream Infections and Antimicrobial Susceptibility Pattern in Pediatric Hematology/Oncology Patients after Anticancer Chemotherapy. Infect. Drug Resist. 2014, 7, 289. [Google Scholar] [CrossRef] [Green Version]
  56. AlOtair, H.A.; Hussein, M.A.; Elhoseny, M.A.; Alzeer, A.H.; Khan, M.F. Severe Pneumonia Requiring ICU Admission: Revisited. J. Taibah Univ. Med. Sci. 2015, 10, 293–299. [Google Scholar] [CrossRef]
  57. Alqasim, A.; Abu Jaffal, A.; Alyousef, A.A. Prevalence of Multidrug Resistance and Extended-Spectrum β -Lactamase Carriage of Clinical Uropathogenic Escherichia coli Isolates in Riyadh, Saudi Arabia. Int. J. Microbiol. 2018, 2018, 3026851. [Google Scholar] [CrossRef] [Green Version]
  58. Alshareef, H.; Alfahad, W.; Albaadani, A.; Alyazid, H.; Talib, R.B. Impact of Antibiotic De-Escalation on Hospitalized Patients with Urinary Tract Infections: A Retrospective Cohort Single Center Study. J. Infect. Public Health 2020, 13, 985–990. [Google Scholar] [CrossRef]
  59. Alshukairi, A.N.; Moalim, H.M.; Alsaedi, A.; Almansouri, W.Y.; Al-Zahrani, M.; Aljuaid, A.; Alraddadi, B.M.; Altorkistani, H.H.; Alrajhi, A.A.; Al-Hajoj, S.A. Family Cluster of Multi-Drug Resistant Tuberculosis in Kingdom of Saudi Arabia. J. Infect. Public Health 2020, 13, 154–157. [Google Scholar] [CrossRef]
  60. Altalhi, A.D.; Gherbawy, Y.A.; Hassan, S.A. Antibiotic Resistance in Escherichia coli Isolated from Retail Raw Chicken Meat in Taif, Saudi Arabia. Foodborne Pathog. Dis. 2010, 7, 281–285. [Google Scholar] [CrossRef]
  61. Awayid, H.S.; Sahar, B.R.; Jalil, I.S.; Nouman, K.T. Immunization against Multi Drug Resistance Uropathogenic E. coli Isolate from Urinary Tract Infection in Pregnancy. Res. J. Pharm. Technol. 2019, 12, 5444. [Google Scholar] [CrossRef]
  62. Azab, K.S.M.; Abdel-Rahman, M.A.; El-Sheikh, H.H.; Azab, E.; Gobouri, A.A.; Farag, M.M.S. Distribution of Extended-Spectrum β-Lactamase (ESBL)-Encoding Genes among Multidrug-Resistant Gram-Negative Pathogens Collected from Three Different Countries. Antibiotics 2021, 10, 247. [Google Scholar] [CrossRef]
  63. Azim, N.S.A.; Al-Harbi, M.A.; Al-Zaban, M.I.; Nofal, M.Y.; Somily, A.M. Prevalence and Antibiotic Susceptibility among Gram Negative Bacteria Isolated from Intensive Care Units at a Tertiary Care Hospital in Riyadh, Saudi Arabia. J. Pure Appl. Microbiol. 2019, 13, 201–208. [Google Scholar] [CrossRef] [Green Version]
  64. Badran, E.F.; Din, R.A.Q.; Shehabi, A.A. Low Intestinal Colonization of Escherichia coli Clone ST131 Producing CTX-M-15 in Jordanian Infants. J. Med. Microbiol. 2016, 65, 137–141. [Google Scholar] [CrossRef] [PubMed]
  65. Balkhy, H.H.; El-Saed, A.; Alshamrani, M.M.; Alsaedi, A.; Al Nasser, W.; El Gammal, A.; Aljohany, S.M.; Almunif, S.; Arabi, Y.; Alqahtani, S.; et al. Ten-Year Resistance Trends in Pathogens Causing Healthcare-Associated Infections; Reflection of Infection Control Interventions at a Multi-Hospital Healthcare System in Saudi Arabia, 2007–2016. Antimicrob. Resist. Infect. Control 2020, 9, 21. [Google Scholar] [CrossRef] [Green Version]
  66. Balkhy, H.H.; El-Saed, A.; Alshamrani, M.M.; Alsaedi, A.; Nasser, W.A.; Gammal, A.E.; Aljohany, S.M.; Arabi, Y.; Alqahtani, S.; Bonnie, H.B.; et al. High Burden of Resistant Gram Negative Pathogens Causing Device-Associated Healthcare Infections in a Tertiary Care Setting in Saudi Arabia, 2008–2016. J. Glob. Antimicrob. Resist. 2020, 23, 26–32. [Google Scholar] [CrossRef] [PubMed]
  67. Bindayna, K.M.; Khanfar, H.S.; Senok, A.C.; Botta, G.A. Predominance of CTX-M Genotype among Extended Spectrum Beta Lactamase Isolates in a Tertiary Hospital in Saudi Arabia. Saudi Med. J. 2010, 31, 859–863. [Google Scholar]
  68. Burjaq, S.Z.; Shehabi, A. Fresh Leafy Green Vegetables Associated with Multidrug Resistant E. coli. Int. ARABIC J. Antimicrob. Agents 2013, 3, 1–7. [Google Scholar]
  69. Darwish, R.M.; Aburjai, T.A. Effect of Ethnomedicinal Plants Used in Folklore Medicine in Jordan as Antibiotic Resistant Inhibitors on Escherichia coli. BMC Complement Altern. Med. 2010, 10, 9. [Google Scholar] [CrossRef] [Green Version]
  70. Dashti, A.A.; Vali, L.; El-Shazly, S.; Jadaon, M.M. The Characterization and Antibiotic Resistance Profiles of Clinical Escherichia coli O25b-B2-ST131 Isolates in Kuwait. BMC Microbiol. 2014, 14, 214. [Google Scholar] [CrossRef] [Green Version]
  71. Dawood, W.S. Molecular and Susceptibility Study of Antibiotic Resistance Genes in E. coli Isolated from Selected Iraqi Patients. Syst. Rev. Pharm. 2020, 11, 10. [Google Scholar]
  72. El-Ghareeb, W.R.; Abdel-Raheem, S.M.; Al-Marri, T.M.; Alaql, F.A.; Fayez, M.M. Isolation and Identification of Extended Spectrum β-Lactamases (ESBLs) Escherichia coli from Minced Camel Meat in Eastern Province, Saudi Arabia. Thai J. Vet. Med. 2020, 50, 155–161. [Google Scholar]
  73. El-Saed, A.; Balkhy, H.H.; Alshamrani, M.M.; Aljohani, S.; Alsaedi, A.; Al Nasser, W.; El Gammal, A.; Almohrij, S.A.; Alyousef, Z.; Almunif, S.; et al. High Contribution and Impact of Resistant Gram Negative Pathogens Causing Surgical Site Infections at a Multi-Hospital Healthcare System in Saudi Arabia, 2007–2016. BMC Infect. Dis. 2020, 20, 275. [Google Scholar] [CrossRef] [PubMed]
  74. Elsohaby, I.; Samy, A.; Elmoslemany, A.; Alorabi, M.; Alkafafy, M.; Aldoweriej, A.; Al-Marri, T.; Elbehiry, A.; Fayez, M. Migratory Wild Birds as a Potential Disseminator of Antimicrobial-Resistant Bacteria around Al-Asfar Lake, Eastern Saudi Arabia. Antibiotics 2021, 10, 260. [Google Scholar] [CrossRef] [PubMed]
  75. Eltai, N.O.; Abdfarag, E.A.; Al-Romaihi, H.; Wehedy, E.; Mahmoud, M.H.; Alawad, O.K.; Al-Hajri, M.M.; Al Thani, A.A.; Yassine, H.M. Antibiotic Resistance Profile of Commensal Escherichia coli Isolated from Broiler Chickens in Qatar. J. Food Prot. 2017, 81, 302–307. [Google Scholar] [CrossRef] [PubMed]
  76. Eltai, N.O.; Al Thani, A.A.; Al Hadidi, S.H.; Al Ansari, K.; Yassine, H.M. Antibiotic Resistance and Virulence Patterns of Pathogenic Escherichia coli Strains Associated with Acute Gastroenteritis among Children in Qatar. BMC Microbiol. 2020, 20, 54. [Google Scholar] [CrossRef] [PubMed]
  77. Fadlelmula, A.; Al-Hamam, N.A.; Al-Dughaym, A.M. A Potential Camel Reservoir for Extended-Spectrum β-Lactamase-Producing Escherichia coli Causing Human Infection in Saudi Arabia. Trop. Anim. Health Prod. 2016, 48, 427–433. [Google Scholar] [CrossRef]
  78. Garcell, H.G.; Arias, A.V.; Pancorbo Sandoval, C.A.; García, E.G.; Valle Gamboa, M.E.; Sado, A.B.; Alfonso Serrano, R.N. Incidence and Etiology of Surgical Site Infections in Appendectomies: A 3-Year Prospective Study. Oman Med. J. 2017, 32, 31–35. [Google Scholar] [CrossRef]
  79. Ghanem, B.; Haddadin, R.N. Multiple Drug Resistance and Biocide Resistance in Escherichia coli Environmental Isolates from Hospital and Household Settings. Antimicrob. Resist. Infect. Control 2018, 7, 47. [Google Scholar] [CrossRef] [Green Version]
  80. Haddadin, R.N.; Assaf, A.M.; Homsi, A.; Collier, P.J.; Shehabi, A. Investigating Possible Association between Multidrug Resistance and Isolate Origin with Some Virulence Factors of Escherichia coli Strains Isolated from Infant Faeces and Fresh Green Vegetables. J. Appl. Microbiol. 2019, 127, 88–98. [Google Scholar] [CrossRef] [PubMed]
  81. Hameed, T.; Al Nafeesah, A.; Chishti, S.; Al Shaalan, M.; Al Fakeeh, K. Community-Acquired Urinary Tract Infections in Children: Resistance Patterns of Uropathogens in a Tertiary Care Center in Saudi Arabia. Int. J. Pediatrics Adolesc. Med. 2019, 6, 51–54. [Google Scholar] [CrossRef] [PubMed]
  82. Hammoudi, A. Antibiotics Susceptibility Pattern of Some Enterobacteriaceae Isolates from Different Clinical Infectious Sources. Int. J. Res. Pharm. Sci. 2019, 10, 734–741. [Google Scholar]
  83. Hassan, H.; Abdalhamid, B. Molecular Characterization of Extended-Spectrum Beta-Lactamase Producing Enterobacteriaceae in a Saudi Arabian Tertiary Hospital. J. Infect. Dev. Ctries 2014, 8, 282–288. [Google Scholar] [CrossRef] [Green Version]
  84. Huang, X.-Z.; Frye, J.G.; Chahine, M.A.; Glenn, L.M.; Ake, J.A.; Su, W.; Nikolich, M.P.; Lesho, E.P. Characteristics of Plasmids in Multi-Drug-Resistant Enterobacteriaceae Isolated during Prospective Surveillance of a Newly Opened Hospital in Iraq. PLoS ONE 2012, 7, e40360. [Google Scholar] [CrossRef]
  85. Ibrahim, R.A.; Cryer, T.L.; Lafi, S.Q.; Basha, E.-A.; Good, L.; Tarazi, Y.H. Identification of Escherichia coli from Broiler Chickens in Jordan, Their Antimicrobial Resistance, Gene Characterization and the Associated Risk Factors. BMC Vet. Res. 2019, 15, 159. [Google Scholar] [CrossRef] [PubMed]
  86. Ibrahim, I.; Al- Shwaikh, R.; Ismaeil, M. Virulence and Antimicrobial Resistance of Escherichia coli Isolated from Tigris River and Children Diarrhea. Infect. Drug Resist. 2014, 317. [Google Scholar] [CrossRef] [Green Version]
  87. Ibrahim, M.E.; Bilal, N.E.; Hamid, M.E. Comparison of Phenotypic Characteristics and Antimicrobial Resistance Patterns of Clinical Escherichia coli Collected From Two Unrelated Geographical Areas. GJHS 2014, 6, 126. [Google Scholar] [CrossRef] [Green Version]
  88. Jaloob Aljanaby, A.A.; Aljanaby, I.A.J. Antimicrobial Sensitivity Pattern of Pathogenic Bacteria Isolated from Older Women with Asymptomatic Bacteriuria. Biomed. Res. 2018, 29. [Google Scholar] [CrossRef] [Green Version]
  89. Karomi, A.S.A. Screening Study for Some Strains of E. coli Collected from Five Regions in Kurdistan-Iraq for Its Sensitivity, Resistance and MDR against Thirteen Antibiotics. Med. Leg. Update 2020, 20, 526–531. [Google Scholar] [CrossRef]
  90. Khairy, G.A.; Kambal, A.M.; Al-Dohayan, A.A.; Al-Shehri, M.Y.; Zubaidi, A.M.; Al-Naami, M.Y.; AlSaif, F.A.; Al-Obaid, O.A.; Al-Saif, A.A.; El-Farouk, O.Y.; et al. Surgical Site Infection in a Teaching Hospital: A Prospective Study. J. Taibah Univ. Med. Sci. 2011, 6, 114–120. [Google Scholar] [CrossRef]
  91. Majeed, H.T.; Aljanaby, A.A.J. Antibiotic Susceptibility Patterns and Prevalence of Some Extended Spectrum Beta- Lactamases Genes in Gram-Negative Bacteria Isolated from Patients Infected with Urinary Tract Infections in Al-Najaf City, Iraq. Avicenna J. Med. Biotechnol. 2019, 11, 192–201. [Google Scholar]
  92. Marie, M.A.; John, J.; Krishnappa, L.G.; Gopalkrishnan, S. Molecular Characterization of the β-Lactamases in Escherichia coli and Klebsiella Pneumoniae from a Tertiary Care Hospital in Riyadh, Saudi Arabia: β-Lactamases in Enterobacteriaceae. Microbiol. Immunol. 2013, 57, 805–810. [Google Scholar] [CrossRef]
  93. Mazi, W.; Begum, Z.; Abdulla, D.; Hesham, A.; Maghari, S.; Assiri, A.; Senok, A. Central Line–Associated Bloodstream Infection in a Trauma Intensive Care Unit: Impact of Implementation of Society for Healthcare Epidemiology of America/Infectious Diseases Society of America Practice Guidelines. Am. J. Infect. Control 2014, 42, 865–867. [Google Scholar] [CrossRef]
  94. Memish, Z.A.; Assiri, A.; Almasri, M.; Roshdy, H.; Hathout, H.; Kaase, M.; Gatermann, S.G.; Yezli, S. Molecular Characterization of Carbapenemase Production Among Gram-Negative Bacteria in Saudi Arabia. Microb. Drug Resist. 2015, 21, 307–314. [Google Scholar] [CrossRef]
  95. Mutti, M.; Sonnevend, Á.; Pál, T.; Junttila, S.; Ekker, H.; Galik, B.; Gyenesei, A.; Nagy, G.; Nagy, E.; Szijártó, V. Complete Genome Sequence of Escherichia coli 81009, a Representative of the Sequence Type 131 C1-M27 Clade with a Multidrug-Resistant Phenotype. Genome Announc. 2018, 6, e00056-18. [Google Scholar] [CrossRef] [Green Version]
  96. Nairoukh, Y.R.; Mahafzah, A.M.; Irshaid, A.; Shehabi, A.A. Molecular Characterization of Multidrug Resistant Uropathogenic E. coli Isolates from Jordanian Patients. Open Microbiol. J. 2018, 12, 1–7. [Google Scholar] [CrossRef] [PubMed]
  97. Narchi, H.; Al-Hamdani, M. Uropathogen Resistance to Antibiotic Prophylaxis in Urinary Tract Infections. Microb. Drug Resist. 2010, 16, 151–154. [Google Scholar] [CrossRef] [PubMed]
  98. Nimri, L.; Abu AL- Dahab, F.; Batchoun, R. Foodborne Bacterial Pathogens Recovered from Contaminated Shawarma Meat in Northern Jordan. J. Infect. Dev. Ctries 2014, 8, 1407–1414. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Nimri, L.; Samara, H.; Batchoun, R. Detection of Mutations Associated with Multidrug-Resistant Mycobacterium Tuberculosis Clinical Isolates. FEMS Immunol. Med. Microbiol. 2011, 62, 321–327. [Google Scholar] [CrossRef] [Green Version]
  100. Obaidat, M.M. Prevalence and Antimicrobial Resistance of Listeria Monocytogenes, Salmonella Enterica and Escherichia coli O157:H7 in Imported Beef Cattle in Jordan. Comp. Immunol. Microbiol. Infect. Dis. 2020, 70, 101447. [Google Scholar] [CrossRef]
  101. Pál, T.; Ghazawi, A.; Darwish, D.; Villa, L.; Carattoli, A.; Hashmey, R.; Aldeesi, Z.; Jamal, W.; Rotimi, V.; Al-Jardani, A.; et al. Characterization of NDM-7 Carbapenemase-Producing Escherichia coli Isolates in the Arabian Peninsula. Microb. Drug Resist. 2017, 23, 871–878. [Google Scholar] [CrossRef]
  102. Radwan Ali, M.; Khudhair, A.M. Detection of Colony Adhesion Factors and Genetic Background of Adhesion Genes Among Multidrug-Resistant Uropathogenic Escherichia coli Isolated in Iraq. J. Pure Appl. Microbiol. 2018, 12, 2017–2026. [Google Scholar] [CrossRef] [Green Version]
  103. Rana, M.A.; Abd El Rahaman, B.; Mady, A.F.; Al Odat, M.; Al Harthy, A.; Ramadan, O.E.S.; Mumtaz, S.A.; Omrani, A.S. Intra-Pleural Colistin Methanesulfonate Therapy for Pleural Infection Caused by Carbapenem-Resistant Acinetobacter Baumannii: A Successful Case Report. Infect. Dis. Rep. 2014, 6, 38–40. [Google Scholar] [CrossRef] [Green Version]
  104. Salah, M.; Badran, E.; Shehabi, A. High Incidence of Multidrug Resistant Escherichia coli Producing CTX-M-Type ESBLs Colonizing the Intestine of Jordanian Infants. Int. Arab. J. Antimicrob. Agents 2014, 3, 1–8. [Google Scholar]
  105. Shobrak, M.Y.; Hassan, S.A.; Stiévenart, C.; El-Deeb, B.A.; Gherbawy, Y.A. Prevalence and Antibiotic Resistance Profile of Intestinal Bacteria Isolated from Captive Adult Houbara Bustards ( ) Exposed to Natural Weather Conditions in Saudi Arabia. Escherichia coli. Glob. Vet. 2013, 10, 276–284. [Google Scholar]
  106. Sonnevend, A.; Yahfoufi, N.; Ghazawi, A.; Jamal, W.; Rotimi, V.; Pal, T. Contribution of Horizontal Gene Transfer to the Emergence of VIM-4 Carbapenemase Producer Enterobacteriaceae in Kuwait. Infect. Drug Resist. 2017, 10, 469–478. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Taha, M.M.E.; Homeida, H.E.; Dafalla, O.M.E.; Abdelwahab, S.I. Multidrug Resistance, Prevalence and Phylogenetic Analysis of Genes Encoding Class II and III Integrons in Clinically Isolated Escherichia coli. Cell. Mol. Biol. 2018, 64, 122. [Google Scholar] [CrossRef]
  108. Taher, I.; Almaeen, A.; Aljourfi, H.; Bohassan, E.; Helmy, A.; El-Masry, E.; Saleh, B.; Aljaber, N. Surveillance of Antibiotic Resistance among Uropathogens in Aljouf Region Northern Saudi Arabia. Iran. J. Microbiol. 2020, 11, 468. [Google Scholar] [CrossRef]
  109. Tarazi, Y.H.; Abu-Basha, E.A.; Ismail, Z.B.; Tailony, R.A. In Vitro and in Vivo Efficacy Study of Cefepime, Doripenem, Tigecycline, and Tetracycline against Extended-Spectrum Beta-Lactamases Escherichia coli in Chickens. Vet. World 2020, 13, 446–451. [Google Scholar] [CrossRef]
  110. Thani, A.S.B. Characterization of Previously Identified Novel DNA Fragment Associated with Pathogenicity Island III536 Reveals New Bla Gene. Infect. Genet. Evol. 2019, 75, 103971. [Google Scholar] [CrossRef]
  111. Saeed, N.K.; Kambal, A.M.; El-Khizzi, N.A. Antimicrobial-Resistant Bacteria in a General Intensive Care Unit in Saudi Arabia. Saudi Med. J. 2010, 31, 1341–1349. [Google Scholar]
  112. Ahmad, S.; Mokaddas, E.; Al-Mutairi, N.; Eldeen, H.S.; Mohammadi, S. Discordance across Phenotypic and Molecular Methods for Drug Susceptibility Testing of Drug-Resistant Mycobacterium Tuberculosis Isolates in a Low TB Incidence Country. PLoS ONE 2016, 11, e0153563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Ahmed, M.M.; Mohammed, S.H.; Nasurallah, H.A.A.; Ali, M.M.; Couvin, D.; Rastogi, N. Snapshot of the Genetic Diversity of Mycobacterium Tuberculosis Isolates in Iraq. Int. J. Mycobacteriol. 2014, 3, 184–196. [Google Scholar] [CrossRef] [PubMed]
  114. Ahmed-Abakur, E.; Saad Alnour, T. Detection of Multidrug Resistant Mycobacterium Tuberculosis in Tabuk, Saudi Arabia, Using Genotype MTBDRplus. Int. J. Mycobacteriol. 2019, 8, 25. [Google Scholar] [CrossRef]
  115. Al Mahbashi, A.A.; Mukhtar, M.M.; Mahgoub, E.S. Molecular Typing of Mycobacterium spp. Isolates from Yemeni Tuberculosis Patients. East Mediterr. Health J. 2013, 19, 942–946. [Google Scholar] [CrossRef]
  116. AL Qurainees, G.I.; Tufenkeji, H.T. A Child with Complicated Mycobacterium Tuberculosis. Int. J. Pediatrics Adolesc. Med. 2016, 3, 28–33. [Google Scholar] [CrossRef] [Green Version]
  117. Alateah, S.M.; Othman, M.W.; Ahmed, M.; Al Amro, M.S.; Al Sherbini, N.; Ajlan, H.H. A Retrospective Study of Tuberculosis Prevalence amongst Patients Attending a Tertiary Hospital in Riyadh, Saudi Arabia. J. Clin. Tuberc. Other Mycobact. Dis. 2020, 21, 100185. [Google Scholar] [CrossRef]
  118. Al-Hajoj, S.; Varghese, B.; Shoukri, M.M.; Al-Omari, R.; Al-Herbwai, M.; AlRabiah, F.; Alrajhi, A.A.; Abuljadayel, N.; Al-Thawadi, S.; Zumla, A.; et al. Epidemiology of Antituberculosis Drug Resistance in Saudi Arabia: Findings of the First National Survey. Antimicrob. Agents Chemother. 2013, 57, 2161–2166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  119. Al-Hajoj, S.; Shoukri, M.; Memish, Z.; AlHakeem, R.; AlRabiah, F.; Varghese, B. Exploring the Sociodemographic and Clinical Features of Extrapulmonary Tuberculosis in Saudi Arabia. PLoS ONE 2015, 10, e0101667. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  120. Ali, M.; Howady, F.; Munir, W.; Karim, H.; Al-Suwaidi, Z.; Al-Maslamani, M.; Alkhal, A.; Elmaki, N.; Ziglam, H. Drug-Resistant Tuberculosis: An Experience from Qatar. Libyan J. Med. 2020, 15, 1744351. [Google Scholar] [CrossRef] [Green Version]
  121. Ali Chaudhry, L.; Rambhala, N.; Al-Shammri, A.S.; Al-Tawfiq, J.A. Patterns of Antituberculous Drug Resistance in Eastern Saudi Arabia: A 7-Year Surveillance Study from 1/2003 to 6/2010. J. Epidemiol. Glob. Health 2011, 2, 57. [Google Scholar] [CrossRef] [Green Version]
  122. Al-Mutairi, N.M.; Ahmad, S.; Mokaddas, E.; Eldeen, H.S.; Joseph, S. Occurrence of Disputed RpoB Mutations among Mycobacterium Tuberculosis Isolates Phenotypically Susceptible to Rifampicin in a Country with a Low Incidence of Multidrug-Resistant Tuberculosis. BMC Infect. Dis. 2019, 19, 3. [Google Scholar] [CrossRef] [Green Version]
  123. Al-Mutairi, N.M.; Ahmad, S.; Mokaddas, E. First Report of Molecular Detection of Fluoroquinolone Resistance-Associated GyrA Mutations in Multidrug-Resistant Clinical Mycobacterium Tuberculosis Isolates in Kuwait. BMC Res. Notes 2011, 4, 123. [Google Scholar] [CrossRef] [Green Version]
  124. Al-Mutairi, N.M.; Ahmad, S.; Mokaddas, E. Molecular Screening Versus Phenotypic Susceptibility Testing of Multidrug-Resistant Mycobacterium Tuberculosis Isolates for Streptomycin and Ethambutol. Microb. Drug Resist. 2018, 24, 923–931. [Google Scholar] [CrossRef] [PubMed]
  125. Al-Mutairi, N.M.; Ahmad, S.; Mokaddas, E.M. Correction to: Molecular Characterization of Multidrug-Resistant Mycobacterium Tuberculosis (MDR-TB) Isolates Identifies Local Transmission of Infection in Kuwait, a Country with a Low Incidence of TB and MDR-TB. Eur. J. Med. Res. 2020, 25, 14. [Google Scholar] [CrossRef]
  126. Al-Rubaye, D.S.; Henihan, G.; Al-Abasly, A.K.A.; Seagar, A.-L.; Al-Attraqchi, A.A.F.; Schulze, H.; Hashim, D.S.; Kamil, J.K.; Laurenson, I.F.; Bachmann, T.T. Genotypic Assessment of Drug-Resistant Tuberculosis in Baghdad and Other Iraqi Provinces Using Low-Cost and Low-Density DNA Microarrays. J. Med. Microbiol. 2016, 65, 114–122. [Google Scholar] [CrossRef] [PubMed]
  127. Altuwaijri, T.A.; Alhindi, G.K.; Al-Qattan, N.M.; Alkharashi, S.K.; Somily, A.M.; Altoijry, A.H. Occurrence of Venous Thromboembolism in Hospitalized Patients with Tuberculosis in Saudi Arabia: A Retrospective Cohort Study. Int. J. Mycobacteriol. 2020, 9, 4. [Google Scholar]
  128. Alyamani, E.J.; Marcus, S.A.; Ramirez-Busby, S.M.; Hansen, C.; Rashid, J.; El-kholy, A.; Spalink, D.; Valafar, F.; Almehdar, H.A.; Jiman-Fatani, A.A.; et al. Genomic Analysis of the Emergence of Drug-Resistant Strains of Mycobacterium Tuberculosis in the Middle East. Sci. Rep. 2019, 9, 4474. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  129. Al-Zarouni, M.; Dash, N.; Al Ali, M.; Al-Shehhi, F.; Panigrahi, D. Tuberculosis and MDR-TB in the Northern Emirates of United Arab Emirates: A 5-Year Study. Southeast Asian J. Trop Med. Public Health 2010, 41, 163–168. [Google Scholar] [PubMed]
  130. Asaad, A.M.; Alqahtani, J.M. Primary Anti-Tuberculous Drugs Resistance of Pulmonary Tuberculosis in Southwestern Saudi Arabia. J. Infect. Public Health 2012, 5, 281–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  131. El Mahalli, A.A.; Al-Qahtani, M.F. Predictors of Drug Resistance in Tuberculosis Patients in the Eastern Province, Saudi Arabia. J. Egypt. Public Health Assoc. 2015, 90, 24–28. [Google Scholar] [CrossRef] [PubMed]
  132. Flaifel, D.K.; Al-Azawi, I.H. The Role of IL-6 Gene Polymorphism in Multidrug-Resistant Tuberculosis Patients in Iraq. Int. J. Drug Deliv. Technol. 2020, 10, 81–84. [Google Scholar] [CrossRef]
  133. Habous, M.; Elimam, M.; AlDabal, L.; Chidambaran, B.; AlDeesi, Z. Pattern of Primary Tuberculosis Drug Resistance and Associated Risk Factors at Dubai Health Authority in Dubai. Int. J. Mycobacteriol. 2020, 9, 6. [Google Scholar]
  134. Kareem, P.A.; Alsammak, E.G.H.; Abdullah, Y.J.; Bdaiwi, Q.M. Estimation of Antibacterial Activity of Zinc Oxide, Titanium Dioxide, and Silver Nanoparticles against Multidrug-Resistant Bacteria Isolated from Clinical Cases in Amara City, Iraq. Drug Invent. Today 2019, 11, 5. [Google Scholar]
  135. Elhassan, M.M.; Hemeg, H.A.; Elmekki, M.A.; Turkistani, K.A.; Abdul-Aziz, A.A. Burden of Multidrug Resistant Mycobacterium Tuberculosis Among New Cases in Al-Madinah Al-Monawarah, Saudi Arabia. Infect. Disord.-Drug Targets 2017, 17, 14–23. [Google Scholar] [CrossRef] [Green Version]
  136. Merza, M.A.; Farnia, P.; Salih, A.M.; Masjedi, M.R.; Velayati, A.A. First Insight into the Drug Resistance Pattern of Mycobacterium Tuberculosis in Dohuk, Iraq: Using Spoligotyping and MIRU-VNTR to Characterize Multidrug Resistant Strains. J. Infect. Public Health 2011, 4, 41–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  137. Mokaddas, E.; Ahmad, S.; Eldeen, H.S.; Al-Mutairi, N. Discordance between Xpert MTB/RIF Assay and Bactec MGIT 960 Culture System for Detection of Rifampin-Resistant Mycobacterium Tuberculosis Isolates in a Country with a Low Tuberculosis (TB) Incidence. J. Clin. Microbiol. 2015, 53, 1351–1354. [Google Scholar] [CrossRef] [Green Version]
  138. Sambas, M.F.M.K.; Rabbani, U.; Al-Gethamy, M.M.M.; Surbaya, S.H.; Alharbi, F.F.I.; Ahmad, R.G.A.; Qul, H.K.H.; Nassar, S.M.S.; Maddah, A.K.M.A.; Darweesh, B.A.K. Prevalence and Determinants of Multidrug-Resistant Tuberculosis in Makkah, Saudi Arabia. Infect. Drug Resist. 2020, 13, 4031–4038. [Google Scholar] [CrossRef]
  139. Somily, A.M.; Naeem, T.; Habib, H.A.; Sarwar, M.S.; Kunimoto, D.Y.; Kambal, A.M. Changing Epidemiology of Tuberculosis Detected by an 8-Year Retrospective Laboratory Study in a Tertiary Teaching Hospital in Central Saudi Arabia. Saudi Med. J. 2014, 35, 691–698. [Google Scholar]
  140. Varghese, B.; Supply, P.; Allix-Béguec, C.; Shoukri, M.; Al-Omari, R.; Herbawi, M.; Al-Hajoj, S. Admixed Phylogenetic Distribution of Drug Resistant Mycobacterium Tuberculosis in Saudi Arabia. PLoS ONE 2013, 8, e55598. [Google Scholar] [CrossRef]
  141. Varghese, B.; Al-Hajoj, S. First Insight Into the Fluoroquinolone and Aminoglycoside Resistance of Multidrug-Resistant Mycobacterium Tuberculosis in Saudi Arabia. Am. J. Trop. Med. Hyg. 2017, 96, 1066–1070. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  142. Abulhasan, Y.B.; Abdullah, A.A.; Shetty, S.A.; Ramadan, M.A.; Yousef, W.; Mokaddas, E.M. Health Care-Associated Infections in a Neurocritical Care Unit of a Developing Country. Neurocrit. Care 2020, 32, 836–846. [Google Scholar] [CrossRef] [PubMed]
  143. Ahmed, S.S.; Shariq, A.; Alsalloom, A.A.; Babikir, I.H.; Alhomoud, B.N. Uropathogens and Their Antimicrobial Resistance Patterns: Relationship with Urinary Tract Infections. Int. J. Health Sci. 2019, 13, 8. [Google Scholar]
  144. Al Bshabshe, A.; Joseph, M.R.P.; Al Hussein, A.; Haimour, W.; Hamid, M.E. Multidrug Resistance Acinetobacter Species at the Intensive Care Unit, Aseer Central Hospital, Saudi Arabia: A One Year Analysis. Asian Pac. J. Trop. Med. 2016, 9, 903–908. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  145. Al-Agamy, M.H.; Jeannot, K.; El-Mahdy, T.S.; Shibl, A.M.; Kattan, W.; Plésiat, P.; Courvalin, P. First Detection of GES-5 Carbapenemase-Producing Acinetobacter Baumannii Isolate. Microb. Drug Resist. 2017, 23, 556–562. [Google Scholar] [CrossRef]
  146. Alamri, A.M.; Alsultan, A.A.; Ansari, M.A.; Alnimr, A.M. Biofilm-Formation in Clonally Unrelated Multidrug-Resistant Acinetobacter Baumannii Isolates. Pathogens 2020, 9, 630. [Google Scholar] [CrossRef]
  147. Al-Anazi, K.A.; Abdalhamid, B.; Alshibani, Z.; Awad, K.; Alzayed, A.; Hassan, H.; Alsayiegh, M. Acinetobacter Baumannii Septicemia in a Recipient of an Allogeneic Hematopoietic Stem Cell Transplantation. Case Rep. Transplant. 2012, 2012, 646195. [Google Scholar] [CrossRef] [PubMed]
  148. Al-Dabaibah, N.; Obeidat, N.; Shehabi, A. Epidemiology Features of Acinetobacter Baumannii Colonizing Respiratory Tracts of ICU Patients. Int. Arab. J. Antimicrob. Agents 2012, 2, 1–7. [Google Scholar]
  149. ALfadli, M.; EL-sehsah, E.M.; Ramadan, M.A.-M. Risk Factors and Distribution of MDROs among Patients with Healthcare Associated Burn Wound Infection. Germs 2018, 8, 199–206. [Google Scholar] [CrossRef]
  150. Alhaddad, M.; AlBarjas, A.; Alhammar, L.; Al Rashed, A.; Badger-Emeka, L. Molecular Characterization and Antibiotic Susceptibility Pattern of Acinetobacter Baumannii Isolated in Intensive Care Unit Patients in Al-Hassa, Kingdom of Saudi Arabia. Int. J. Appl. Basic Med. Res. 2018, 8, 19. [Google Scholar] [CrossRef]
  151. Al-Hamad, A.; Pal, T.; Leskafi, H.; Abbas, H.; Hejles, H.; Alsubikhy, F.; Darwish, D.; Ghazawi, A.; Sonnevend, A. Molecular Characterization of Clinical and Environmental Carbapenem Resistant Acinetobacter Baumannii Isolates in a Hospital of the Eastern Region of Saudi Arabia. J. Infect. Public Health 2020, 13, 632–636. [Google Scholar] [CrossRef]
  152. Alharbi, A.; Alshami, I. In Vitro Effects of Tigecycline in Combination with Other Antimicrobials against Multidrug-Resistant Acinetobacter Baumannii Isolates. J. Pure Appl. Microbiol. 2015, 8, 497–502. [Google Scholar]
  153. AL-Harmoosh, R.; Jarallah, E.; AL-Shamari, A. Coexistence of the BlaIMP and BlaSIM Genes in Clinical Isolates of Acinetobacter baumanniiIN Babylon Hospitals Iraq. Int. J. PharmTech Res. 2016, 9, 257–264. [Google Scholar]
  154. Ali, H.M.; Salem, M.Z.M.; El-Shikh, M.S.; Megeed, A.A.; Alogaibi, Y.A.; Talea, I.A. Investigation of the Virulence Factors and Molecular Characterization of the Clonal Relations of Multidrug-Resistant Acinetobacter Baumannii Isolates. J. AOAC Int. 2017, 100, 152–158. [Google Scholar] [CrossRef]
  155. Ali, K.M.; Al-Jaff, B.M.A. Source and Antibiotic Susceptibility of Gram-Negative Bacteria Causing Superficial Incisional Surgical Site Infections. Int. J. Surg. Open 2021, 30, 100318. [Google Scholar] [CrossRef]
  156. Ali, M.; Marie, M.; Gowda Krishnappa, L.; Alzahrani, A.J.; Mubaraki, M.A.; Alyousef, A.A. A Prospective Evaluation of Synergistic Effect of Sulbactam and Tazobactam Combination with Meropenem or Colistin against Multidrug Resistant Acinetobacter Baumannii. Bosn. J. Basic Med. Sci. 2015, 15, 24. [Google Scholar] [CrossRef] [Green Version]
  157. Aljindan, R.; Bukharie, H.; Alomar, A.; Abdalhamid, B. Prevalence of Digestive Tract Colonization of Carbapenem-Resistant Acinetobacter Baumannii in Hospitals in Saudi Arabia. J. Med. Microbiol. 2015, 64, 400–406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  158. AL-Kadmy, I.; Ali, A.; Salman, I.; Khazaal, S. Molecular Characterization of Acinetobacter Baumannii Isolated from Iraqi Hospital Environment. New Microbes New Infect. 2017, 21, 51–57. [Google Scholar] [CrossRef] [PubMed]
  159. Almaghrabi, M.K.; Joseph, M.R.P.; Assiry, M.M.; Hamid, M.E. Multidrug-Resistant Acinetobacter Baumannii: An Emerging Health Threat in Aseer Region, Kingdom of Saudi Arabia. Can. J. Infect. Dis. Med. Microbiol. 2018, 2018, 9182747. [Google Scholar] [CrossRef] [Green Version]
  160. Almutairy, R.; Aljrarri, W.; Noor, A.; Elsamadisi, P.; Shamas, N.; Qureshi, M.; Ismail, S. Impact of Colistin Dosing on the Incidence of Nephrotoxicity in a Tertiary Care Hospital in Saudi Arabia. Antibiotics 2020, 9, 485. [Google Scholar] [CrossRef]
  161. Al-Obeid, S.; Jabri, L.; Al-Agamy, M.; Al-Omari, A.; Shibl, A. Epidemiology of Extensive Drug Resistant Acinetobacter Baumannii (XDRAB) at Security Forces Hospital (SFH) in Kingdom of Saudi Arabia (KSA). J. Chemother. 2015, 27, 156–162. [Google Scholar] [CrossRef]
  162. Al-Ouqaili, M.T.S.; Jal’oot, A.S.; Badawy, A.S. Identification of an OprD and Bla IMP Gene-Mediated Carbapenem Resistance in Acinetobacter Baumannii and Pseudomonas Aeruginosa among Patients with Wound Infections in Iraq. Asian J. Pharm. 2018, 12. [Google Scholar] [CrossRef]
  163. Al-Sweih, N.A.; Al-Hubail, M.A.; Rotimi, V.O. Emergence of Tigecycline and Colistin Resistance in Acinetobacter Species Isolated from Patients in Kuwait Hospitals. J. Chemother. 2011, 23, 13–16. [Google Scholar] [CrossRef]
  164. Al-Sweih, N.A.; Al-Hubail, M.; Rotimi, V.O. Three Distinct Clones of Carbapenem-Resistant Acinetobacter Baumannii with High Diversity of Carbapenemases Isolated from Patients in Two Hospitals in Kuwait. J. Infect. Public Health 2012, 5, 102–108. [Google Scholar] [CrossRef] [Green Version]
  165. Aly, M.; Tayeb, H.T.; Al Johani, S.M.; Alyamani, E.J.; Aldughaishem, F.; Alabdulkarim, I.; Balkhy, H.H. Genetic Diversity of OXA-51-like Genes among Multidrug-Resistant Acinetobacter Baumannii in Riyadh, Saudi Arabia. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33, 1223–1228. [Google Scholar] [CrossRef] [PubMed]
  166. Aly, M.M.; Abu Alsoud, N.M.; Elrobh, M.S.; Al Johani, S.M.; Balkhy, H.H. High Prevalence of the PER-1 Gene among Carbapenem-Resistant Acinetobacter Baumannii in Riyadh, Saudi Arabia. Eur. J. Clin. Microbiol. Infect. Dis. 2016, 35, 1759–1766. [Google Scholar] [CrossRef] [PubMed]
  167. Azeez, Z.F.; Hatite Al-Daraghi, W.A. Isolation of Lytic Acinetobacter Baumannii Phage VB_Acib_C_A10 from Iraq Pond Waters and Comparing Its Antibacterial Effect with Cefotaxime Antibiotic. Int. J. Pharm. Qual. Assur. 2019, 10, 84–89. [Google Scholar] [CrossRef]
  168. Bakour, S.; Alsharapy, S.A.; Touati, A.; Rolain, J.-M. Characterization of Acinetobacter Baumannii Clinical Isolates Carrying Bla OXA-23 Carbapenemase and 16S RRNA Methylase ArmA Genes in Yemen. Microb. Drug Resist. 2014, 20, 604–609. [Google Scholar] [CrossRef] [PubMed]
  169. Batarseh, A.; Al-Sarhan, A.; Maayteh, M.; Al-Khatirei, S.; Alarmouti, M. Antibiogram of Multidrug Resistant Acinetobacter Baumannii Isolated from Clinical Specimens at King Hussein Medical Centre, Jordan: A Retrospective Analysis. Easter Mediterr. Health J. 2015, 21, 828–834. [Google Scholar] [CrossRef]
  170. Conlon, J.M.; Ahmed, E.; Pal, T.; Sonnevend, A. Potent and Rapid Bactericidal Action of Alyteserin-1c and Its [E4K] Analog against Multidrug-Resistant Strains of Acinetobacter Baumannii. Peptides 2010, 31, 1806–1810. [Google Scholar] [CrossRef] [PubMed]
  171. Conlon, J.M.; Mechkarska, M.; Arafat, K.; Attoub, S.; Sonnevend, A. Analogues of the Frog Skin Peptide Alyteserin-2a with Enhanced Antimicrobial Activities against Gram-Negative Bacteria: ALYTESERIN-2: STRUCTURE-ACTIVITY. J. Pept. Sci. 2012, 18, 270–275. [Google Scholar] [CrossRef]
  172. Conlon, J.M.; Sonnevend, A.; Pál, T.; Vila-Farrés, X. Efficacy of Six Frog Skin-Derived Antimicrobial Peptides against Colistin-Resistant Strains of the Acinetobacter Baumannii Group. Int. J. Antimicrob. Agents 2012, 39, 317–320. [Google Scholar] [CrossRef] [PubMed]
  173. El-Ageery, S.M.; Abo-Shadi, M.A.; Elgendy, A.M.; Alghaithy, A.A.; Kandeel, A.Y. The Role of Health Care Workers and Environment on Transmission of Methicillin–Resistant Staphylococcus Aureus among Patients in a Medical Intensive Care Unit in a Saudi Hospital. Appl. Microbiol. 2011, 5, 1–8. [Google Scholar]
  174. Ghaima, K.; Saadedin, S.; Jassim, K. Prevalence of BlaOXA like Carbapenemase Genes in Multidrug Resistant Acinetobacter Baumannii Isolated from Burns and Wounds in Baghdad Hospitals. Res. J. Pharm. Biol. Chem. Sci. 2016, 7, 1347. [Google Scholar]
  175. Gowda, K.L.; Marie, M.A.M.; Al-Sheikh, Y.A.; John, J.; Gopalkrishnan, S.; Shashidhar, P.C.; Dabwan, K.H.M. A 6-Year Surveillance of Antimicrobial Resistance Patterns of Acinetobacter Baumannii Bacteremia Isolates from a Tertiary Care Hospital in Saudi Arabia during 2005–2010. Libyan J. Med. 2014, 9, 24039. [Google Scholar] [CrossRef]
  176. Hoang, V.-T.; Dao, T.-L.; Ly, T.D.A.; Gouriet, F.; Hadjadj, L.; Belhouchat, K.; Chaht, K.L.; Yezli, S.; Alotaibi, B.; Raoult, D.; et al. Acquisition of Multidrug-Resistant Bacteria and Encoding Genes among French Pilgrims during the 2017 and 2018 Hajj. Eur. J. Clin. Microbiol. Infect. Dis. 2021, 40, 1199–1207. [Google Scholar] [CrossRef]
  177. Kareem, S.M.; Al-Kadmy, I.M.S.; Al-Kaabi, M.H.; Aziz, S.N.; Ahmad, M. Acinetobacter Baumannii Virulence Is Enhanced by the Combined Presence of Virulence Factors Genes Phospholipase C (PlcN) and Elastase (LasB). Microb. Pathog. 2017, 110, 568–572. [Google Scholar] [CrossRef] [PubMed]
  178. Kusradze, I.; Diene, S.M.; Goderdzishvili, M.; Rolain, J.-M. Molecular Detection of OXA Carbapenemase Genes in Multidrug-Resistant Acinetobacter Baumannii Isolates from Iraq and Georgia. Int. J. Antimicrob. Agents 2011, 38, 164–168. [Google Scholar] [CrossRef] [Green Version]
  179. Lopes, B.S.; Al-Agamy, M.H.; Ismail, M.A.; Shibl, A.M.; Al-Qahtani, A.A.; Al-Ahdal, M.N.; Forbes, K.J. The Transferability of BlaOXA-23 Gene in Multidrug-Resistant Acinetobacter Baumannii Isolates from Saudi Arabia and Egypt. Int. J. Med. Microbiol. 2015, 305, 581–588. [Google Scholar] [CrossRef]
  180. Mahdi, L.; Mahdi, N.; Al-kakei, S.; Musafer, H.; Al-Joofy, I.; Essa, R.; Zwain, L.; Salman, I.; Mater, H.; Al-Alak, S.; et al. Treatment Strategy by Lactoperoxidase and Lactoferrin Combination: Immunomodulatory and Antibacterial Activity against Multidrug-Resistant Acinetobacter Baumannii. Microb. Pathog. 2018, 114, 147–152. [Google Scholar] [CrossRef] [PubMed]
  181. Mazi, W.; Alshammari, F.; Yu, J.; Saeed, A. A Descriptive Analysis of PVL-Positive Multidrug-Resistant Staphylococcus Aureus in Hospital-Associated Infections in Saudi Arabia. Bioinformation 2020, 16, 586–593. [Google Scholar] [CrossRef]
  182. Mechkarska, M.; Prajeep, M.; Radosavljevic, G.D.; Jovanovic, I.P.; Baloushi, A.A.; Sonnevend, A.; Lukic, M.L.; Conlon, J.M. An Analog of the Host-Defense Peptide Hymenochirin-1B with Potent Broad-Spectrum Activity against Multidrug-Resistant Bacteria and Immunomodulatory Properties. Peptides 2013, 50, 153–159. [Google Scholar] [CrossRef] [PubMed]
  183. Muslim, S.N.; Al-Kadmy, I.M.S.; Auda, I.G.; Ali, A.N.M.; Al-Jubori, S.S. A Novel Genetic Determination of a Lectin Gene in Iraqi Acinetobacter Baumannii Isolates and Use of Purified Lectin as an Antibiofilm Agent. J. AOAC Int. 2018, 101, 1623–1630. [Google Scholar] [CrossRef] [PubMed]
  184. Nasser, K.; Mustafa, A.S.; Khan, M.W.; Purohit, P.; Al-Obaid, I.; Dhar, R.; Al-Fouzan, W. Draft Genome Sequences of Six Multidrug-Resistant Clinical Strains of Acinetobacter Baumannii, Isolated at Two Major Hospitals in Kuwait. Genome Announc. 2018, 6, e00264-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  185. Obeidat, N.; Jawdat, F.; Al-Bakri, A.G.; Shehabi, A.A. Major Biologic Characteristics of Acinetobacter Baumannii Isolates from Hospital Environmental and Patients’ Respiratory Tract Sources. Am. J. Infect. Control 2014, 42, 401–404. [Google Scholar] [CrossRef]
  186. Qasim, Z.J.; Kadhim, H.S.; Abdulamir, A.S. Identification of Antibiotic Resistance Genes in Multi-Drug Resistant Acinetobacter Baumannii Clinical Isolates of Iraqi Patients (Zq Strains), Using Whole-Genome Sequencing. Int. J. Pharm. Qual. Assur. 2019, 10, 670–680. [Google Scholar] [CrossRef]
  187. Rabaan, A.A.; Saunar, J.V.; Bazzi, A.M.; Raslan, W.F.; Taylor, D.R.; Al-Tawfiq, J.A. Epidemiology and Detection of Acinetobacter Using Conventional Culture and In-House Developed PCR Based Methods. J. Infect. Public Health 2017, 10, 124–128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  188. Radhi, S.H.; Al-Charrakh, A.H. Occurrence of MBLs and Carbapenemases among MDR and XDR Acinetobacter Baumannii Isolated from Hospitals in Iraq. Ind. J. Publ. Health Res. Dev. 2019, 10, 668. [Google Scholar] [CrossRef]
  189. Ridha, D.; Ali, M.; Jassim, K. Occurrence of Metallo-β-Lactamase Genes among Acinetobacter Baumannii Isolated from Different Clinical Samples. J. Pure Appl. Microbiol. 2019, 13, 1111–1119. [Google Scholar] [CrossRef] [Green Version]
  190. Salahuddin, N.; Amer, L.; Joseph, M.; El Hazmi, A.; Hawa, H.; Maghrabi, K. Determinants of Deescalation Failure in Critically Ill Patients with Sepsis: A Prospective Cohort Study. Crit. Care Res. Pract. 2016, 2016, 6794861. [Google Scholar] [CrossRef] [Green Version]
  191. Samrah, S.; Bashtawi, Y.; Hayajneh, W.; Almomani, B.; Momany, S.; Khader, Y. Impact of Colistin-Initiation Delay on Mortality of Ventilator-Associated Pneumonia Caused by A. Baumannii. J. Infect. Dev. Ctries 2016, 10, 1129–1134. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  192. Senok, A.; Garaween, G.; Raji, A.; Khubnani, H.; Kim Sing, G.; Shibl, A. Genetic Relatedness of Clinical and Environmental Acinetobacter Baumanii Isolates from an Intensive Care Unit Outbreak. J. Infect. Dev. Ctries 2015, 9, 665–669. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  193. Shah, M.W.; Yasir, M.; Farman, M.; Jiman-Fatani, A.A.; Almasaudi, S.B.; Alawi, M.; El-Hossary, D.; Azhar, E.I. Antimicrobial Susceptibility and Molecular Characterization of Clinical Strains of Acinetobacter Baumannii in Western Saudi Arabia. Microb. Drug Resist. 2019, 25, 1297–1305. [Google Scholar] [CrossRef]
  194. Somily, A.M. Comparison of E-Test and Disc Diffusion Methods for the in Vitro Evaluation of the Antimicrobial Activity of Colistin in Multi-Drug Resistant Gram-Negative Bacilli. Saudi Med. J. 2010, 5, 507–511. [Google Scholar]
  195. Somily, A.M.; Absar, M.M.; Arshad, M.Z.; Al Aska, A.I.; Shakoor, Z.A.; Fatani, A.J.; Siddiqui, Y.M.; Murray, T.S. Antimicrobial Susceptibility Patterns of Multidrug-Resistant Pseudomonas Aeruginosa and Acinetobacter Baumannii against Carbapenems, Colistin, and Tigecycline. Saudi Med. J. 2012, 33, 750–755. [Google Scholar]
  196. Vijayakumar, R.; Sandle, T.; Al-Aboody, M.S.; AlFonaisan, M.K.; Alturaiki, W.; Mickymaray, S.; Premanathan, M.; Alsagaby, S.A. Distribution of Biocide Resistant Genes and Biocides Susceptibility in Multidrug-Resistant Klebsiella Pneumoniae, Pseudomonas Aeruginosa and Acinetobacter Baumannii—A First Report from the Kingdom of Saudi Arabia. J. Infect. Public Health 2018, 11, 812–816. [Google Scholar] [CrossRef]
  197. Wahaab, I.T.A.; Almaroof, S.Q.M.; Yaseen, Z.T. Causative Microorganisms and Antibiotics Susceptibility in Neonatal Sepsis at Neonatal Intensive Care Unit: A Longitudinal Study from Diyala Governorate in Iraq. Indian J. Forensic Med. Toxicol. 2021, 15, 101–110. [Google Scholar] [CrossRef]
  198. Wibberg, D.; Salto, I.P.; Eikmeyer, F.G.; Maus, I.; Winkler, A.; Nordmann, P.; Pühler, A.; Poirel, L.; Schlüter, A. Complete Genome Sequencing of Acinetobacter Baumannii Strain K50 Discloses the Large Conjugative Plasmid PK50a Encoding Carbapenemase OXA-23 and Extended-Spectrum β-Lactamase GES-11. Antimicrob. Agents Chemother. 2018, 62, e00212-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  199. Yasir, M.; Shah, M.W.; Jiman-Fatani, A.A.; Almasaudi, S.B.; Ahmad, H.; Alawi, M.; Azhar, E.I. Draft Genome Sequence of a Clinical Acinetobacter Baumannii Isolate of New Sequence Type ST1688 from Saudi Arabia. J. Glob. Antimicrob. Resist. 2019, 18, 151–152. [Google Scholar] [CrossRef]
  200. Al-Agamy, M.H.; El-Mahdy, T.S.; Radwan, H.H.; Poirel, L. Cooccurrence of NDM-1, ESBL, RmtC, AAC(6′)-Ib, and QnrB in Clonally Related Klebsiella Pneumoniae Isolates Together with Coexistence of CMY-4 and AAC(6′)-Ib in Enterobacter Cloacae Isolates from Saudi Arabia. BioMed Res. Int. 2019, 2019, 6736897. [Google Scholar] [CrossRef] [Green Version]
  201. Alatoom, A.; Sartawi, M.; Lawlor, K.; AbdelWareth, L.; Thomsen, J.; Nusair, A.; Mirza, I. Persistent Candidemia despite Appropriate Fungal Therapy: First Case of Candida Auris from the United Arab Emirates. Int. J. Infect. Dis. 2018, 70, 36–37. [Google Scholar] [CrossRef] [Green Version]
  202. Al-Baloushi, A.E.; Pál, T.; Ghazawi, A.; Sonnevend, A. Genetic Support of Carbapenemases in Double Carbapenemase Producer Klebsiella Pneumoniae Isolated in the Arabian Peninsula. Acta Microbiol. Immunol. Hung. 2018, 65, 135–150. [Google Scholar] [CrossRef] [Green Version]
  203. Alghoribi, M.F.; Binkhamis, K.; Alswaji, A.A.; Alhijji, A.; Alsharidi, A.; Balkhy, H.H.; Doumith, M.; Somily, A. Genomic Analysis of the First KPC-Producing Klebsiella Pneumoniae Isolated from a Patient in Riyadh: A New Public Health Concern in Saudi Arabia. J. Infect. Public Health 2020, 13, 647–650. [Google Scholar] [CrossRef]
  204. Algowaihi, R.; Ashgar, S.; Sirag, B.; Shalam, S.; Nassir, A.; Ahmed, A. Draft Genome Sequence of a Multidrug-Resistant Klebsiella Pneumoniae Strain Isolated from King Abdullah Medical City, Makkah, Saudi Arabia. Genome Announc. 2016, 4, e00375-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  205. AL-Khikani, F.H.O.; Abadi, R.M.; Ayit, A.S. Emerging Carbapenemase Klebsiella Oxytoca with Multidrug Resistance Implicated in Urinary Tract Infection. Biomed. Biotechnol. Res. J. 2020, 2, 148–151. [Google Scholar]
  206. AL-Muqdadi, B.M.J.; AL-Saadi, B.Q.H. Detection Of Arma Gene, Kpc Enzyme And Molecular Typing Of K. Pneumoniae Clinical Isolate From Public Hospitals In Baghdad City, Iraq. Biochem. Cell. Arch. 2020, 20, 2101–2105. [Google Scholar]
  207. Al-Qahtani, A.A.; Al-Agamy, M.H.; Ali, M.S.; Al-Ahdal, M.N.; Aljohi, M.A.; Shibl, A.M. Characterization of Extended-Spectrum Beta-Lactamase-Producing Klebsiella Pneumoniae from Riyadh, Saudi Arabia. J. Chemother. 2014, 26, 139–145. [Google Scholar] [CrossRef]
  208. Alsanie, W.F. Molecular Diversity and Profile Analysis of Virulence-Associated Genes in Some Klebsiella Pneumoniae Isolates. Pract. Lab. Med. 2020, 19, e00152. [Google Scholar] [CrossRef] [PubMed]
  209. Alyousef, A.A.; Khazaal, S.S.; Ali, A.N.M.; Hussein, N.H.; Hussein, S.M.A. Detection of Prevalent Mechanism of Extended Spectrum β-Lactamases, Metallo β-Lactamases, and AmpC β Lactamases-Producing Klebsiella Pneumoniae in the Tertiary Care Hospital. Rev. Med. Microbiol. 2017, 28, 133–139. [Google Scholar] [CrossRef]
  210. Salman, R.A.; Ghaima, K.K. Prevalence of ESBL genes in ESBL producing Klebsiella pneumoniae isolated from patients with urinary tract infections in Baghdad, Iraq. Biosci. Res. 2018, 15, 2049–2059. [Google Scholar]
  211. El Nekidy, W.S.; Mooty, M.Y.; Attallah, N.; Cardona, L.; Bonilla, M.F.; Ghazi, I.M. Successful Treatment of Multidrug Resistant Klebsiella Pneumoniae Using Dual Carbapenem Regimen in Immunocompromised Patient. IDCases 2017, 9, 53–55. [Google Scholar] [CrossRef]
  212. Hassan, M.I.; Alkharsah, K.R.; Alzahrani, A.J.; Obeid, O.E.; Khamis, A.H.; Diab, A. Detection of Extended Spectrum Beta-Lactamases-Producing Isolates and Effect of AmpC Overlapping. J. Infect. Dev. Ctries 2013, 7, 618–629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  213. Lagha, R.; Ben Abdallah, F.; ALKhammash, A.A.H.; Amor, N.; Hassan, M.M.; Mabrouk, I.; Alhomrani, M.; Gaber, A. Molecular Characterization of Multidrug Resistant Klebsiella Pneumoniae Clinical Isolates Recovered from King Abdulaziz Specialist Hospital at Taif City, Saudi Arabia. J. Infect. Public Health 2021, 14, 143–151. [Google Scholar] [CrossRef]
  214. Poirel, L.; Al Maskari, Z.; Al Rashdi, F.; Bernabeu, S.; Nordmann, P. NDM-1-Producing Klebsiella Pneumoniae Isolated in the Sultanate of Oman. J. Antimicrob. Chemother. 2011, 66, 304–306. [Google Scholar] [CrossRef]
  215. Saaid Tuwaij, N.S.; Al-khilkhali, H.J.B.; Mohsen, H.M. Prevalence of SUL(1,2), GYR(A, B) and OXA Genes among Multidrug Resistance Klebsiella Pneumoniae Isolates Recovered from Women Suffering Urinary Tract Infection. Int. J. Res. Pharm. Sci. 2020, 11, 2424–2432. [Google Scholar] [CrossRef]
  216. Shibl, A.; Al-Agamy, M.; Memish, Z.; Senok, A.; Khader, S.A.; Assiri, A. The Emergence of OXA-48- and NDM-1-Positive Klebsiella Pneumoniae in Riyadh, Saudi Arabia. Int. J. Infect. Dis. 2013, 17, e1130–e1133. [Google Scholar] [CrossRef] [Green Version]
  217. Shlash, A.A.A.; Tuwaij, N.S.S. Molecular Dissemination Of Ambler Class A And C Β- Lactamase Genes Among Ceftriaxone Resistant Klebsiella Pneumoniae Infection In Najaf City, Iraq. Biochem. Cell. Arch. 2018, 18, 2511–2522. [Google Scholar]
  218. Vali, L.; Dashti, A.A.; Jadaon, M.M.; El-Shazly, S. The Emergence of Plasmid Mediated Quinolone Resistance QnrA2 in Extended Spectrum β-Lactamase Producing Klebsiella Pneumoniae in the Middle East. DARU J. Pharm Sci. 2015, 23, 34. [Google Scholar] [CrossRef] [Green Version]
  219. uz Zaman, T.; Alrodayyan, M.; Albladi, M.; Aldrees, M.; Siddique, M.I.; Aljohani, S.; Balkhy, H.H. Clonal Diversity and Genetic Profiling of Antibiotic Resistance among Multidrug/Carbapenem-Resistant Klebsiella Pneumoniae Isolates from a Tertiary Care Hospital in Saudi Arabia. BMC Infect. Dis. 2018, 18, 205. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  220. uz Zaman, T.; Aldrees, M.; Al Johani, S.M.; Alrodayyan, M.; Aldughashem, F.A.; Balkhy, H.H. Multi-Drug Carbapenem-Resistant Klebsiella Pneumoniae Infection Carrying the OXA-48 Gene and Showing Variations in Outer Membrane Protein 36 Causing an Outbreak in a Tertiary Care Hospital in Riyadh, Saudi Arabia. Int. J. Infect. Dis. 2014, 28, 186–192. [Google Scholar] [CrossRef] [Green Version]
  221. AbdulWahab, A.; Taj-Aldeen, S.J.; Ibrahim, E.B.; Hussain, S.; Muhammed, R.; Ahmed, I.; Abdeen, Y.; Sadek, O.; Abu-Madi, M. Genetic Relatedness and Host Specificity of Pseudomonas Aeruginosa Isolates from Cystic Fibrosis and Non-Cystic Fibrosis Patients. Infect. Drug Resist. 2014, 7, 309. [Google Scholar] [CrossRef] [Green Version]
  222. AbdulWahab, A.; Zahraldin, K.; Ahmed, M.A.; Jarir, S.A.; Muneer, M.; Mohamed, S.F.; Hamid, J.M.; Hassan, A.A.; Ibrahim, E.B. The Emergence of Multidrug-Resistant Pseudomonas Aeruginosa in Cystic Fibrosis Patients on Inhaled Antibiotics. Lung India 2017, 34, 527. [Google Scholar] [CrossRef]
  223. Ahmad, I.; Irfan, S.; Abohashrh, M.; Wahab, S.; Abullais, S.S.; Javali, M.A.; Nisar, N.; Alam, M.M.; Srivastava, S.; Saleem, M.; et al. Inhibitory Effect of Nepeta Deflersiana on Climax Bacterial Community Isolated from the Oral Plaque of Patients with Periodontal Disease. Molecules 2021, 26, 202. [Google Scholar] [CrossRef] [PubMed]
  224. Alamri, A.M.; Alfifi, S.; Aljehani, Y.; Alnimr, A. Whole Genome Sequencing of Ceftolozane-Tazobactam and Ceftazidime-Avibactam Resistant Pseudomonas Aeruginosa Isolated from a Blood Stream Infection Reveals VEB and Chromosomal Metallo-Beta Lactamases as Genetic Determinants: A Case Report. Infect. Drug Resist. 2020, 13, 4215–4222. [Google Scholar] [CrossRef]
  225. Al-Delaimi, M.S.; Yacoob Aldosky, H.Y. Amending the Efficiency of Antimicrobials against Multidrug-Resistant Pseudomonas Aeruginosa by Low-Frequency Magnetic Fields. Bull. Exp. Biol. Med. 2020, 170, 35–39. [Google Scholar] [CrossRef]
  226. Alhamdani, R.J.M.; Al-Luaibi, Y.Y.Y. Detection of exoA, nan1 genes, the biofilm production with the effect of Oyster shell and two plant extracts on Pseudomonas aeroginosa isolated from burn’ patient and their surrounding environment. Syst. Rev. Pharm. 2020, 11, 11. [Google Scholar]
  227. Al-Zahrani, I.A.; Al-Ahmadi, B.M. Dissemination of VIM-Producing Pseudomonas Aeruginosa Associated with High-Risk Clone ST654 in a Tertiary and Quaternary Hospital in Makkah, Saudi Arabia. J. Chemother. 2021, 33, 12–20. [Google Scholar] [CrossRef]
  228. Asghar, A. Antimicrobial Susceptibility and Metallo-β-Lactamase Production among Pseudomonas Aeruginosa Isolated from Makkah Hospitals. Pak. J. Med. Sci. 2012, 28, 781–786. [Google Scholar]
  229. Behbahani, M.R.; Keshavarzi, A.; Pirbonyeh, N.; Javanmardi, F.; Khoob, F.; Emami, A. Plasmid- related β-Lactamase Genes in Pseudomonas Aeruginosa Isolates: A Molecular Study in Burn Patients. J. Med. Microbiol. 2019, 68, 1740–1746. [Google Scholar]
  230. Bourghli, A.; Boissiere, L.; Obeid, I. Thoracic Kyphotic Deformity Secondary to Old Pseudomonas Aeruginosa Spondylodiscitis in an Immunocompromised Patient With Persistent Infection Foci—A Case Report. Int. J. Spine Surg. 2019, 13, 392–398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  231. Hassan, S.; Najati, A.; Abass, K. Isolation and Identification of Multi-Drug Resistant “Pseudomonas Aeruginosa” from Burn Wound Infection in Kirkuk City, Iraq. Eurasian J. Biosci. 2019, 13, 1045–1050. [Google Scholar]
  232. Hassan, S.A.; Shobrak, M.Y. Prevalence and Antimicrobial Resistance Characteristics of Gram-Negative Bacteria Associated with Wild Animals Presenting at Live Animal Market, Taif, Western Saudi Arabia. Antimicrob. Resist. 2014, 8, 273–282. [Google Scholar]
  233. Jaaffar, A.I. Detection of BlaIMP Gene among Pseudomonas Aeruginosa Isolated from Different Clinical Samples. Drug Invent. Today 2019, 12, 5. [Google Scholar]
  234. Khan, R.; Al-Dorzi, H.M.; Tamim, H.M.; Rishu, A.H.; Balkhy, H.; El-Saed, A.; Arabi, Y.M. The Impact of Onset Time on the Isolated Pathogens and Outcomes in Ventilator Associated Pneumonia. J. Infect. Public Health 2016, 9, 161–171. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  235. Khan, M.A.; Faiz, A. Antimicrobial Resistance Patterns of Pseudomonas Aeruginosa in Tertiary Care Hospitals of Makkah and Jeddah. Ann. Saudi Med. 2016, 36, 23–28. [Google Scholar] [CrossRef] [Green Version]
  236. Mahdi, L.H.; Jabbar, H.S.; Auda, I.G. Antibacterial Immunomodulatory and Antibiofilm Triple Effect of Salivaricin LHM against Pseudomonas Aeruginosa Urinary Tract Infection Model. Int. J. Biol. Macromol. 2019, 134, 1132–1144. [Google Scholar] [CrossRef] [PubMed]
  237. Nasser, M.; Gayen, S.; Kharat, A.S. Prevalence of β-Lactamase and Antibiotic-Resistant Pseudomonas Aeruginosa in the Arab Region. J. Glob. Antimicrob. Resist. 2020, 22, 152–160. [Google Scholar] [CrossRef]
  238. Nasser, M.; Kharat, A.S. Phenotypic Demonstration of SS-Lactamase (ESßLs, MßLs, and Amp-C) among MDR Pseudomonas Aeruginosa Isolates Obtained From Burn Wound Infected in Yemen. J. Appl. Biol. Biotechnol. 2019, 7, 31–34. [Google Scholar] [CrossRef] [Green Version]
  239. Sid Ahmed, M.A.; Khan, F.A.; Sultan, A.A.; Söderquist, B.; Ibrahim, E.B.; Jass, J.; Omrani, A.S. β-Lactamase-Mediated Resistance in MDR-Pseudomonas Aeruginosa from Qatar. Antimicrob. Resist. Infect. Control 2020, 9, 170. [Google Scholar] [CrossRef] [PubMed]
  240. Tarazi, Y.H.; Abu-Basha, E.; Ismail, Z.B.; Al-Jawasreh, S.I. Antimicrobial Susceptibility of Multidrug-Resistant Pseudomonas Aeruginosa Isolated from Drinking Water and Hospitalized Patients in Jordan. Acta Trop. 2021, 217, 105859. [Google Scholar] [CrossRef]
  241. Zikri, A.; El Masri, K. Use of Ceftolozane/Tazobactam for the Treatment of Multidrug-Resistant Pseudomonas Aeruginosa Pneumonia in a Pediatric Patient with Combined Immunodeficiency (CID): A Case Report from a Tertiary Hospital in Saudi Arabia. Antibiotics 2019, 8, 67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  242. Abulreesh, H.H.; Organji, S.R.; Osman, G.E.H.; Elbanna, K.; Almalki, M.H.K.; Ahmad, I. Prevalence of Antibiotic Resistance and Virulence Factors Encoding Genes in Clinical Staphylococcus Aureus Isolates in Saudi Arabia. Clin. Epidemiol. Glob. Health 2017, 5, 196–202. [Google Scholar] [CrossRef] [Green Version]
  243. Abulreesh, H.H.; Organji, S.R. The Prevalence of Multidrug-Resistant Staphylococci in Food and the Environment of Makkah, Saudi Arabia. Res. J. Microbiol. 2011, 6, 510–523. [Google Scholar] [CrossRef] [Green Version]
  244. Al Zebary, M.K.; Yousif, S.Y.; Assafi, M.S. The Prevalence, Molecular Characterization and Antimicrobial Susceptibility of S. Aureus Isolated from Impetigo Cases in Duhok, Iraq. Open Dermatol. J. 2017, 11, 22–29. [Google Scholar] [CrossRef] [Green Version]
  245. AlFouzan, W.; Al-Haddad, A.; Udo, E.; Mathew, B.; Dhar, R. Frequency and Clinical Association of Panton-Valentine Leukocidin-Positive Staphylococcus Aureus Isolates: A Study from Kuwait. Med Princ. Pract. 2013, 22, 245–249. [Google Scholar] [CrossRef]
  246. Alghizzi, M.J.; Alansari, M.; Shami, A. The Prevalence of Staphylococcus Aureus and Methicillin Resistant Staphylococcus Aureus in Processed Food Samples in Riyadh, Saudi Arabia. J. Pure Appl. Microbiol. 2021, 15, 91–99. [Google Scholar] [CrossRef]
  247. Al-Zoubi, M.S.; Al-Tayyar, I.A.; Hussein, E.; Jabali, A.A.; Khudairat, S. Antimicrobial Susceptibility Pattern of Staphylococcus Aureus Isolated from Clinical Specimens in Northern Area of Jordan. Iran. J. Microbiol. 2015, 7, 265. [Google Scholar]
  248. Hamid, M.E. Prevalence of Bacterial Pathogens in Aseer Region, Kingdom of Saudi Arabia: Emphasis on Antimicrobial Susceptibility of Staphylococcus Aureus. Oman Med. J. 2011, 26, 368–369. [Google Scholar] [CrossRef]
  249. Ismail, Z.B. Molecular Characteristics, Antibiogram and Prevalence of Multi-Drug Resistant Staphylococcus Aureus (MDRSA) Isolated from Milk Obtained from Culled Dairy Cows and from Cows with Acute Clinical Mastitis. Asian Pac. J. Trop. Biomed. 2017, 7, 694–697. [Google Scholar] [CrossRef]
  250. Kanaan, M.H.G. Antibacterial Effect of Ozonated Water against Methicillin-Resistant Staphylococcus Aureus Contaminating Chicken Meat in Wasit Province, Iraq. Vet. World 2018, 11, 1445–1453. [Google Scholar] [CrossRef]
  251. Kanaan, M.H.G.; Al-Isawi, A.J.O. Prevalence Of Methicillin Or Multiple Drug-Resistant Staphylococcus Aureus In Cattle Meat Marketed In Wasit Province. Biochem. Cell. Arch. 2019, 19, 495–502. [Google Scholar]
  252. Obaidat, M.M.; Bani Salman, A.E.; Lafi, S.Q. Prevalence of Staphylococcus Aureus in Imported Fish and Correlations between Antibiotic Resistance and Enterotoxigenicity. J. Food Prot. 2015, 78, 1999–2005. [Google Scholar] [CrossRef] [PubMed]
  253. Vellappally, S.; Divakar, D.D.; Al Kheraif, A.A.; Ramakrishnaiah, R.; Alqahtani, A.; Dalati, M.H.N.; Anil, S.; Khan, A.A.; Harikrishna Varma, P.R. Occurrence of Vancomycin-Resistant Staphylococcus Aureus in the Oral Cavity of Patients with Dental Caries. Acta Microbiol. Et Immunol. Hung. 2017, 64, 343–351. [Google Scholar] [CrossRef] [Green Version]
  254. Abdalla, N.M.; Osman, A.A.; Haimour, W.O.; Sarhan, M.A.; Mohammed, M.N.; Zyad, E.M.; Al-ghtani, A.M. Antimicrobial Susceptibility Pattern in Nosocomial Infections Caused by Acinetobacter Species in Asir Region, Saudi Arabia. Pak. J. Biol. Sci. 2013, 16, 275–280. [Google Scholar] [CrossRef]
  255. Balkhy, H.H.; Bawazeer, M.S.; Kattan, R.F.; Tamim, H.M.; Johani, S.M.; Aldughashem, F.A.; Al Alem, H.A.; Adlan, A.; Herwaldt, L.A. Epidemiology of Acinetobacter spp.-Associated Healthcare Infections and Colonization among Children at a Tertiary-Care Hospital in Saud Arabia: A 6-Year Retrospective Cohort Study. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31, 2645–2651. [Google Scholar] [CrossRef] [PubMed]
  256. Somily, A.M.; Al-Khattaf, A.S.; Kambal, A.M. Antimicrobial Activity of Tigecycline against Bacterial Isolates from Intensive Care Units in a Teaching Hospital in Central Saudi Arabia. Saudi Med. J. 2010, 31, 18–24. [Google Scholar] [PubMed]
  257. Al-Kharousi, Z.S.; Guizani, N.; Al-Sadi, A.M.; Al-Bulushi, I.M. Antibiotic Resistance of Enterobacteriaceae Isolated from Fresh Fruits and Vegetables and Characterization of Their AmpC β-Lactamases. J. Food Prot. 2019, 82, 1857–1863. [Google Scholar] [CrossRef]
  258. Alkofide, H.; Alhammad, A.M.; Alruwaili, A.; Aldemerdash, A.; Almangour, T.A.; Alsuwayegh, A.; Almoqbel, D.; Albati, A.; Alsaud, A.; Enani, M. Multidrug-Resistant and Extensively Drug-Resistant Enterobacteriaceae: Prevalence, Treatments, and Outcomes—A Retrospective Cohort Study. Infect. Drug Resist. 2020, 13, 4653–4662. [Google Scholar] [CrossRef] [PubMed]
  259. Jamal, W.Y.; Albert, M.J.; Rotimi, V.O. High Prevalence of New Delhi Metallo-β-Lactamase-1 (NDM-1) Producers among Carbapenem-Resistant Enterobacteriaceae in Kuwait. PLoS ONE 2016, 11, e0152638. [Google Scholar] [CrossRef] [Green Version]
  260. Al-Mayahi, F.S.A.; Ali, R.H. Preliminary study of emergence MDR of Providencia spp. isolates producing ESBL, AmpC and MBL among patients with RTI and in wastewater in Al-Diwaniya city, Iraq. Biochem. Cell. Arch. 2018, 18, 12. [Google Scholar]
  261. Ayyal Al-Gburi, N.M. Isolation and Molecular Identification and Antimicrobial Susceptibility of Providencia spp. from Raw Cow’s Milk in Baghdad, Iraq. Vet. Med. Int. 2020, 2020, 8874747. [Google Scholar] [CrossRef]
  262. Al-Lahham, A.; Qayyas, J.A. The Impact of the 7-Valent Pneumococcal Conjugate Vaccine on Nasopharyngeal Carriage of Streptococcus Pneumoniae in Infants of Ajlun Governorate in Jordan. Jordan J. Biol. Sci. 2018, 11, 8. [Google Scholar]
  263. Al-Mazrou, K.A.; Shibl, A.M.; Kandeil, W.; Pirçon, J.-Y.; Marano, C. A Prospective, Observational, Epidemiological Evaluation of the Aetiology and Antimicrobial Susceptibility of Acute Otitis Media in Saudi Children Younger than 5 Years of Age. J. Epidemiol. Glob. Health 2014, 4, 231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  264. Almazrou, Y.; Shibl, A.M.; Alkhlaif, R.; Pirçon, J.-Y.; Anis, S.; Kandeil, W.; Hausdorff, W.P. Epidemiology of Invasive Pneumococcal Disease in Saudi Arabian Children Younger than 5 Years of Age. J. Epidemiol. Glob. Health 2015, 6, 95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  265. Alnimr, A.M.; Farhat, M. Phenotypic and Molecular Study of Pneumococci Causing Respiratory Tract Infections: A 3-Year Prospective Cohort. Saudi Med. J. 2017, 38, 350–358. [Google Scholar] [CrossRef]
  266. Al-Sa’ady, A.T.; Hussein, F.H. Nanomedical Applications of Titanium Dioxide Nanoparticles as Antibacterial Agent against Multi-Drug Resistant Streptococcus Pneumoniae. Syst. Rev. Pharm. 2020, 11, 11. [Google Scholar]
  267. Elshafie, S.; Taj-Aldeen, S.J. Emerging Resistant Serotypes of Invasive Streptococcus Pneumoniae. Infect. Drug Resist. 2016, 9, 153–160. [Google Scholar] [CrossRef] [Green Version]
  268. Sallam, M. Trends in Antimicrobial Drug Resistance of Streptococcus Pneumoniae Isolates at Jordan University Hospital (2000–2018). Antibiotics 2019, 8, 41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  269. Shin, J.; Baek, J.Y.; Kim, S.H.; Song, J.-H.; Ko, K.S. Predominance of ST320 among Streptococcus Pneumoniae Serotype 19A Isolates from 10 Asian Countries. J. Antimicrob. Chemother. 2011, 66, 1001–1004. [Google Scholar] [CrossRef] [PubMed]
  270. Al Baidani, A.; Elshoni, W.; Shawa, T. Antibiotic Susceptibility Pattern of Methicillin-Resistant Staphylococcus Aureus in Three Hospitals at Hodeidah City, Yemen. Glob. J. Pharmacol. 2011, 55, 105–111. [Google Scholar]
  271. Albarrag, A.; Shami, A.; Almutairi, A.; Alsudairi, S.; Aldakeel, S.; Al-Amodi, A. Prevalence and Molecular Genetics of Methicillin-Resistant Staphylococcus Aureus Colonization in Nursing Homes in Saudi Arabia. Can. J. Infect. Dis. Med. Microbiol. 2020, 2020, 2434350. [Google Scholar] [CrossRef] [PubMed]
  272. Alfouzan, W.; Udo, E.E.; Modhaffer, A.; Alosaimi, A. Molecular Characterization of Methicillin- Resistant Staphylococcus Aureus in a Tertiary Care Hospital in Kuwait. Sci. Rep. 2019, 9, 18527. [Google Scholar] [CrossRef] [Green Version]
  273. Alhussaini, M.S. Methicillin-Resistant Staphylococcus Aureus Nasal Carriage Among Patients Admitted at Shaqra General Hospital in Saudi Arabia. Pak. J. Biol. Sci. 2016, 19, 233–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  274. Alkharsah, K.R.; Rehman, S.; Alkhamis, F.; Alnimr, A.; Diab, A.; Al-Ali, A.K. Comparative and Molecular Analysis of MRSA Isolates from Infection Sites and Carrier Colonization Sites. Ann. Clin. Microbiol. Antimicrob. 2018, 17, 7. [Google Scholar] [CrossRef] [Green Version]
  275. Aziz, Z.S.; Hassan, M.A. Phenotypic and Molecular Study of MecA Gene in MRSA Isolated from Clinical Cases in Misan Province/Iraq. Indian J. Public Health 2019, 10, 553. [Google Scholar] [CrossRef]
  276. Helmi, N.R.; Zaman, R.M.; Aly, M.M. Prevalence Of Gram-Positive Bacteria In Jeddah, Kingdom Of Saudi Arabia: Study Of Antimicrobial Resistance Patterns And Molecular Typing. Int. J. Pharma Biol. Sci. 2013, 4, 1231–1245. [Google Scholar]
  277. Obaidat, M.M.; Bani Salman, A.E.; Roess, A.A. High Prevalence and Antimicrobial Resistance of MecA Staphylococcus Aureus in Dairy Cattle, Sheep, and Goat Bulk Tank Milk in Jordan. Trop. Anim. Health Prod. 2018, 50, 405–412. [Google Scholar] [CrossRef]
  278. Udo, E.E.; Boswihi, S.S. Antibiotic Resistance Trends in Methicillin-Resistant Staphylococcus aureus Isolated in Kuwait Hospitals: 2011–2015. Med Princ. Pract. 2017, 26, 485–490. [Google Scholar] [CrossRef] [PubMed]
  279. Hala, S.; Antony, C.P.; Alshehri, M.; Althaqafi, A.O.; Alsaedi, A.; Mufti, A.; Kaaki, M.; Alhaj-Hussein, B.T.; Zowawi, H.M.; Al-Amri, A.; et al. First Report of Klebsiella Quasipneumoniae Harboring BlaKPC-2 in Saudi Arabia. Antimicrob. Resist. Infect. Control 2019, 8, 203. [Google Scholar] [CrossRef]
  280. Ejaz, H.; Alzahrani, B.; Hamad, M.F.S.; Abosalif, K.O.A.; Junaid, K.; Abdalla, A.E.; Elamir, M.Y.M.; Aljaber, N.J.; Hamam, S.S.M.; Younas, S. Molecular Analysis of the Antibiotic Resistant NDM-1 Gene in Clinical Isolates of Enterobacteriaceae. Clin. Lab. 2020, 66. [Google Scholar] [CrossRef]
  281. Ahmad, S.; Khan, Z.; Al-Sweih, N.; Alfouzan, W.; Joseph, L. Candida Auris in Various Hospitals across Kuwait and Their Susceptibility and Molecular Basis of Resistance to Antifungal Drugs. Mycoses 2020, 63, 104–112. [Google Scholar] [CrossRef] [PubMed]
  282. Emara, M.; Ahmad, S.; Khan, Z.; Joseph, L.; Al-Obaid, I.; Purohit, P.; Bafna, R. Candida Auris Candidemia in Kuwait, 2014. Emerg. Infect. Dis. 2015, 21, 1091–1092. [Google Scholar] [CrossRef] [Green Version]
  283. Khan, Z.; Ahmad, S.; Benwan, K.; Purohit, P.; Al-Obaid, I.; Bafna, R.; Emara, M.; Mokaddas, E.; Abdullah, A.A.; Al-Obaid, K.; et al. Invasive Candida Auris Infections in Kuwait Hospitals: Epidemiology, Antifungal Treatment and Outcome. Infection 2018, 46, 641–650. [Google Scholar] [CrossRef]
  284. Hassan, M.M.; Belal, E.-S.B. Antibiotic Resistance and Virulence Genes in Enterococcus Strains Isolated from Different Hospitals in Saudi Arabia. Biotechnol. Biotechnol. Equip. 2016, 30, 726–732. [Google Scholar] [CrossRef] [Green Version]
  285. Salem-Bekhit, M.; Moussa, I.; Muharram, M.; Alanazy, F.; Hefni, H. Prevalence and Antimicrobial Resistance Pattern of Multidrug-Resistant Enterococci Isolated from Clinical Specimens. Indian J. Med. Microbiol. 2012, 30, 44–51. [Google Scholar] [CrossRef]
  286. Dibby, H.; Shlash, R. The Problem of Multidrug Resistance Bacterial Strains in Daily Clinical Practice in Dealing with Typhoid Fever in Mid-Euphrates Region of Iraq: A Cross Sectional Study. Indian J. Forensic Med. Toxicol. 2020, 14, 626–630. [Google Scholar]
  287. El-Tayeb, M.A.; Ibrahim, A.S.S.; Al-Salamah, A.A.; Almaary, K.S.; Elbadawi, Y.B. Prevalence, Serotyping and Antimicrobials Resistance Mechanism of Salmonella Enterica Isolated from Clinical and Environmental Samples in Saudi Arabia. Braz. J. Microbiol. 2017, 48, 499–508. [Google Scholar] [CrossRef] [PubMed]
  288. Harb, A.; O’Dea, M.; Hanan, Z.K.; Abraham, S.; Habib, I. Prevalence, Risk Factors and Antimicrobial Resistance of Salmonella Diarrhoeal Infection among Children in Thi-Qar Governorate, Iraq. Epidemiol. Infect. 2017, 145, 3486–3496. [Google Scholar] [CrossRef] [Green Version]
  289. Sahan, Z.A.; Hamed, S.L. Molecular Detection of Extended-Spectrum β-Lactamases- Producer Serratia Marcescens Causing Neonatal Sepsis in Iraq. Int. J. Res. Pharm. Sci. 2020, 11, 5803–5808. [Google Scholar] [CrossRef]
  290. Abdel-Haleem, A.M.; Rchiad, Z.; Khan, B.K.; Abdallah, A.M.; Naeem, R.; Nikhat Sheerin, S.; Solovyev, V.; Ahmed, A.; Pain, A. Genome Sequence of a Multidrug-Resistant Strain of Stenotrophomonas Maltophilia with Carbapenem Resistance, Isolated from King Abdullah Medical City, Makkah, Saudi Arabia. Genome Announc. 2015, 3. [Google Scholar] [CrossRef] [Green Version]
  291. El-Kersh, T.A.; Marie, M.A.; Al-Sheikh, Y.A.; Al-Agamy, M.H.; Al-Bloushy, A.A. Prevalence and Risk Factors of Early Fecal Carriage of Enterococcus Faecalis and Staphylococcus spp. and Their Antimicrobial Resistant Patterns among Healthy Neonates Born in a Hospital Setting in Central Saudi Arabia. Saudi Med. J. 2016, 37, 280–287. [Google Scholar] [CrossRef] [PubMed]
  292. Farman, M.; Yasir, M.; Al-Hindi, R.R.; Farraj, S.A.; Jiman-Fatani, A.A.; Alawi, M.; Azhar, E.I. Genomic Analysis of Multidrug-Resistant Clinical Enterococcus Faecalis Isolates for Antimicrobial Resistance Genes and Virulence Factors from the Western Region of Saudi Arabia. Antimicrob. Resist. Infect. Control 2019, 8, 55. [Google Scholar] [CrossRef]
  293. George, S.K.; Suseela, M.R.; El Safi, S.; Elnagi, E.A.; Al-Naam, Y.A.; Adam, A.A.; Jacob, A.M.; Al-Maqati, T.; Ks, H.K. Molecular Determination of van Genes among Clinical Isolates of Enterococci at a Hospital Setting. Saudi J. Biol. Sci. 2021, 28, 2895–2899. [Google Scholar] [CrossRef]
  294. Garaween, G.; Somily, A.; Raji, A.; Braun, S.; Al-Kattan, W.; Shibl, A.; Ehricht, R.; Senok, A. Serogenotyping and Emergence of Extended-Spectrum β-Lactamase Genes in Non-Typhoidal Salmonella: First Report from Saudi Arabia. J. Med. Microbiol. 2016, 65, 1343–1346. [Google Scholar] [CrossRef]
  295. Alsalem, Z.; Elhadi, N.; Aljeldah, M.; Alzahrani, F.; Nishibuchi, M. Characterization of Vibrio Vulnificus Isolated from the Coastal Areas in the Eastern Province of Saudi Arabia. J. Pure Appl. Microbiol. 2018, 12, 1355–1364. [Google Scholar] [CrossRef]
  296. M Kurdi Al-Dulaimi, M.; Abd Mutalib, S.; Abd Ghani, M.; Mohd Zaini, N.A.; Ariffin, A.A. Multiple Antibiotic Resistance (MAR), Plasmid Profiles, and DNA Polymorphisms among Vibrio Vulnificus Isolates. Antibiotics 2019, 8, 68. [Google Scholar] [CrossRef] [Green Version]
  297. Abro, A.H. Salmonella Typhi: Antibiotic Sensitivity Pattern in Dubai, United Arab Emirates. Pak. J. Med. Sci. 2011, 27, 6. [Google Scholar]
  298. AL-Fatlawy, H.N.K.; AL-Hadrawi, H.A.N. Molecular Profiling of Class I Integron Gene in MDR Salmonella Typhi Isolates. J. Pure Appl. Microbiol. 2020, 14, 1825–1833. [Google Scholar] [CrossRef]
  299. Yassin, M.T.; Mostafa, A.A.; Al-Askar, A.A.; Bdeer, R. In Vitro Antifungal Resistance Profile of Candida Strains Isolated from Saudi Women Suffering from Vulvovaginitis. Eur. J. Med. Res. 2020, 25, 1. [Google Scholar] [CrossRef]
  300. Alaboudi, A.R.; Malkawi, I.M.; Osaili, T.M.; Abu-Basha, E.A.; Guitian, J. Prevalence, Antibiotic Resistance and Genotypes of Campylobacter Jejuni and Campylobacter Coli Isolated from Chickens in Irbid Governorate, Jordan. Int. J. Food Microbiol. 2020, 327, 108656. [Google Scholar] [CrossRef] [PubMed]
  301. Ghunaim, H.; Behnke, J.M.; Aigha, I.; Sharma, A.; Doiphode, S.H.; Deshmukh, A.; Abu-Madi, M.M. Analysis of Resistance to Antimicrobials and Presence of Virulence/Stress Response Genes in Campylobacter Isolates from Patients with Severe Diarrhoea. PLoS ONE 2015, 10, e0119268. [Google Scholar] [CrossRef]
  302. Kanaan, M.H.G.; Mohammed, F.A. Antimicrobial Resistance of Campylobacter Jejuni from Poultry Meat in Local Markets of Iraq. Plant Arch. 2020, 20, 410–415. [Google Scholar]
  303. Jasim, S.A.; Al-abodi, H.R.; Ali, W.S. Resistance Rate and Novel Virulence Factor Determinants of Arcobacter spp., from Cattle Fresh Meat Products from Iraq. Microb. Pathog. 2021, 152, 104649. [Google Scholar] [CrossRef]
  304. AbdAlhussen, L.S.; Darweesh, M.F. Prevelance and Antibiotic Susceptibility Patterns of Pantoea spp. Int. J. ChemTech Res. 2016, 9, 430–437. [Google Scholar]
  305. Fazaa, S.A.; Darweesh, M.F. Prevalence of Pantoea spp. among Recurrent UTI Patients with Emphasis on Risk Factors and Antibiotic Resistance Patterns in Al-Qadisiyah Hospitals, Iraq. Ann. Trop. Med. Public Health 2020, 23, sp231202. [Google Scholar] [CrossRef]
  306. Burjaq, S.Z.; Abu-Romman, S.M. Prevalence and Antimicrobial Resistance of Salmonella spp. From Irrigation Water in Two Major Sources in Jordan. Curr. Microbiol. 2020, 77, 3760–3766. [Google Scholar] [CrossRef] [PubMed]
  307. Jassim, A.A.; Al-Gburi, N.M. Virulence Genes And Antimicrobial Resistance Of Salmonella Isolated From Milk In Wasit Province, Iraq. Plant Arch. 2020, 20, 2033–2039. [Google Scholar]
  308. Olaitan, A.O.; Dia, N.M.; Gautret, P.; Benkouiten, S.; Belhouchat, K.; Drali, T.; Parola, P.; Brouqui, P.; Memish, Z.; Raoult, D.; et al. Acquisition of Extended-Spectrum Cephalosporin- and Colistin-Resistant Salmonella Enterica Subsp. Enterica Serotype Newport by Pilgrims during Hajj. Int. J. Antimicrob. Agents 2015, 45, 600–604. [Google Scholar] [CrossRef]
  309. Osaili, T.M.; Al-Nabulsi, A.A.; Shaker, R.R.; Jaradat, Z.W.; Taha, M.; Al-Kherasha, M.; Meherat, M.; Holley, R. Prevalence of Salmonella Serovars, Listeria Monocytogenes, and Escherichia coli O157:H7 in Mediterranean Ready-to-Eat Meat Products in Jordan. J. Food Prot. 2014, 77, 106–111. [Google Scholar] [CrossRef]
  310. Abd Al-Mayahi, F.S.; Jaber, S.M. Multiple Drug Resistance of Listeria Monocytogenes Isolated from Aborted Women by Using Serological and Molecular Techniques in Diwaniyah City/Iraq. Iran. J. Microbiol. 2020, 12, 305. [Google Scholar] [CrossRef] [PubMed]
  311. Ahmed, M.S.; Taha, Z.M.A.; Omer, L.T. Isolation and Molecular Identification with Resistant Profile Determination of Listeria Monocytogenes from Imported Chicken Carcasses in Duhok, Kurdistan Region, Iraq. J. Pure Appl. Microbiol. 2015, 9, 97–103. [Google Scholar]
  312. Alanber, M.N.; Alharbi, N.S.; Khaled, J.M. Evaluation of Multidrug-Resistant Bacillus Strains Causing Public Health Risks in Powdered Infant Milk Formulas. J. Infect. Public Health 2020, 13, 1462–1468. [Google Scholar] [CrossRef]
  313. Hayder, T.; Aljanaby, A.A.J.J. Antibiotics Susceptibility Patterns of Citrobacter Freundii Isolated from Pa-Tients with Urinary Tract Infection in Al-Najaf Governorate—Iraq. Int. J. Res. Pharm. Sci. 2019, 10, 1481–1488. [Google Scholar] [CrossRef]
  314. Talat, A.; Khalid, S.; Majeed, H.A.R.; Khan, A.U. Whole-Genome Sequence Analysis of Multidrug-Resistant Staphylococcus EpidermiDis. ST35 Strain Isolated from Human Ear Infection of an Iraqi Patient. J. Glob. Antimicrob. Resist. 2020, 21, 318–320. [Google Scholar] [CrossRef]
  315. Al-Muhanna, A.S.; Al-Muhanna, S.; Alzuhairi, M.A. Molecular Investigation of Extended-Spectrum Beta-Lactamase Genes and Potential Drug Resistance in Clinical Isolates of Morganella Morganii. Ann. Saudi Med. 2016, 36, 223–228. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  316. Hanan, Z.K. Molecular Detection of Cholera Infection during the Outbreak in Thi-Qar Province/Iraq in 2015–2016. J. Phys. Conf. Ser. 2019, 1279, 012068. [Google Scholar] [CrossRef] [Green Version]
  317. AlJindan, R.; AlEraky, D.M.; Borgio, J.F.; AbdulAzeez, S.; Abdalhamid, B.; Mahmoud, N.; Farhat, M. Diagnostic Deficiencies of C. Difficile Infection among Patients in a Tertiary Hospital in Saudi Arabia: A Laboratory-Based Case Series. Saudi J. Biol. Sci. 2021, 28, 4472–4477. [Google Scholar] [CrossRef]
  318. Al-Sa’ady, A.T. Detection of Vancomycin Resistance in Multidrug-Resistant Enterococcus Faecalis Isolated from Burn Infections. Drug Invent. Today 2019, 11, 7. [Google Scholar]
  319. Ulger Toprak, N.; Veloo, A.C.M.; Urban, E.; Wybo, I.; Justesen, U.S.; Jean-Pierre, H.; Morris, T.; Akgul, O.; Kulekci, G.; Soyletir, G.; et al. A Multicenter Survey of Antimicrobial Susceptibility of Prevotella Species as Determined by Etest Methodology. Anaerobe 2018, 52, 9–15. [Google Scholar] [CrossRef] [Green Version]
  320. Taj-Aldeen, S.J.; Deshmukh, A.; Doiphode, S.; Abdul Wahab, A.; Allangawi, M.; AlMuzrkchi, A.; Klaassen, C.H.; Meis, J.F. Molecular Identification and Susceptibility Pattern of Clinical Nocardia Species: Emergence of Nocardia Crassostreae as an Agent of Invasive Nocardiosis. Can. J. Infect. Dis. Med. Microbiol. 2013, 24, e33–e38. [Google Scholar] [CrossRef] [Green Version]
  321. El-Mahdy, T.S.; Al-Agamy, M.H.; Al-Qahtani, A.A.; Shibl, A.M. Detection of Bla OXA-23-like and Bla NDM-1 in Acinetobacter Baumannii from the Eastern Region, Saudi Arabia. Microb. Drug Resist. 2017, 23, 115–121. [Google Scholar] [CrossRef]
  322. Khan, Z.; Ahmad, S.; Joseph, L.; Al-Obaid, K. Isolation of Cholesterol-Dependent, Multidrug-Resistant Candida Glabratastrains from Blood Cultures of a Candidemia Patient in Kuwait. BMC Infect. Dis. 2014, 14, 188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  323. Alosaimi, R.S.; Kaaki, M.M. Catheter-Related ESBL-Producing Leclercia Adecarboxylata Septicemia in Hemodialysis Patient: An Emerging Pathogen? Case Rep. Infect. Dis. 2020, 2020, 7403152. [Google Scholar] [CrossRef] [PubMed]
  324. Guan, Q.; Almutairi, T.S.; Alhalouli, T.; Pain, A.; Alasmari, F. Metagenomics of Imported Multidrug-Resistant Mycobacterium Leprae, Saudi Arabia, 2017. Emerg. Infect. Dis. 2020, 26, 615–617. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  325. Abdalhamid, B.; Elhadi, N.; Alsamman, K.; Aljindan, R. Chryseobacterium Gleum Pneumonia in an Infant with Nephrotic Syndrome. IDCases 2016, 5, 34–36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  326. Aljindan, R.; Elhadi, N. Genetic Relationship of Multi-Resistant Acinetobacter Baumannii Isolates in Kingdom of Saudi Arabia. J. Pure Appl. Microbiol. 2018, 12, 1951–1958. [Google Scholar] [CrossRef] [Green Version]
  327. Yasir, M.; Farman, M.; Shah, M.W.; Jiman-Fatani, A.A.; Othman, N.A.; Almasaudi, S.B.; Alawi, M.; Shakil, S.; Al-Abdullah, N.; Ismaeel, N.A.; et al. Genomic and Antimicrobial Resistance Genes Diversity in Multidrug-Resistant CTX-M-Positive Isolates of Escherichia coli at a Health Care Facility in Jeddah. J. Infect. Public Health 2020, 13, 94–100. [Google Scholar] [CrossRef]
  328. Johani, K.; Abualsaud, D.; Costa, D.M.; Hu, H.; Whiteley, G.; Deva, A.; Vickery, K. Characterization of Microbial Community Composition, Antimicrobial Resistance and Biofilm on Intensive Care Surfaces. J. Infect. Public Health 2018, 11, 418–424. [Google Scholar] [CrossRef]
  329. Hamza, W.; Salama, M.; Morsi, S.; Abdo, N.; Al-Fadhli, M. Benchmarking for Surgical Site Infections among Gastrointestinal Surgeries and Related Risk Factors: Multicenter Study in Kuwait. Infect. Drug Resist. 2018, 11, 1373–1381. [Google Scholar] [CrossRef] [Green Version]
  330. Balkhair, A.; Al-Farsi, Y.M.; Al-Muharrmi, Z.; Al-Rashdi, R.; Al-Jabri, M.; Neilson, F.; Al-Adawi, S.S.; El-Beeli, M.; Al-Adawi, S. Epidemiology of Multi-Drug Resistant Organisms in a Teaching Hospital in Oman: A One-Year Hospital-Based Study. Sci. World J. 2014, 2014, 157102. [Google Scholar] [CrossRef]
  331. Al Awaidy, S.T. Tuberculosis Elimination in Oman: Winning the War on the Disease. ERJ Open Res. 2018, 4, 00121–02018. [Google Scholar] [CrossRef]
  332. Metry, A.M.; Al Salmi, I.; Al-Abri, S.; Al Ismaili, F.; Al Mahrouqi, Y.; Hola, A.; Shaheen, F.A.M. Epidemiology and Outcome of Tuberculosis in Immunocompromised Patients. Saudi J. Kidney Dis. Transpl. 2017, 28, 806–817. [Google Scholar] [PubMed]
  333. Hasan, M.R.; Sundaram, M.S.; Sundararaju, S.; Tsui, K.-M.; Karim, M.Y.; Roscoe, D.; Imam, O.; Janahi, M.A.; Thomas, E.; Dobson, S.; et al. Unusual Accumulation of a Wide Array of Antimicrobial Resistance Mechanisms in a Patient with Cytomegalovirus-Associated Hemophagocytic Lymphohistiocytosis: A Case Report. BMC Infect. Dis. 2020, 20, 237. [Google Scholar] [CrossRef] [PubMed]
  334. Alkhawaja, E.; Hammadi, S.; Abdelmalek, M.; Mahasneh, N.; Alkhawaja, B.; Abdelmalek, S.M. Antibiotic Resistant Cutibacterium Acnes among Acne Patients in Jordan: A Cross Sectional Study. BMC Dermatol. 2020, 20, 17. [Google Scholar] [CrossRef]
  335. Al-Shamahy, H.A.; Sabrah, A.A.; Al-Robasi, A.B.; Naser, S.M. Types of Bacteria Associated with Neonatal Sepsis in Al-Thawra University Hospital, Sana’a, Yemen, and Their Antimicrobial Profile. Sultan Qaboos Univ. Med J. 2012, 12, 48–54. [Google Scholar] [CrossRef]
  336. Kordalewska, M.; Guerrero, K.D.; Garcia-Rubio, R.; Jiménez-Ortigosa, C.; Mediavilla, J.R.; Cunningham, M.H.; Hollis, F.; Hong, T.; Chow, K.F.; Kreiswirth, B.N.; et al. Antifungal Drug Susceptibility and Genetic Characterization of Fungi Recovered from COVID-19 Patients. J. Fungi 2021, 7, 552. [Google Scholar] [CrossRef]
  337. Al-Mutairi, N.M.; Ahmad, S.; Mokaddas, E. Performance Comparison of Four Methods for Detecting Multidrug-Resistant Mycobacterium Tuberculosis Strains. Int. J. Tuberc. Lung Dis. 2011, 15, 110–115. [Google Scholar]
  338. Ali, R.M.; Alsudani, A.A. Discordance between GeneXpert Assay and Conventional Drug-Susceptibility Testing in Detecting Rifampicin-Resistant Tuberculosis: A Perspective of the Line Probe Assay. Int. J. Mycobacteriol. 2016, 5, S193–S194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  339. Arastehfar, A.; Fang, W.; Daneshnia, F.; Al-Hatmi, A.M.; Liao, W.; Pan, W.; Khan, Z.; Ahmad, S.; Rosam, K.; Lackner, M.; et al. Novel Multiplex Real-Time Quantitative PCR Detecting System Approach for Direct Detection of Candida Auris and Its Relatives in Spiked Serum Samples. Future Microbiol. 2019, 14, 33–45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  340. Alabdullatif, M.; Alrehaili, J. Three Years of Evaluation to Determine Reduction of Antibiotic Resistance in Gram-Negative Bacteria by the Saudi National Action Plan. Infect. Drug Resist. 2020, 13, 3657–3667. [Google Scholar] [CrossRef]
  341. Amoudy, H.A.; Safar, H.A.; Mustafa, A.S. Development of Escherichia coli and Mycobacterium Smegmatis Recombinants Expressing Major Mycobacterium Tuberculosis-Specific Antigenic Proteins. Int. J. Mycobacteriol. 2016, 5, S84–S85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  342. Lesho, E.; Lin, X.; Clifford, R.; Snesrud, E.; Onmus-Leone, F.; Appalla, L.; Ong, A.; Maybank, R.; Nielsen, L.; Kwak, Y.; et al. From the Battlefield to the Bedside: Supporting Warfighter and Civilian Health With the “ART” of Whole Genome Sequencing for Antibiotic Resistance and Outbreak Investigations. Mil. Med. 2016, 181, 621–624. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  343. Al Tall, Y.; Abualhaijaa, A.; Alsaggar, M.; Almaaytah, A.; Masadeh, M.; Alzoubi, K.H. Design and Characterization of a New Hybrid Peptide from LL-37 and BMAP-27. Infect. Drug Resist. 2019, 12, 1035–1045. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  344. Almaaytah, A.; Abualhaijaa, A.; Alqudah, O. The Evaluation of the Synergistic Antimicrobial and Antibiofilm Activity of AamAP1-Lysine with Conventional Antibiotics against Representative Resistant Strains of Both Gram-Positive and Gram-Negative Bacteria. Infect. Drug Resist. 2019, 12, 1371–1380. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  345. Obeidat, M.; Shatnawi, M.; Al-alawi, M.; Al-Zu‘bi, E.; Al-Dmoor, H.; Al-Qudah, M.; El-Qudah, J.; Otri, I. Antimicrobial Activity of Crude Extracts of Some Plant Leaves. Res. J. Microbiol. 2012, 7, 59–67. [Google Scholar] [CrossRef] [Green Version]
  346. Ahmed, A.A.; Salih, F.A. Low Concentrations of Local Honey Modulate ETA Expression, and Quorum Sensing Related Virulence in Drug-Resistant Pseudomonas Aeruginosa Recovered from Infected Burn Wounds. Iran. J. Basic Med. Sci. 2019, 22, 568. [Google Scholar] [CrossRef]
  347. Al-Somat, M.; Al-Adhal, A.; Al-Arwali, A.; Al, K.; Al-Moyed, K.; Shopit, A.; Karbane, M.E.; AL-Kamarany, M.A. Sensitivity of Clinical Bacterial Isolates to Honey Marketed in Yemen. Int. J. Pharm. Sci. Rev. Res. 2014, 27, 267–271. [Google Scholar]
  348. Darwish, R.M.; Fares, R.J.A.; Zarga, M.H.A.; Nazer, I.K. Antibacterial Effect of Jordanian Propolis and Isolated Flavonoids against Human Pathogenic Bacteria. Afr. J. Biotechnol. 2010, 9, 9. [Google Scholar]
  349. Yang, S.-K.; Yusoff, K.; Thomas, W.; Akseer, R.; Alhosani, M.S.; Abushelaibi, A.; Lim, S.-H.-E.; Lai, K.-S. Lavender Essential Oil Induces Oxidative Stress Which Modifies the Bacterial Membrane Permeability of Carbapenemase Producing Klebsiella Pneumoniae. Sci. Rep. 2020, 10, 819. [Google Scholar] [CrossRef]
  350. Soliman, S.S.M.; Semreen, M.H.; El-Keblawy, A.A.; Abdullah, A.; Uppuluri, P.; Ibrahim, A.S. Assessment of Herbal Drugs for Promising Anti-Candida Activity. BMC Complement Altern Med. 2017, 17, 257. [Google Scholar] [CrossRef] [Green Version]
  351. Perveen, K.; Husain, F.M.; Qais, F.A.; Khan, A.; Razak, S.; Afsar, T.; Alam, P.; Almajwal, A.M.; Abulmeaty, M.M.A. Microwave-Assisted Rapid Green Synthesis of Gold Nanoparticles Using Seed Extract of Trachyspermum Ammi: ROS Mediated Biofilm Inhibition and Anticancer Activity. Biomolecules 2021, 11, 197. [Google Scholar] [CrossRef] [PubMed]
  352. Almaaytah, A.; Qaoud, M.; Khalil Mohammed, G.; Abualhaijaa, A.; Knappe, D.; Hoffmann, R.; Al-Balas, Q. Antimicrobial and Antibiofilm Activity of UP-5, an Ultrashort Antimicrobial Peptide Designed Using Only Arginine and Biphenylalanine. Pharmaceuticals 2018, 11, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  353. Soliman, S.S.M.; Saeed, B.Q.; Elseginy, S.A.; Al-Marzooq, F.; Ahmady, I.M.; El-Keblawy, A.A.; Hamdy, R. Critical Discovery and Synthesis of Novel Antibacterial and Resistance-Modifying Agents Inspired by Plant Phytochemical Defense Mechanisms. Chem.-Biol. Interact. 2021, 333, 109318. [Google Scholar] [CrossRef] [PubMed]
  354. Muthukrishnan, P.; Chithra Devi, D.; Mostafa, A.A.; Alsamhary, K.I.; Abdel-Raouf, N.; Nageh Sholkamy, E. Antimicrobial Efficacy of Nocardiopsis Sp. MK_MSt033 against Selected Multidrug Resistant Clinical Microbial Pathogens. J. Infect. Public Health 2020, 13, 1522–1532. [Google Scholar] [CrossRef]
  355. Almaaytah, A.; Ajingi, Y.; Abualhaijaa, A.; Tarazi, S.; Alshar’i, N.; Al-Balas, Q. Peptide Consensus Sequence Determination for the Enhancement of the Antimicrobial Activity and Selectivity of Antimicrobial Peptides. Infect. Drug Resist. 2017, 10, 1. [Google Scholar] [CrossRef] [Green Version]
  356. Almaaytah, A.; Mohammed, G.; Abualhaijaa, A.; Al-Balas, Q. Development of Novel Ultrashort Antimicrobial Peptide Nanoparticles with Potent Antimicrobial and Antibiofilm Activities against Multidrug-Resistant Bacteria. Drug Des. Dev. Ther. 2017, 11, 3159–3170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  357. Mechkarska, M.; Ahmed, E.; Coquet, L.; Leprince, J.; Jouenne, T.; Vaudry, H.; King, J.D.; Conlon, J.M. Antimicrobial Peptides with Therapeutic Potential from Skin Secretions of the Marsabit Clawed Frog Xenopus Borealis (Pipidae). Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2010, 152, 467–472. [Google Scholar] [CrossRef] [PubMed]
  358. Omran, Z.; Bader, A.; Porta, A.; Vandamme, T.; Anton, N.; Alehaideb, Z.; El-Said, H.; Faidah, H.; Essa, A.; Vassallo, A.; et al. Evaluation of Antimicrobial Activity of Triphala Constituents and Nanoformulation. Evid.-Based Complementary Altern. Med. 2020, 2020, 6976973. [Google Scholar] [CrossRef]
  359. Mahdi, L.; Musafer, H.; Zwain, L.; Salman, I.; Al-Joofy, I.; Rasool, K.; Mussa, A.; Al-kakei, S.; Al-Oqaili, R.; Al-Alak, S.; et al. Two Novel Roles of Buffalo Milk Lactoperoxidase, Antibiofilm Agent and Immunomodulator against Multidrug Resistant Salmonella Enterica Serovar Typhi and Listeria Monocytogenes. Microb. Pathog. 2017, 109, 221–227. [Google Scholar] [CrossRef]
  360. Rahmeh, R.; Akbar, A.; Kishk, M.; Al-Onaizi, T.; Al-Azmi, A.; Al-Shatti, A.; Shajan, A.; Al-Mutairi, S.; Akbar, B. Distribution and Antimicrobial Activity of Lactic Acid Bacteria from Raw Camel Milk. New Microbes New Infect. 2019, 30, 100560. [Google Scholar] [CrossRef]
  361. Abdel-Aziz, H.; Eldehna, W.; Keeton, A.; Piazza, G.; Kadi, A.; Attwa, M.; Abdelhameed, A.; Attia, M. Isatin-Benzoazine Molecular Hybrids as Potential Antiproliferative Agents: Synthesis and in Vitro Pharmacological Profiling. Drug Des. Dev. Ther. 2017, 11, 2333–2346. [Google Scholar] [CrossRef] [Green Version]
  362. Aboul-Fadl, T.; Bin-Jubair, F.A.S.; Aboul-Wafa, O. Schiff Bases of Indoline-2,3-Dione (Isatin) Derivatives and Nalidixic Acid Carbohydrazide, Synthesis, Antitubercular Activity and Pharmacophoric Model Building. Eur. J. Med. Chem. 2010, 45, 4578–4586. [Google Scholar] [CrossRef]
  363. Ahamed, A.; Arif, I.A.; Mateen, M.; Surendra Kumar, R.; Idhayadhulla, A. Antimicrobial, Anticoagulant, and Cytotoxic Evaluation of Multidrug Resistance of New 1,4-Dihydropyridine Derivatives. Saudi J. Biol. Sci. 2018, 25, 1227–1235. [Google Scholar] [CrossRef] [PubMed]
  364. Bogue, A.L.; Panmanee, W.; McDaniel, C.T.; Mortensen, J.E.; Kamau, E.; Actis, L.A.; Johannigman, J.A.; Schurr, M.J.; Satish, L.; Kotagiri, N.; et al. AB569, a Non-Toxic Combination of Acidified Nitrite and EDTA, is Effective at Killing the Notorious Iraq/Afghanistan Combat Wound Pathogens, Multi-Drug Resistant Acinetobacter Baumannii and Acinetobacter spp. PLoS ONE 2021, 16, e0247513. [Google Scholar] [CrossRef] [PubMed]
  365. Venugopala, K.N.; Uppar, V.; Chandrashekharappa, S.; Abdallah, H.H.; Pillay, M.; Deb, P.K.; Morsy, M.A.; Aldhubiab, B.E.; Attimarad, M.; Nair, A.B.; et al. Cytotoxicity and Antimycobacterial Properties of Pyrrolo[1,2-a]Quinoline Derivatives: Molecular Target Identification and Molecular Docking Studies. Antibiotics 2020, 9, 233. [Google Scholar] [CrossRef] [PubMed]
  366. Ahmad, I.; Wahab, S.; Nisar, N.; Dera, A.A.; Alshahrani, M.Y.; Abullias, S.S.; Irfan, S.; Alam, M.M.; Srivastava, S. Evaluation of Antibacterial Properties of Matricaria Aurea on Clinical Isolates of Periodontitis Patients with Special Reference to Red Complex Bacteria. Saudi Pharm. J. 2020, 28, 1203–1209. [Google Scholar] [CrossRef]
  367. Al-Asmari, A.K.; Alamri, M.A.; Almasoudi, A.S.; Abbasmanthiri, R.; Mahfoud, M. Evaluation of the in Vitro Antimicrobial Activity of Selected Saudi Scorpion Venoms Tested against Multidrug-Resistant Micro-Organisms. J. Glob. Antimicrob. Resist. 2017, 10, 14–18. [Google Scholar] [CrossRef]
  368. Alkhedaide, A.Q.; Ismail, T.A.; Alotaibi, S.H.; Nassan, M.A.; Shehri, Z.S.A. Preventive Effect of Artemisinin Extract against Cholestasis Induced via Lithocholic Acid Exposure. Biosci. Rep. 2018, 38, BSR20181011. [Google Scholar] [CrossRef] [Green Version]
  369. El-Newehy, M.H.; Moydeen A., M.; Aldalbahi, A.K.; Thamer, B.M.; Mahmoud, Y.A.-G.; El-Hamshary, H. Biocidal Polymers: Synthesis, Characterization and Antimicrobial Activity of Bis-Quaternary Onium Salts of Poly(Aspartate-Co-Succinimide). Polymers 2020, 13, 23. [Google Scholar] [CrossRef]
  370. Manzoor, S.; Bilal, A.; Khan, S.; Ullah, R.; Iftikhar, S.; Emwas, A.-H.; Alazmi, M.; Gao, X.; Jawaid, A.; Saleem, R.S.Z.; et al. Identification and Characterization of SSE15206, a Microtubule Depolymerizing Agent That Overcomes Multidrug Resistance. Sci. Rep. 2018, 8, 3305. [Google Scholar] [CrossRef] [Green Version]
  371. Al-Dhabi, N.A.; Ghilan, A.-K.M.; Esmail, G.A.; Valan Arasu, M.; Duraipandiyan, V.; Ponmurugan, K. Bioactivity Assessment of the Saudi Arabian Marine Streptomyces Sp. Al-Dhabi-90, Metabolic Profiling and Its in Vitro Inhibitory Property against Multidrug Resistant and Extended-Spectrum Beta-Lactamase Clinical Bacterial Pathogens. J. Infect. Public Health 2019, 12, 549–556. [Google Scholar] [CrossRef] [PubMed]
  372. Alekish, M.; Ismail, Z.B.; Albiss, B.; Nawasrah, S. In Vitro Antibacterial Effects of Zinc Oxide Nanoparticles on Multiple Drug-Resistant Strains of Staphylococcus Aureus and Escherichia coli: An Alternative Approach for Antibacterial Therapy of Mastitis in Sheep. Vet. World 2018, 11, 1428–1432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  373. Alsamhary, K.I. Eco-Friendly Synthesis of Silver Nanoparticles by Bacillus Subtilis and Their Antibacterial Activity. Saudi J. Biol. Sci. 2020, 27, 2185–2191. [Google Scholar] [CrossRef]
  374. Al-Dhabi, N.; Ghilan, A.-K.M.; Arasu, M. Characterization of Silver Nanomaterials Derived from Marine Streptomyces Sp. Al-Dhabi-87 and Its In Vitro Application against Multidrug Resistant and Extended-Spectrum Beta-Lactamase Clinical Pathogens. Nanomaterials 2018, 8, 279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  375. Abdulmughni, J.; Mahyoub, E.M.; Alaghbari, A.T.; Al Serouri, A.A.; Khader, Y. Performance of Multidrug-Resistant Tuberculosis Surveillance in Yemen: Interview Study. JMIR Public Health Surveill 2019, 5, e14294. [Google Scholar] [CrossRef]
  376. Ganaie, F.; Nagaraj, G.; Govindan, V.; Basha, R.; Hussain, M.; Ashraf, N.; Ahmed, S.; Ravi Kumar, K.L. Impact of Hajj on the S. Pneumoniae Carriage among Indian Pilgrims during 2016- a Longitudinal Molecular Surveillance Study. Travel Med. Infect. Dis. 2018, 23, 64–71. [Google Scholar] [CrossRef]
  377. Leangapichart, T.; Gautret, P.; Griffiths, K.; Belhouchat, K.; Memish, Z.; Raoult, D.; Rolain, J.-M. Acquisition of a High Diversity of Bacteria during the Hajj Pilgrimage, Including Acinetobacter Baumannii with Bla OXA-72 and Escherichia coli with Bla NDM-5 Carbapenemase Genes. Antimicrob. Agents Chemother. 2016, 60, 5942–5948. [Google Scholar] [CrossRef] [Green Version]
  378. Zumla, A.; Saeed, A.B.; Alotaibi, B.; Yezli, S.; Dar, O.; Bieh, K.; Bates, M.; Tayeb, T.; Mwaba, P.; Shafi, S.; et al. Tuberculosis and Mass Gatherings—Opportunities for Defining Burden, Transmission Risk, and the Optimal Surveillance, Prevention, and Control Measures at the Annual Hajj Pilgrimage. Int. J. Infect. Dis. 2016, 47, 86–91. [Google Scholar] [CrossRef] [Green Version]
  379. Aurilio, C.; Sansone, P.; Paladini, A.; Barbarisi, M.; Coppolino, F.; Pota, V.; Pace, M.C. Multidrug Resistence Prevalence in COVID Area. Life 2021, 11, 601. [Google Scholar] [CrossRef]
  380. Vaillancourt, M.; Jorth, P. The Unrecognized Threat of Secondary Bacterial Infections with COVID-19. mBio 2020, 11, e01806-20. [Google Scholar] [CrossRef]
Biology 10 01144 g001 550
Figure 1. PRISMA 2009 flow diagram for the selection of articles reporting multi drug-resistant micro-organisms from the Arabian Peninsula, since 2010. * There were three papers reporting MDR micro-organisms in multiple countries [1]: Bahrain, Saudi Arabia and United Arab Emirates; [2]: Saudi Arabia, United Arab Emirates, Oman, Qatar, Bahrain, and Kuwait; [3]: Saudi Arabia, Kuwait, Oman and United Arab Emirates. # Google scholar not considered. Country-wise data for the number of articles from various databases are presented in Supplementary Table S1.
Figure 1. PRISMA 2009 flow diagram for the selection of articles reporting multi drug-resistant micro-organisms from the Arabian Peninsula, since 2010. * There were three papers reporting MDR micro-organisms in multiple countries [1]: Bahrain, Saudi Arabia and United Arab Emirates; [2]: Saudi Arabia, United Arab Emirates, Oman, Qatar, Bahrain, and Kuwait; [3]: Saudi Arabia, Kuwait, Oman and United Arab Emirates. # Google scholar not considered. Country-wise data for the number of articles from various databases are presented in Supplementary Table S1.
Biology 10 01144 g001
Biology 10 01144 g002 550
Figure 2. List of multidrug-resistant bacteria and fungi reported in Arabian Peninsula. Numbers in the doughnut indicate the number of multidrug-resistant organisms reported in the respective countries of the Arabian Peninsula. MRSA: Methicillin-resistant Staphylococcus aureus.
Figure 2. List of multidrug-resistant bacteria and fungi reported in Arabian Peninsula. Numbers in the doughnut indicate the number of multidrug-resistant organisms reported in the respective countries of the Arabian Peninsula. MRSA: Methicillin-resistant Staphylococcus aureus.
Biology 10 01144 g002
Biology 10 01144 g003 550
Figure 3. (A) Multidrug-resistant microbial associated mortality reported in the Arabian Peninsula. (B) Dark red line indicates linear trend line of annual mortality due to multidrug-resistant microbial infection. (C) Number of deaths reported due to specific MDR microbial infection in Arabian Peninsula. Map in blue color indicate the country wise mortality due to Acinetobacter baumannii. (D) Percentage mortality due to MDR microbes. Gender information were not reported on the mortality in certain articles. UAE: United Arab Emirates.
Figure 3. (A) Multidrug-resistant microbial associated mortality reported in the Arabian Peninsula. (B) Dark red line indicates linear trend line of annual mortality due to multidrug-resistant microbial infection. (C) Number of deaths reported due to specific MDR microbial infection in Arabian Peninsula. Map in blue color indicate the country wise mortality due to Acinetobacter baumannii. (D) Percentage mortality due to MDR microbes. Gender information were not reported on the mortality in certain articles. UAE: United Arab Emirates.
Biology 10 01144 g003
Table
Table 1. Logical relation between sets of multidrug-resistant bacteria and fungi in countries of Arabian Peninsula.
Table 1. Logical relation between sets of multidrug-resistant bacteria and fungi in countries of Arabian Peninsula.
CountriesNumber of MDROMultidrug-Resistant Micro-Organism(s)
Bahrain, Iraq, Jordan, Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates, Yemen1Acinetobacter baumannii
Bahrain, Iraq, Jordan, Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates1Escherichia coli
Iraq, Jordan, Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates, Yemen,3Mycobacterium tuberculosis, Staphylococcus aureus, Pseudomonas aeruginosa
Iraq, Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates1Klebsiella pneumoniae
Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates2Enterobacter cloacae, Stenotrophomonas maltophilia
Iraq, Kuwait, Oman, Qatar, Saudi Arabia1Enterococcus faecium
Iraq, Jordan, Kuwait, Qatar, Saudi Arabia1Streptococcus pneumoniae
Iraq, Jordan, Kuwait, Saudi Arabia1Salmonella enterica
Iraq, Qatar, Saudi Arabia, United Arab Emirates1Salmonella typhi
Kuwait, Saudi Arabia, United Arab Emirates1Candida auris
Iraq, Kuwait, Saudi Arabia, Oman 3Serratia marcescens, Proteus mirabilis, Klebsiella oxytoca
Iraq, Saudi Arabia, United Arab Emirates, Oman1Citrobacter freundii
Iraq, Jordan, United Arab Emirates, Qatar1Staphylococcus epidermis
Kuwait, Saudi Arabia1Candida glabrata
Oman, Saudi Arabia1Pantoea agglomerans
Qatar, Saudi Arabia1Vibrio vulnificus
Iraq, Saudi Arabia6Klebsiella aerogenes, Morganella morganii, Citrobacter koseri, Pantoea spp., Providencia spp., Staphylococcus saprophyticus
Iraq, Saudi Arabia, Qatar Staphylococcus haemolyticus
Kuwait,1Enterococcus gallinarum
Iraq, Jordan2Listeria monocytogenes, Campylobacter jejuni
Saudi Arabia, Qatar4Staphylococcus hominis, Klebsiella spp., Salmonella spp., Streptococcus spp.
Iraq, Qatar 1Enterobacter spp.
Saudi Arabia53Staphylococcus capitis, Staphylococcus caprae, Acinetobacter calcoaceticus baumannii, Pseudomonas, Bacillus subtilis, Leuconostoc mesenteroides, Candida albicans, Staphylococcus epidermidis, Proteus vulgaris, Proteus sp., Bacillus cereus, Lactobacillus plantarum, Bipolaris oryzae, Methicillin-resistant Staphylococcus aureus, Bacillus tequilensis, Staphylococcus, Enterococcus, Staphylococcus saccharolyticus, Leclercia adecarboxylata, Shigella flexnari, Staphylococcus spp., Pantoea eucrina, Enterobacteriaceae, Citrobacter youngae, Staphylococcus petrasii, Lactococcus garvieae, Escherichia fergusonii, Caldimonas manganoxidans, Chryseobacterium gleum, Citrobacter sp., Providencia stuartii, Vancomycin-resistant Enterococcus, Mycobacterium leprae, Clostridium spp., Stenotrophomonus maltophilia, Enterococcus faecalis, Acinetobacter, Non-typhoidal Salmonella, Enterobacter aerogenes, Acinetobacter lwoffii, A. baumannii complex, A. baumannii/haemolyticus, Acinetobacter haemolyticus, Pseudomonas luteola, Serratia fonticola, Penicillin-resistant Streptococcus pyogenes, Bacillus spp., Serratia spp., Candida spp.
Kuwait5Legionella pneumophila, Aeromonas hydrophila, Moraxella catarrhalis, Prevotella spp., Haemophilus influenzae
Oman5Pantoea dispersa, Burkholderia cepacia, Enterobacter asburiae, Enterobacter hormaechei Enterobacter ludwigii
Qatar7Campylobacter spp., Nocardia crassostreae, Chryseobacterium indologenes, Acinetobacter spp., Bacteroid spp., Coagulase negative Staphylococci, Enterococcus spp.
Jordan1Propionibacterium acnes
Iraq1Vibrio cholerae
Table
Table 2. Total number of studies that reported the MDR microbe in countries of the Arabian Peninsula.
Table 2. Total number of studies that reported the MDR microbe in countries of the Arabian Peninsula.
S. NoMDR MicrobeSaudi ArabiaBahrainKuwaitOmanQatarUnited Arab EmiratesJordanIraqYemenTotal Number of Reports *
1Acinetobacter baumannii5918225612196 #
2Escherichia coli51245661110 94
3Mycobacterium tuberculosis31 1121216458
4Klebsiella pneumoniae36 3444 7 58
5Pseudomonas aeruginosa36 414119157
6Staphylococcus aureus16 411255135
7Acinetobacter14 2 16
8Streptococcus pneumoniae7 1 1 21 12
9Stenotrophomonas maltophilia7 112 11
10Enterobacter cloacae6 1211 11
11Candida auris4 6 1 11
12Enterobacteriaceae6 5 11
13MRSA11 11
14Stenotrophomonus maltophilia6 1 10
15Salmonella enterica2 1 24 9
16Proteus mirabilis8 1 9
17Serratia marcescens3 31 2 8
18Enterococcus faecalis8 8
19Citrobacter freundii4 1 1 1 7
20Enterococcus faecium6 6
21Klebsiella oxytoca2 2 2 6
22Listeria monocytogenes 23 5
23Morganella morganii4 1 5
24Staphylococcus epidermidis3 11 1 5
25Salmonella spp.4 1 1 5
26Klebsiella spp.4 1 1 5
27Candida spp.4 1 5
28Streptococcus spp.2 3 1 5
29Enterobacter4 1 5
30Enterococcus3 2 5
31Staphylococcus spp.5 5
32Salmonella typhi2 11 1 5
33Enterobacter aerogenes5 5
34Staphylococcus hominis4 1 4
35Candida albicans4 4
36Non-typhoidal Salmonella2 2 4
37Citrobacter koseri2 1 4
38Klebsiella aerogenes4 4
39Enterococcus faecalis/faecium 11 1 3
40Providencia spp.1 2 3
41Pantoea spp.1 2 3
42Providencia stuartii3 3
43Acinetobacter lwoffii3 3
44Serratia spp.3 3
45Campylobacter jejuni 11 2
46Staphylococcus (MRSA) 2 2
47Proteus sp.1 1 2
48Candida glabrata1 1 2
49Pantoea agglomerans1 1 2
50Bacillus subtilis2 2
51Staphylococcus capitis2 2
52Staphylococcus saprophyticus2 2
* MDR organisms reported more than once in the countries of Arabian Peninsula are listed: # includes Acinetobacter calcoaceticus baumannii = 2, A. baumannii complex = 1 and A. baumannii/haemolyticus = 1. MRSA: methicillin-resistant Staphylococcus aureus.
Table
Table 3. Reports of mortality caused by MDR microbial infection from Qatar, Kuwait, Iraq and Yemen.
Table 3. Reports of mortality caused by MDR microbial infection from Qatar, Kuwait, Iraq and Yemen.
CountryQatarQatarQatarQatarKuwaitKuwaitKuwaitKuwaitKuwaitKuwaitKuwaitIraqYemenYemen
MDR/Reference[4][5][6][7][8][9][10][11][12][13][14][15][16][17]
Total cases4810239452617114154911143065411580
Median age years484349.145.985859.563.956.655.649.857.5184545
Gender F 1571591924561567303815032
Gender M 91822934247993457002736548
No. of Discharged patients 5174350 34 6469141555610166
Total number of non-survivors15565102437983215981414
Number of non-survivors F 352 33 1
Number of non-survivors M 5 672 65 1
Multiple MDR pathogens 102 9 3215
Acinetobacter baumannii15 65
Pseudomonas aeruginosa
Staphylococcus aureus 98
Mycobacterium tuberculosis 1414
Escherichia coli
Klebsiella pneumoniae 5
Staphylococcus epidermidis
Enterobacteria
Candida auris 37 8
Acinetobacter
Enterobacteriaceae
Proteus sp.
Salmonella typhi 1
Salmonella enterica 1
Table
Table 4. Reports of mortality caused by MDR microbial infection from Saudi Arabia and Jordan.
Table 4. Reports of mortality caused by MDR microbial infection from Saudi Arabia and Jordan.
CountrySaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaSaudi ArabiaJordanJordanJordanJordan
MDR/Reference[18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][34]
Total cases498360712905719713863381464572111956
Median age yearsnewborn5050.437.573.559.963.6635737564360.547.3270.655.553.4
Gender F11 23032 110294313144262 6422
Gender M18 374825856941955 24104395 5534
No. of Discharged patients2630 34 472 198196930
Total number of non-survivors33154725433411039113413725026
Number of non-survivors F0 34141 2612
Number of non-survivors M3 7625 2414
Multiple MDR pathogens 31 39 4137
Acinetobacter baumannii 54 5026
Pseudomonas aeruginosa 54 4
Staphylococcus aureus
Mycobacterium tuberculosis 7 110
Escherichia coli
K. pneumoniae
Staphylococcus epidermidis3
Enterobacteria
Candida auris 2 33 1
Acinetobacter 2
Enterobacteriaceae 13
Proteus sp.
Salmonella typhi
Salmonella Enteritidis
Table
Table 5. Number of multi drug-resistant strains reported in the Arabian Peninsula. Details of the number of strains are presented in the Supplementary Table S2.
Table 5. Number of multi drug-resistant strains reported in the Arabian Peninsula. Details of the number of strains are presented in the Supplementary Table S2.
MDROTotal StrainReference
Escherichia coli13254[1,3,7,10,11,14,31,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111]
Mycobacterium tuberculosis13087[16,17,21,27,38,50,51,56,99,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141]
Acinetobacter baumannii5600[2,6,12,28,40,42,46,47,48,51,55,56,58,63,73,88,93,94,103,105,108,111,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184,185,186,187,188,189,190,191,192,193,194,195,196,197,198,199]
Klebsiella pneumoniae5480[3,5,10,11,12,14,28,30,38,39,40,41,42,45,46,47,48,51,52,55,56,58,62,63,67,81,82,83,84,88,91,92,93,105,106,111,127,143,149,155,160,181,196,200,201,202,203,204,205,206,207,208,209,210,211,212,213,214,215,216,217,218,219,220]
Pseudomonas aeruginosa3445[11,12,14,23,26,28,31,38,41,42,45,46,47,48,50,51,52,55,56,58,62,63,81,82,83,88,90,91,93,94,109,111,143,149,160,162,180,181,184,190,194,195,196,221,222,223,224,225,226,227,228,229,230,231,232,233,234,235,236,237,238,239,240,241]
Staphylococcus aureus3133[7,11,12,15,42,46,56,58,62,65,73,90,108,143,149,242,243,244,245,246,247,248,249,250,251,252,253]
Acinetobacter2033[6,14,31,33,38,41,65,66,73,187,194,254,255,256]
Enterobacteriaceae1411[3,13,19,20,73,101,176,190,232,257,258,259]
Providencia spp.1216[19,232,260,261]
Streptococcus pneumoniae1077[56,262,263,264,265,266,267,268,269]
Methicillin-resistant Staphylococcus aureus (MRSA)1000[9,11,19,31,46,47,56,93,142,173,176,181,182,190,270,271,272,273,274,275,276,277,278]
Klebsiella spp.927[31,65,66,73,94,108,111,279]
Enterobacter815[11,31,41,48,50,65,66,94,280]
Proteus vulgaris722[40,42,232]
Candida auris580[9,11,22,24,25,29,281,282,283]
Enterococcus553[65,66,81,105,108,284,285]
Pseudomonas spp.481[46,65,66,73,83,108]
Klebsiella oxytoca434[12,40,42,46,50,105,143,205,232]
Salmonella enterica413[100,286,287,288]
Serratia marcescens289[12,40,41,42,46,47,51,88,111,143,149,289]
Stenotrophomonus maltophilia257[31,41,47,65,66,290]
Enterococcus faecalis256[42,47,58,93,143,181,291,292]
Vancomycin resistant Enterococcus (VRE)255[19,73,190,293]
Non-typhoidal Salmonella248[8,203,294]
Vibrio vulnificus234[295,296]
Salmonella typhi231[8,297,298]
Proteus sp.220[12,38,41,48,51,65,108,143]
Candida spp.180[65,66,299]
Stenotrophomonas maltophilia149[40,46,48,111,172,190,256]
Proteus mirabilis137[14,42,46,58,62,81,82,91,93,105,111,143,181,232]
Campylobacter jejuni125[250,300,301,302]
Arcobacter butzleri100[303]
Pantoea spp.99[143,304,305]
salmonella spp.85[46,98,105,232,306,307,308,309]
Listeria monocytogenes83[40,100,309,310,311]
Staphylococcus spp.78[46,74,108,291]
Bacillus spp.77[312]
Citrobacter freundii66[42,81,91,105,143,232,313]
Serratia spp.66[65,66,232]
Staphylococcus epidermidis59[18,46,55,314]
Enterobacter cloacae54[10,42,46,58,81,83,93,105,106,110,111,143]
Morganella morganii54[42,46,58,83,111,143,315]
Citrobacter spp.54[11,38,41,83,232]
Enterobacter aerogenes40[42,46,83,91,111,143]
A. baumannii/haemolyticus32[144]
Streptococcus spp.23[58,108]
Vibrio vulnificus23[296]
Staphylococcus saprophyticus20[42,51,88,143]
Arcobacter cryaerophilus20[303]
Vibrio cholerae20[316]
A. baumannii complex19[144]
Clostridioides difficile18[317]
Enterococcus faecium17[42,46,143,149,318]
Salmonella Enteritidies15[8]
Prevotella spp.14[319]
Nocardia crassostreae13[267,320]
Candida albicans11[190]
Staphylococcus hominis11[46,55]
Acinetobacter lwoffii11[42,143,144]
Providencia stuartii10[46,48,58]
Acinetobacter calcoaceticus baumannii10[321]
Citrobacter koseri9[46,58,111,155]
Pseudomonas luteola9[42]
Pantoea agglomerans9[42]
Staphylococcus capitis4[46]
Acinetobacter haemolyticus4[144]
Serratia fonticola4[42]
Candida glabrata2[322]
methicillin-resistant Staphylococcus epidermidis (MRSE)1[47]
penicillin-resistant Streptococcus pyogenes1[47]
Leclercia adecarboxylata1[323]
Mycobacterium leprae1[324]
Chryseobacterium gleum1[325]
Enterococcus gallinarum1[149]
Klebsiella oxytoca1[10]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Borgio, J.F.; Rasdan, A.S.; Sonbol, B.; Alhamid, G.; Almandil, N.B.; AbdulAzeez, S. Emerging Status of Multidrug-Resistant Bacteria and Fungi in the Arabian Peninsula. Biology 2021, 10, 1144. https://doi.org/10.3390/biology10111144

AMA Style

Borgio JF, Rasdan AS, Sonbol B, Alhamid G, Almandil NB, AbdulAzeez S. Emerging Status of Multidrug-Resistant Bacteria and Fungi in the Arabian Peninsula. Biology. 2021; 10(11):1144. https://doi.org/10.3390/biology10111144

Chicago/Turabian Style

Borgio, J. Francis, Alia Saeed Rasdan, Bayan Sonbol, Galyah Alhamid, Noor B. Almandil, and Sayed AbdulAzeez. 2021. "Emerging Status of Multidrug-Resistant Bacteria and Fungi in the Arabian Peninsula" Biology 10, no. 11: 1144. https://doi.org/10.3390/biology10111144

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop