Next Article in Journal
Targeting BAM for Novel Therapeutics against Pathogenic Gram-Negative Bacteria
Next Article in Special Issue
Antimicrobial Dispensing Practices during COVID-19 and the Implications for Pakistan
Previous Article in Journal
Chemical Profiling, Anticholinesterase, Antioxidant, and Antibacterial Potential of the Essential Oil from Myrcianthes discolor (Kunth) McVaugh, an Aromatic Tree from Southern Ecuador
Previous Article in Special Issue
Antibiotic Overprescribing among Neonates and Children Hospitalized with COVID-19 in Pakistan and the Implications
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Antibiotics
Volume 12
Issue 4
10.3390/antibiotics12040678
antibiotics-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:
Article

Antibiotic Utilization Patterns for Different Wound Types among Surgical Patients: Findings and Implications

by
Zikria Saleem
1,*,
Umar Ahsan
2,
Abdul Haseeb
3,
Ummara Altaf
4,
Narjis Batool
5,
Hira Rani
6,
Javeria Jaffer
6,
Fatima Shahid
6,
Mujahid Hussain
7,
Afreenish Amir
8,
Inaam Ur Rehman
9,
Umar Saleh
9,
Sana Shabbir
9,
Muhammad Usman Qamar
10,
Waleed Mohammad Altowayan
11,
Fahad Raees
12,
Aisha Azmat
13,
Mohammad Tarique Imam
14,
Phumzile P. Skosana
15 and
Brian Godman
16,17,18,*
1
Department of Pharmacy Practice, Faculty of Pharmacy, Bahuddin Zakaria University, Multan 60800, Pakistan
2
Department of Infection Prevention and Control, Alnoor Specialist Hospital, Ministry of Health, Makkah 24241, Saudi Arabia
3
Department of Clinical Pharmacy, College of Pharmacy, Umm Al-Qura University, Makkah 24382, Saudi Arabia
4
Department of Pharmacy, Ghurki Trust Teaching Hospital, Lahore 54000, Pakistan
5
Center of Health Systems and Safety Research, Faculty of Medicine, Health and Human Sciences, Australian Institute of Health Innovation, Macquarie University, Sydney 2109, Australia
6
Department of Pharmacy, Faculty of Pharmacy, University of Lahore, Lahore 54000, Pakistan
7
Department of Pharmacy, Indus Hospital and Health Network, Karachi 75190, Pakistan
8
Department of Microbiology, Armed Forces Institute of Pathology, National University of Medical Sciences, Rawalpindi 46000, Pakistan
9
Punjab University College of Pharmacy, Faculty of Pharmacy, University of the Punjab, Lahore 54000, Pakistan
10
Institute of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, Faisalabad 38000, Pakistan
11
Department of Pharmacy Practice, College of Pharmacy, Qassim University, Buraydah 52571, Saudi Arabia
12
Department of Medical Microbiology, Faculty of Medicine, Umm Al-Qura University, Makkah 24382, Saudi Arabia
13
Department of Physiology, Faculty of Medicine, Umm Al-Qura University, Makkah 24382, Saudi Arabia
14
Department of Clinical Pharmacy, College of Pharmacy, Prince Sattam Bin Abdul Aziz University, Al Kharj 11942, Saudi Arabia
15
Department of Clinical Pharmacy, School of Pharmacy, Sefako Makgatho Health Sciences University, Molotlegi Street, Ga-Rankuwa, Pretoria 0208, South Africa
16
School of Pharmacy, Sefako Makgatho Health Sciences University, Ga-Rankuwa, Pretoria 0208, South Africa
17
Strathclyde Institute of Pharmacy and Biomedical Sciences, Strathclyde University, Glasgow G4 0RE, UK
18
Centre of Medical and Bio-Allied Health Sciences Research, Ajman University, Ajman 346, United Arab Emirates
 
add Show full affiliation list
 
remove Hide full affiliation list
*
Authors to whom correspondence should be addressed.
Antibiotics 2023, 12(4), 678; https://doi.org/10.3390/antibiotics12040678
Submission received: 28 February 2023 / Revised: 20 March 2023 / Accepted: 27 March 2023 / Published: 30 March 2023
(This article belongs to the Special Issue Antimicrobial Stewardship and Prescribing Practice)
Review Reports Versions Notes

Abstract

:
Antimicrobial prophylaxis is effective in reducing the rate of surgical site infections (SSIs) post-operatively. However, there are concerns with the extent of prophylaxis post-operatively, especially in low- and middle-income countries (LMICs). This increases antimicrobial resistance (AMR), which is a key issue in Pakistan. Consequently, we conducted an observational cross-sectional study on 583 patients undergoing surgery at a leading teaching hospital in Pakistan with respect to the choice, time and duration of antimicrobials to prevent SSIs. The identified variables included post-operative prophylactic antimicrobials given to all patients for all surgical procedures. In addition, cephalosporins were frequently used for all surgical procedures, and among these, the use of third-generation cephalosporins was common. The duration of post-operative prophylaxis was 3–4 days, appreciably longer than the suggestions of the guidelines, with most patients prescribed antimicrobials until discharge. The inappropriate choice of antimicrobials combined with prolonged post-operative antibiotic administration need to be addressed. This includes appropriate interventions, such as antimicrobial stewardship programs, which have been successful in other LMICs to improve antibiotic utilization associated with SSIs and to reduce AMR.

1. Introduction

Healthcare-associated infections (HAIs) are a common adverse event in hospitals, resulting in increased length-of-stay, morbidity and mortality as well as increased costs [1,2,3,4,5,6,7,8]. In higher-income countries (HIC), device-associated infections are the most common HAI, while among low-and middle-income countries (LMICs), surgical-site infections (SSIs) are the most common HAI [7,9,10,11,12]. Consequently, these patients need to be carefully managed to prevent SSIs, especially in LMICs.
SSIs arise from infective microorganisms, which grow either on the incision site (superficial and deep) or involve an organ or space within 30 days after operation [13,14,15]. They are one of the main problems arising from surgical operations and are the primary source of nosocomial infections in hospital [16,17,18]. SSIs have a considerable burden in terms of their impact on morbidity and mortality as well as increasing costs through increased lengths-of-stay in hospital [4,19,20,21]. The rate of SSIs varies considerably according to the hospital setting, experience of the surgeon, the surgical procedure and the country [7,17,18,22]. Reported prevalence rates vary between 3% to 50% of surgical procedures, with typically appreciably higher prevalence rates among LMICs [11,12,17,23,24,25]. Reported prevalence rates in the United Kingdom and United States of America (USA) for SSIs vary between 16% and 31% [19,26]. Across Africa, combined prevalence rates of 14.8% are seen in surgical patients [10]. In Pakistan, SSI rates can vary from 6.5% up to 33.7% of patients admitted to surgical wards [27,28,29]. Overall, SSIs can account for up to 60% of HAIs in LMICs [1,9,11,30,31]. In view of this, the management of surgical patients requires careful scrutiny to improve future care and reduce costs.
Surgical procedures have been classified into four categories, i.e., Clean, Clean/Contaminated, Contaminated and Dirty, with increasing frequency of bacterial impurity and post-operative infections [15,32,33]. Surgical antimicrobial prophylaxis (SAP) is the administration of antimicrobials before or after surgical procedures to prevent post-operative SSIs [11,17,34].
Appropriate prescription of antibiotics is seen as one of the most effective ways to reduce SSIs [17,18,35,36]. Previous studies and organizations have suggested that antibiotics should ideally be administered 60 min before the first incision, with a second dose potentially administered for longer procedures, i.e., longer than 4 h [36,37,38,39,40,41,42]. Administration prior to this can increase the risk of SSIs by up to five-fold, and delaying the administration until after the first incision can potentially double the risk of an SSI [17,43]. Consequently, this should be avoided. However, alongside the pharmacokinetics and pharmacodynamics of antimicrobials prescribed, their timing, dose and route of administration; possible encountered pathogens; and necessary bactericidal concentrations should also be considered for optimum prophylaxis [35,44,45]. According to World Health Organization (WHO), post-operative SAP should be considered for up to 24 h after the incision is made, where pertinent [46]. More recently, the WHO AWaRe guidance book (2022) has suggested that antibiotic prophylaxis should be administered 120 min or less before starting surgery as a single dose, and not continued after surgery. An additional dose of antibiotics should only be considered where the procedure is prolonged or if there has been major blood loss [33]. Cefazolin, an ‘Access antibiotic’, is recommended as a first choice, and can potentially be combined with other antibiotics, including metronidazole or gentamicin, depending on the procedure [33].
However, extending prophylaxis beyond one day does not reduce SSI rates, but at the same time increases adverse events, antimicrobial resistance (AMR) and costs [17,35,36,39,40,41,47]. Consequently, this also needs to be avoided, especially given the rising AMR rates across countries, particularly among LMICs [48].
A number of studies have shown that the prescription of antibiotics to prevent SSIs is currently not being carried out according to the current guidelines. This includes concerns with the timing of the first dose as well as the selection of the antibiotics and the duration of the prescription [17,18,49]. Typically, prophylaxis extends well beyond the post-operative period, especially among LMICs (Supplementary Table S1); however, this is not always the case [17,18,44,50]. The considerable variation seen in practice, especially among LMICs, could be due to several factors. These include differences in published guidelines across countries, lack of awareness of the content of the current guidelines, concerns with the cleanliness of the theaters and wards in the hospital as well as a lack of acceptance of the current guidelines among surgeons [17,18,49,51].
Overall, the irrational prescription of antibiotics, including the excessive use of broad-spectrum antibiotics, is common for surgical procedures. This is especially true among LMICs, including Pakistan [17,18,50,52]. However, there is currently limited available research regarding the prescription of antibiotics for SAP among hospitals in Pakistan that is broken down by the surgical procedures undertaken. This is the first step to developing future quality improvement programs to address current concerns. Consequently, this study was undertaken to observe the utilization patterns of antibiotic prescription during various surgical procedures in a leading tertiary hospital in Pakistan. Key areas of investigation were the choice of antibiotic for given procedures and the timing and duration of the prescription. The findings would be used to provide future guidance for this and other hospitals in Pakistan. Key activities include instigating appropriate antimicrobial stewardship programs (ASPs) to improve future antibiotic prescription if appreciable concerns are found [17,18,29]. This is because a number of ASPs have been successfully introduced among LMICs to improve antibiotic prescription surrounding SSIs, providing direction to all key stakeholders in Pakistan in the future.

2. Results

2.1. Sociodemographic and Clinical Characteristics of Study Participants

The medical records of 583 surgical patients who were prescribed an antimicrobial as part of SAP were evaluated. The mean age of the patients was 42.2 years. Out of the total study population, 51.3% of the participants were male (Table 1). A minority of the patients had comorbid conditions, and the majority of these suffered from diabetes (4.6% of the surgical patients). The majority of the patients were from the general surgery ward (50%), and most of these were admitted due to high pain scores. Table 1 contains further details regarding the wards of the patients along with the diagnoses (Table 1).
Osteomyelitis (27.4%), followed by cholelithiasis (13.4%) and abscess formation (12.1%), were the most common surgical procedures (Table 1). Regarding the types of surgical procedures which were performed, implant fixation due to the removal of dead bone was the most common procedure, accounting for approximately 27.4% of all procedures, followed by caesarean sections (13.8%) (Table 2). As a result, just under half of the patients had a dirty procedure performed (45.7%), followed by those who received a clean contaminated procedure (30.8%) (Table 2).

2.2. Antimicrobial Utilization Patterns for Surgical Prophylaxis

The different antimicrobial classes prescribed as part of SAP for the different types of wound surgery included penicillins (in combination with beta-lactamase inhibitors), cephalosporins (in combination with beta-lactamase inhibitors), aminoglycosides, fluoroquinolones, vancomycin and metronidazole. The most prevalent use of antimicrobials was for dirty procedures (45.7%), followed by clean contaminated wounds (30.7%).
Overall, cephalosporins were the most commonly prescribed type of antibiotic, followed by penicillins. Among the penicillins, co-amoxiclav was extensively prescribed in patients undergoing clean procedures (36.5%), whereas there was appreciable prescription of cefoperazone plus sulbactum (24.4%), of the cephalosporins, in patients undergoing dirty procedures. There was also appreciable prescription of amikacin and vancomycin in patients undergoing dirty procedures. Most of the patients undergoing dirty procedures received a dual combination of antibiotics, e.g., cefoperazone/sulbactum plus amikacin, and in some cases, triple combinations (Table 3). Most of the prescribed antibiotics were in the ‘Watch’ category.
Concerning the timing of antibiotic administration, all the patients in our study were administered their antimicrobials from half an hour to one hour before the surgical procedure.
The duration of antimicrobial prophylaxis was 3.5 ± 1.5 days, typically 3 to 4 days post-operatively. The antibiotics prescribed post-operatively were typically a continuation of those prescribed prior to the first incision. These antibiotics were prescribed post-operatively to prevent SSIs, typically without performing culture sensitivity testing (CST). Overall, antibiotics were considered as prophylactics in clean, clean contaminated and contaminated wounds, and were used for treatment in the case of dirty wounds.

3. Discussion

We believe this study is the first to be conducted in Pakistan to assess the pattern of antimicrobial usage for the different types of surgical wounds, i.e., clean, clean/contaminated, contaminated and dirty. Encouragingly, nearly all patients received their antimicrobial prophylaxis half to one hour before the surgical procedure, indicating good compliance with this particular aspect of prophylaxis in the current guidelines and, in addition, in the recent AWaRe guidance [33,35]. This is certainly not universal, as there have been concerns with the timing of prophylaxis pre-operatively as well as extensive prescription post-operatively among a number of LMICs [11,17,18].
However, a number of areas of concern were identified in our study that need to be addressed to improve the future prescription of antimicrobials in surgical patients to reduce AMR and associated costs. Firstly, all the patients in our study subsequently received antimicrobials for their surgical procedures post-operatively. This indicates their overuse in this situation, as there is no need to prescribe antibiotics post-operatively to prevent SSIs, especially for clean procedures [33,35]. The extensive prescription post-operatively until the day of discharge that was seen in our study in Pakistan may be due to a number of factors. These include a lack of awareness and non-compliance with current international guidelines among physicians, i.e., perceiving that such guidelines are not directly attributable to their hospital and setting, concerns with the cleanliness of their wards, a general lack of infection control practices due to resource issues as well as a lack of trust in the validity of antimicrobial susceptibility data in the hospital [17,53,54,55]. Our findings regarding the extensive prescription of antimicrobials post-operatively for SAP are similar to those of a study by Khan et al. (2020), as well as one by Saleem et al. (2023), in Pakistan alongside other LMICs (Supplementary Table S1), and this issue urgently needs to be addressed going forward [55,56]. Our findings are different from those of a recent study in Ethiopia, where 97.4% of patients who were administered antibiotics for SAP were prescribed a single dose. This typically occurred one hour before surgical procedures (in 88% of patients undergoing SAP) [50]. Successful ASPs have been undertaken in a range of LMICs to improve SAP, thereby providing exemplars to key stakeholder groups in Pakistan for the future. These are summarized in Supplementary Table S2.
Another concern was the frequent use of third generation cephalosporins in this study, which are typically ‘Watch’ antibiotics under the WHO AWaRe classification [57,58]. Unnecessary prescription of ‘Watch’ and ‘Reserve’ antibiotics should be reduced as part of an effort to reduce resistance rates within a country [59,60,61]. This is particularly important in Pakistan given the high rates of AMR in the country, generally high rates of prescription of ‘Watch’ and ‘Reserve’ antibiotics within hospitals and the urgent need to reduce AMR as part of the agreed National Action Plan [52,56,62,63,64,65]. The National Institute of Health (NIH) of Pakistan has recognized the impact of HAIs-initiated activities attempting implement infection control training programs and provide the necessary infrastructure to support prevention programs as part of the agreed National Action Plan (NAP) to reduce AMR in Pakistan [62,65]. This is encouraging, since a number of studies have now shown that a range of interventions as part of ASPs can appreciably improve the use of antimicrobials to prevent SSIs in LMICs (Supplementary Table S2). We are aware that ASPs have begun to be introduced across LMICs, including Pakistan; however, challenges remain [53,66]. The plethora of ASPs that have now been introduced across LMICs to reduce the inappropriate use of antibiotics as part of SAP, including among hospitals in Pakistan (Supplementary Table S2), can serve as exemplars to key stakeholder groups across Pakistan. We will continue to monitor this as a key activity to reduce AMR in hospitals in Pakistan going forward. In addition, the guidance for SAP advocated in the recent AWaRe Guidance book should be promoted. As such, continued extensive prescription of ‘Watch’ antibiotics for SAP in Pakistan should be reduced, alongside prolonged prescriptions [33]. In addition, regularly recording patient outcomes in their notes is essential.
We are aware that there are a number of limitations within our study. Firstly, we only involved one center in this study. However, this center was carefully chosen as an exemplar for a tertiary hospital in Pakistan. Secondly, we only selected patients in the orthopedic, general surgery and gynecology wards, as we were mainly interested in current antimicrobial prescribing patterns to prevent SSIs. Culture reports were also not checked to identify resistance patterns in the hospital. Consequently, we were unable to assess the appropriateness of the antibiotics prescribed, including third generation cephalosporins, based on current sensitivity patterns. We also did not check the actual prevalence of SSIs due to a lack of patient follow-up details in patients’ notes. Lastly, these observational studies, by their very nature, are likely to involve missing key information sets. In addition, it is difficult to identify true risk factors. Nevertheless, we believe that our findings are robust and will provide a direction for all key stakeholder groups in Pakistan in the future.

4. Materials and Methods

4.1. Study Setting and Design

This observational, cross-sectional study was conducted in the orthopedic, general surgery and gynecological wards of Ghurki Trust Teaching Hospital (GTTH), Lahore, Pakistan, to explore the utilization pattern of antimicrobials in surgical patients with clean, clean/contaminated, contaminated and dirty wounds, as defined by ACS-NSQIP (Table 4) [67]. This hospital was chosen for this initial study as it is a leading teaching hospital in Lahore. GTTH is a purpose-built tertiary care hospital located in Lahore, Pakistan. The hospital was established in 2011 by the Ghurki Trust, which aims to provide high-quality healthcare services. The hospital has a capacity of 600 beds and offers a wide range of medical and pharmacy services. It is equipped with state-of-the-art medical equipment and technology to provide the latest and most advanced treatments to its patients. Consequently, if there are issues in this hospital, they are likely to be replicated in other hospitals throughout Pakistan.
All the patients admitted to the gynecologic, general surgical and orthopedic wards who underwent clean, clean/contaminated, contaminated and dirty procedures were included. These wards were carefully chosen to provide the maximum number of patients for the study. Seriously ill patients subsequently requiring admission into the Intensive Care Unit (ICU) and patients admitted to other wards in the hospital were excluded from the study.

4.2. Data Collection Process, Questionnaire and Statistical Analysis

Data were collected from 583 patients who underwent surgery at the admitted hospital. Only antimicrobials used during hospitalization were recorded. Antimicrobials were typically not switched to a peroral form or to a narrow spectrum antibiotic during this period.
The data collection form that was utilized in this study was based on previous publications, combined with the considerable experience of the co-authors [11,13,17,20,23,28,30]. We have used this approach before for similar research projects across different countries [11,64,68].
The form was divided into four key sections. These included:
  • Patient demographic and medical data, e.g., age, gender, co-morbidities, chief complaint, diagnosis, length of hospital stay and duration of antibiotic prescription;
  • Surgical data, i.e., type of surgery;
  • Antimicrobial utilization data, e.g., name, antimicrobial class (ATC code), AWaRe classification, frequency and duration of administration [57,58,69]. Under the AWaRe classification, antibiotics in the ‘Access’ group should be used against commonly encountered infections, as they have a lower resistance rate, while those in the ‘Watch’ group should only be used in critical conditions, as they have a greater chance of resistance development. Antibiotics in the ‘Reserve’ group should only be prescribed in multi-drug resistance cases [57,58];
  • Wound classification (clean, clean/contaminated, contaminated or dirty).
All the collected data were analyzed using the Statistical Package for Social Sciences (SPSS) and the latest versions of Microsoft Excel. Descriptive statistics were used to summarize the patient demographics and clinical data.

4.3. Antimicrobial Stewardship Programs to Reduce Inappropriate Antibiotic Prescription for SAP among LMICs

This will be a narrative review of the literature rather than a systematic review to provide guidance to key stakeholder groups in Pakistan. This is because there have been a number of published reviews to date surrounding the extensive prescription of antibiotics post-operatively as part of SAP, as well as other potential interventions to reduce SSIs [17,18,44,70,71,72,73,74,75,76].
Alongside this, our objective was to document ASPs that have been instigated to improve future SAP as part of the discussion, and to provide exemplars that could subsequently be used to guide key stakeholders in Pakistan regarding potential ways forward to improve appropriate SAP techniques when there are concerns. This builds on the current examples used in Pakistan. In light of this, we performed a narrative review of pertinent publications rather than undertaking a systematic review. We have successfully used this approach before in LMICs to stimulate debate surrounding different key disease areas and topics [77,78]. Consequently, we believed that this methodology was appropriate for this study.

4.4. Ethical Approval

The study was approved by the Human Ethics Committee of College of Pharmacy, Bahauddin Zakariya University, Multan, Pakistan (BZU-DEPP-22-830-1006). The data were collected after obtaining approval from the management of the Ghurki Trust Teaching Hospital.

5. Conclusions

In conclusion, the patterns of antibiotic utilization in this hospital were not in full accordance with the current standard guidelines, including the AWaRe guidance, to prevent SSIs. The overuse of ‘Watch’ antibiotics, as well as the prolonged duration of antibiotic prescription post-operatively, are concerns that need to be addressed going forward to reduce AMR in hospitals in Pakistan. In light of this, there is an urgent need to promote pertinent ASPs throughout Pakistan to improve future antimicrobial prescription for SAP. These can be based on ASPs that have been successfully implemented in other LMICs. We will continue to monitor the situation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/antibiotics12040678/s1, Table S1: Duration of SAP across LMICs [79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99]; Table S2: Programs instigated to improve antibiotic prescribing for SAP among LMICs (including additional references [100,101,102,103,104,105,106,107,108,109,110]).

Author Contributions

Z.S., U.A. (Ummara Altaf), A.H., P.P.S. and B.G. were involved with the conceptualization of the study and the methodology. Z.S., U.A. (Umar Ahsan), P.P.S. and B.G. provided the background for the study and assisted with the methodology. Z.S., U.A. (Ummara Altaf), A.H., U.A. (Umar Ahsan), N.B., H.R., J.J., F.S., M.H., A.A. (Afreenish Amir), I.U.R., U.S., S.S., M.U.Q., W.M.A., F.R., A.A. (Aisha Azmat) and M.T.I. were involved with data collection, analysis, validation and interpretation of the data. Z.S., U.A. (Ummara Altaf), P.P.S. and B.G. produced the first draft, and all authors contributed to successive reviews before submission. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was approved by the Human Ethics Committee of the College of Pharmacy, Bahauddin Zakariya University, Multan, Pakistan (BZU-DEPP-22-830-1006).

Informed Consent Statement

No informed consent was necessary, as this was an anonymous review of patients’ records and there was no direct contact with patients. In addition, all patients’ details were kept confidential by the lead author (Z.S.). This is in line with similar studies undertaken by the co-authors across countries [52,86,97].

Data Availability Statement

Additional data are available upon reasonable request to the corresponding authors.

Acknowledgments

The authors are thankful to Zonera Inayat and Muqaddas Javed for helping with data entry, as well as to the Management of the Pharmacy Services Department of Ghurki Trust Teaching Hospital, for their support.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Labi, A.-K.; Obeng-Nkrumah, N.; Owusu, E.; Bjerrum, S.; Bediako-Bowan, A.; Sunkwa-Mills, G.; Akufo, C.; Fenny, A.P.; Opintan, J.A.; Enweronu-Laryea, C.; et al. Multi-centre point-prevalence survey of hospital-acquired infections in Ghana. J. Hosp. Infect. 2019, 101, 60–68. [Google Scholar] [CrossRef] [PubMed]
  2. Barnett, A.G.; Page, K.; Campbell, M.; Martin, E.; Rashleigh-Rolls, R.; Halton, K.; Paterson, D.L.; Hall, L.; Jimmieson, N.; White, K.; et al. The increased risks of death and extra lengths of hospital and ICU stay from hospital-acquired bloodstream infections: A case–control study. BMJ Open 2013, 3, e003587. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Manoukian, S.; Stewart, S.; Dancer, S.; Graves, N.; Mason, H.; McFarland, A.; Robertson, C.; Reilly, J. Estimating excess length of stay due to healthcare-associated infections: A systematic review and meta-analysis of statistical methodology. J. Hosp. Infect. 2018, 100, 222–235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Zimlichman, E.; Henderson, D.; Tamir, O.; Franz, C.; Song, P.; Yamin, C.K.; Keohane, C.; Denham, C.R.; Bates, D.W. Health care–associated infections: A meta-analysis of costs and financial impact on the US health care system. JAMA Intern. Med. 2013, 173, 2039–2046. [Google Scholar] [CrossRef]
  5. Pouwels, K.B.; Vansteelandt, S.; Batra, R.; Edgeworth, J.; Wordsworth, S.; Robotham, J.V. Estimating the Effect of Healthcare-Associated Infections on Excess Length of Hospital Stay Using Inverse Probability-Weighted Sur-vival Curves. Clin. Infect. Dis. 2020, 71, e415–e420. [Google Scholar]
  6. Cassini, A.; Plachouras, D.; Eckmanns, T.; Abu Sin, M.; Blank, H.P.; Ducomble, T.; Haller, S.; Harder, T.; Klingeberg, A.; Sixtensson, M.; et al. Burden of Six Healthcare-Associated Infections on European Population Health: Estimating Incidence-Based Disability-Adjusted Life Years through a Population Prevalence-Based Modelling Study. PLoS Med. 2016, 13, e1002150. [Google Scholar] [CrossRef] [Green Version]
  7. Saleem, Z.; Godman, B.; Hassali, M.A.; Hashmi, F.K.; Azhar, F.; Rehman, I.U. Point prevalence surveys of health-care-associated infections: A systematic review. Ann. Trop. Med. Parasitol. 2019, 113, 191–205. [Google Scholar] [CrossRef]
  8. Nelson, R.E.; Hatfield, K.M.; Wolford, H.; Samore, M.H.; Scott, R.D.; Reddy, S.C.; Olubajo, B.; Paul, P.; Jernigan, J.A.; Baggs, J. National Estimates of Healthcare Costs Associated with Multidrug-Resistant Bacterial Infections Among Hospitalized Patients in the United States. Clin. Infect. Dis. 2021, 72 (Suppl. 1), S17–S26. [Google Scholar] [CrossRef]
  9. Saleem, Z.; Hassali, M.A.; Godman, B.; Hashmi, F.K.; Saleem, F. A multicenter point prevalence survey of healthcare–associated infections in Pakistan: Findings and implications. Am. J. Infect. Control 2019, 47, 421–424. [Google Scholar] [CrossRef] [Green Version]
  10. Ngaroua Ngah, J.E.; Bénet, T.; Djibrilla, Y. Incidence of surgical site infections in sub-Saharan Africa: Systematic review and meta-analysis. Pan. Afr. Med. J. 2016, 24, 171. [Google Scholar]
  11. Sefah, I.A.; Denoo, E.Y.; Bangalee, V.; Kurdi, A.; Sneddon, J.; Godman, B. Appropriateness of surgical antimicrobial prophylaxis in a teaching hospital in Ghana: Findings and implications. JAC-Antimicrob. Resist. 2022, 4, dlac102. [Google Scholar] [CrossRef] [PubMed]
  12. Rickard, J.; Beilman, G.; Forrester, J.; Sawyer, R.; Stephen, A.; Weiser, T.G.; Valenzuela, J. Surgical Infections in Low- and Middle-Income Countries: A Global Assessment of the Burden and Management Needs. Surg Infect. 2020, 21, 478–494. [Google Scholar] [CrossRef] [PubMed]
  13. Mwita, J.C.; Souda, S.; Magafu, M.G.; Massele, A.; Godman, B.; Mwandri, M. Prophylactic antibiotics to prevent surgical site infections in Botswana: Findings and implications. Hosp. Pract. 2018, 46, 97–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Young, P.Y.; Khadaroo, R.G. Surgical site infections. Surg. Clin. N. Am. 2014, 94, 1245–1264. [Google Scholar] [CrossRef]
  15. Mangram, A.J.; Horan, T.C.; Pearson, M.L.; Silver, L.C.; Jarvis, W.R. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am. J. Infect. Control 1999, 27, 97–132. [Google Scholar] [CrossRef]
  16. Wenzel, R.P. Health Care–Associated Infections: Major Issues in the Early Years of the 21st Century. Clin. Infect. Dis. 2007, 45 (Suppl. 1), S85–S88. [Google Scholar] [CrossRef] [Green Version]
  17. Mwita, J.C.; Ogunleye, O.O.; Olalekan, A.; Kalungia, A.C.; Kurdi, A.; Saleem, Z.; Sneddon, J.; Godman, B. Key Issues Surrounding Appro-priate Antibiotic Use for Prevention of Surgical Site Infections in Low- and Middle-Income Countries: A Narrative Review and the Implications. Int. J. Gen. Med. 2021, 14, 515–530. [Google Scholar] [CrossRef]
  18. Cooper, L.; Sneddon, J.; Afriyie, D.K.; Sefah, I.A.; Kurdi, A.; Godman, B.; Seaton, R.A. Supporting global antimicrobial stew-ardship: Antibiotic prophylaxis for the prevention of surgical site infection in low- and middle-income countries (LMICs): A scoping review and meta-analysis. JAC Antimicrob. Resist. 2020, 2, dlaa070. [Google Scholar] [CrossRef]
  19. Jenks, P.; Laurent, M.; McQuarry, S.; Watkins, R. Clinical and economic burden of surgical site infection (SSI) and predicted financial consequences of elimination of SSI from an English hospital. J. Hosp. Infect. 2014, 86, 24–33. [Google Scholar] [CrossRef]
  20. Biccard, B.M.; Madiba, T.E.; Kluyts, H.L.; Munlemvo, D.M.; Madzimbamuto, F.D.; Basenero, A.; Gordon, C.S.; Youssouf, C.; Rakotoarison, S.R.; Gobin, V.; et al. Perioperative patient outcomes in the African Surgical Outcomes Study: A 7-day prospective observational cohort study. Lancet 2018, 391, 1589–1598. [Google Scholar] [CrossRef] [Green Version]
  21. Badia, J.M.; Casey, A.L.; Petrosillo, N.; Hudson, P.; Mitchell, S.; Crosby, C. Impact of surgical site infection on healthcare costs and patient outcomes: A systematic review in six European countries. J. Hosp. Infect. 2017, 96, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Korol, E.; Johnston, K.; Waser, N.; Sifakis, F.; Jafri, H.; Lo, M.; Kyaw, M.H. A Systematic Review of Risk Factors Associated with Surgical Site Infections among Surgical Patients. PLoS ONE 2013, 8, e83743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Ahuja, S.; Peiffer-Smadja, N.; Peven, K.; White, M.; Leather, A.J.M.; Singh, S.; Mendelson, M.; Holmes, A.; Birgand, G.; Sevdalis, N.; et al. Use of Feedback Data to Reduce Surgical Site Infections and Optimize Antibiotic Use in Surgery: A Systematic Scoping Review. Ann. Surg. 2022, 275, e345–e352. [Google Scholar] [CrossRef] [PubMed]
  24. Olowo-Okere, A.; Ibrahim, Y.E.; Olayinka, B.; Ehinmidu, J. Epidemiology of surgical site infections in Nigeria: A systematic review and meta-analysis. Niger. Postgrad. Med. J. 2019, 26, 143–151. [Google Scholar] [CrossRef]
  25. Aiken, A.M.; Wanyoro, A.K.; Mwangi, J.; Juma, F.; Mugoya, I.K.; Scott, J.A. Changing use of surgical antibiotic prophylaxis in Thika Hospital, Kenya: A quality improvement intervention with an interrupted time series design. PLoS ONE 2013, 8, e78942. [Google Scholar] [CrossRef]
  26. Mahmoud, N.N.; Turpin, R.S.; Yang, G.; Saunders, W.B. Impact of Surgical Site Infections on Length of Stay and Costs in Selected Colorectal Procedures. Surg. Infect. 2009, 10, 539–544. [Google Scholar] [CrossRef] [PubMed]
  27. Sattar, F.; Sattar, Z.; Zaman, M.; Akbar, S. Frequency of Post-operative Surgical Site Infections in a Tertiary Care Hospital in Abbottabad, Pakistan. Cureus 2019, 11, e4243. [Google Scholar] [CrossRef] [Green Version]
  28. Malik, A.Z.; Ali, Q. Surgical Site Infections after Elective Surgery in Pakistan: Surgipak Study. J. Rawalpindi Med. Coll. 2015. [Google Scholar]
  29. Butt, S.Z.; Ahmad, M.; Saeed, H.; Saleem, Z.; Javaid, Z. Post-surgical antibiotic prophylaxis: Impact of pharmacist’s educational intervention on appropriate use of antibiotics. J. Infect. Public Health 2019, 12, 854–860. [Google Scholar] [CrossRef]
  30. Martinez-Sobalvarro, J.V.; Júnior, A.A.P.; Pereira, L.B.; Baldoni, A.O.; Ceron, C.S.; Dos Reis, T.M. Antimicrobial steward-ship for surgical antibiotic prophylaxis and surgical site infections: A systematic review. Int. J. Clin. Pharm. 2022, 44, 301–319. [Google Scholar] [CrossRef]
  31. Abubakar, U. Point-prevalence survey of hospital acquired infections in three acute care hospitals in Northern Nigeria. Antimicrob. Resist. Infect. Control 2020, 9, 63. [Google Scholar] [CrossRef] [PubMed]
  32. Culver, D.H.; Horan, T.C.; Gaynes, R.P.; Martone, W.J.; Jarvis, W.R.; Emori, T.G.; Banerjee, S.N.; Edwards, J.R.; Tolson, J.S.; Henderson, T.S.; et al. Surgical wound infection rates by wound class, operative procedure, and patient risk index. National Nosocomial Infections Surveillance System. Am. J. Med. 1991, 91, 152s–157s. [Google Scholar] [CrossRef] [PubMed]
  33. WHO. The WHO AWaRe (Access, Watch, Reserve) Antibiotic Book. 2022. Available online: https://www.who.int/publications/i/item/9789240062382 (accessed on 23 February 2023).
  34. Maleknejad, A.; Dastyar, N.; Badakhsh, M.; Balouchi, A.; Rafiemanesh, H.; Al Rawajfah, O.; Keikhaie, K.R.; Sheyback, M. Surgical site infections in Eastern Mediterranean region: A systematic review and meta-analysis. Infect. Dis. 2019, 51, 719–729. [Google Scholar] [CrossRef] [PubMed]
  35. Bratzler, D.W.; Dellinger, E.P.; Olsen, K.M.; Perl, T.M.; Auwaerter, P.G.; Bolon, M.K.; Fish, D.N.; Napolitano, L.M.; Sawyer, R.G.; Slain, D.; et al. Clinical Practice Guidelines for Antimicrobial Prophylaxis in Surgery. Surg. Infect. 2013, 14, 73–156. [Google Scholar] [CrossRef] [Green Version]
  36. Bull, A.L.; Worth, L.J.; Spelman, T.; Richards, M.J. Antibiotic Prescribing Practices for Prevention of Surgical Site In-fections in Australia: Increased Uptake of National Guidelines after Surveillance and Reporting and Impact on Infection Rates. Surg. Infect. 2017, 18, 834–840. [Google Scholar] [CrossRef]
  37. Crader, M.F.; Varacallo, M. Preoperative Antibiotic Prophylaxis. StatPearls; Treasure Island (FL): StatPearls Publishing Copyright © 2022; StatPearls Publishing LLC.: Tampa, FL, USA, 2022. [Google Scholar]
  38. Malhotra, N.R.; Piazza, M.; Demoor, R.; McClintock, S.D.; Hamilton, K.; Sharma, N.; Osiemo, B.; Berger, I.; Hossain, E.; Borovskiy, Y.; et al. Impact of Reduced Preincision Antibiotic Infusion Time on Surgical Site Infection Rates: A Retrospective Cohort Study. Ann. Surg. 2020, 271, 774–780. [Google Scholar] [CrossRef]
  39. Branch-Elliman, W.; O’Brien, W.; Strymish, J.; Itani, K.; Wyatt, C.; Gupta, K. Association of Duration and Type of Surgical Prophylaxis with Antimicrobial-Associated Adverse Events. JAMA Surg. 2019, 154, 590–598. [Google Scholar] [CrossRef]
  40. Harbarth, S.; Samore, M.H.; Lichtenberg, D.; Carmeli, Y. Prolonged antibiotic prophylaxis after cardiovascular surgery and its effect on surgical site infections and antimicrobial resistance. Circulation 2000, 101, 2916–2921. [Google Scholar] [CrossRef] [Green Version]
  41. Hawn, M.T.; Knowlton, L.M. Balancing the Risks and Benefits of Surgical Prophylaxis: Timing and Duration Do Matter. JAMA Surg. 2019, 154, 598–599. [Google Scholar] [CrossRef]
  42. Najjar, P.A.; Smink, D.S. Prophylactic Antibiotics and Prevention of Surgical Site Infections. Surg. Clin. N. Am. 2015, 95, 269–283. [Google Scholar] [CrossRef]
  43. de Jonge, S.W.; Gans, S.L.; Atema, J.J.; Solomkin, J.S.; Dellinger, P.E.; Boermeester, M.A. Timing of preoperative antibiotic prophylaxis in 54,552 patients and the risk of surgical site infection: A systematic review and meta-analysis. Medicine 2017, 96, e6903. [Google Scholar] [CrossRef] [PubMed]
  44. Alemkere, G. Antibiotic usage in surgical prophylaxis: A prospective observational study in the surgical ward of Nekemte referral hospital. PLoS ONE 2018, 13, e0203523. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Burke, J.P. Maximizing Appropriate Antibiotic Prophylaxis for Surgical Patients: An Update from LDS Hospital, Salt Lake City. Clin. Infect. Dis. 2001, 33, S78–S83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Allegranzi, B.; Zayed, B.; Bischoff, P.; Kubilay, N.Z.; de Jonge, S.; de Vries, F.; Gomes, S.M.; Gans, S.; Wallert, E.D.; Wu, X.; et al. New WHO recommendations on intraoperative and postoperative measures for surgical site infection prevention: An evidence-based global perspective. Lancet Infect. Dis. 2016, 16, e288–e303. [Google Scholar] [CrossRef]
  47. Dellit, T.H.; Owens, R.C.; McGowan, J.E.; Gerding, D.N.; Weinstein, R.A.; Burke, J.P.; Huskins, W.C.; Paterson, D.L.; Fishman, N.O.; Carpenter, C.F.; et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America Guidelines for Developing an Institutional Program to Enhance Antimicrobial Stewardship. Clin. Infect. Dis. 2007, 44, 159–177. [Google Scholar] [CrossRef]
  48. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [CrossRef]
  49. Ng, R.S.; Chong, C.P. Surgeons’ adherence to guidelines for surgical antimicrobial prophylaxis—A review. Australas Med. J. 2012, 5, 534–540. [Google Scholar] [CrossRef]
  50. Ayele, Y.; Taye, H. Antibiotic utilization pattern for surgical site infection prophylaxis at Dil Chora Referral Hospital Surgical Ward, Dire Dawa, Eastern Ethiopia. BMC Res. Notes 2018, 11, 537. [Google Scholar] [CrossRef]
  51. van Kasteren, M.E.; Kullberg, B.J.; de Boer, A.S.; Mintjes-de Groot, J.; Gyssens, I.C. Adherence to local hospital guidelines for surgical antimicrobial prophylaxis: A multicentre audit in Dutch hospitals. J. Antimicrob. Chemother 2003, 51, 1389–1396. [Google Scholar] [CrossRef] [Green Version]
  52. Saleem, Z.; Hassali, M.A.; Versporten, A.; Godman, B.; Hashmi, F.K.; Goossens, H.; Saleem, F. A multicenter point prevalence survey of antibiotic use in Punjab, Pakistan: Findings and implications. Expert Rev. Anti-Infect. Ther. 2019, 17, 285–293. [Google Scholar] [CrossRef] [Green Version]
  53. Saleem, Z.; Hassali, M.A.; Hashmi, F.K.; Godman, B.; Ahmed, Z. Snapshot of antimicrobial stewardship programs in the hospitals of Pakistan: Findings and implications. Heliyon 2019, 5, e02159. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Mustafa, Z.U.; Majeed, H.K.; Latif, S.; Salman, M.; Hayat, K.; Mallhi, T.H.; Khan, Y.H.; Khan, A.H.; Abubakar, U.; Sultana, K.; et al. Adherence to Infection Prevention and Control Measures Among Health-Care Workers Serving in COVID-19 Treatment Centers in Punjab, Pakistan. Disaster Med. Public Health Prep. 2023, 17, e298. [Google Scholar] [CrossRef] [PubMed]
  55. Khan, Z.; Ahmed, N.; Rehman, A.; Khan, F.U.; Saqlain, M.; Martins, M.A.P.; Rahman, H. Audit of pre-operative antibiotic prophylaxis usage in elective surgical procedures in two teaching hospitals, Islamabad, Pakistan: An observational cross-sectional study. PLoS ONE 2020, 15, e0231188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Saleem, Z.; Haseeb, A.; Godman, B.; Batool, N.; Altaf, U.; Ahsan, U.; Khan, F.U.; Mustafa, Z.U.; Nadeem, M.U.; Farrukh, M.J.; et al. Point Prevalence Survey of Antimicrobial Use during the COVID-19 Pandemic among Different Hospitals in Pakistan: Findings and Implications. Antibiotics 2023, 12, 70. [Google Scholar] [CrossRef]
  57. Sharland, M.; Pulcini, C.; Harbarth, S.; Zeng, M.; Gandra, S.; Mathur, S.; Magrini, N. Classifying antibiotics in the WHO Essential Medicines List for optimal use-be AWaRe. Lancet Infect. Dis. 2018, 18, 18–20. [Google Scholar] [CrossRef] [Green Version]
  58. Sharland, M.; Gandra, S.; Huttner, B.; Moja, L.; Pulcini, C.; Zeng, M.; Mendelson, M.; Cappello, B.; Cooke, G.; Magrini, N.; et al. Encouraging AWaRe-ness and discouraging inappropriate antibiotic use—The new 2019 Essential Medicines List becomes a global antibiotic stewardship tool. Lancet Infect. Dis. 2019, 19, 1278–1280. [Google Scholar] [CrossRef]
  59. Sharland, M.; Zanichelli, V.; Ombajo, L.A.; Bazira, J.; Cappello, B.; Chitatanga, R.; Chuki, P.; Gandra, S.; Getahun, H.; Harbarth, S.; et al. The WHO essential medicines list AWaRe book: From a list to a quality improvement system. Clin. Microbiol. Infect. 2022, 28, 1533–1535. [Google Scholar] [CrossRef]
  60. Sulis, G.; Sayood, S.; Katukoori, S.; Bollam, N.; George, I.; Yaeger, L.H.; Chavez, M.A.; Tetteh, E.; Yarrabelli, S.; Pulcini, C.; et al. Exposure to World Health Organization’s AWaRe antibiotics and isolation of multidrug resistant bacteria: A systematic review and meta-analysis. Clin. Microbiol. Infect. 2022, 28, 1193–1202. [Google Scholar] [CrossRef]
  61. Pauwels, I.; Versporten, A.; Drapier, N.; Vlieghe, E.; Goossens, H.; Koraqi, A.; Hoxha, I.; Tafaj, S.; Cornistein, W.; Quiros, R.; et al. Hospital antibiotic prescribing patterns in adult patients according to the WHO Access, Watch and Reserve classification (AWaRe): Results from a worldwide point prevalence survey in 69 countries. J. Antimicrob. Chemother. 2021, 76, 1614–1624. [Google Scholar] [CrossRef]
  62. Saleem, Z.; Hassali, M.A.; Hashmi, F.K. Pakistan’s national action plan for antimicrobial resistance: Translating ideas into reality. Lancet Infect. Dis. 2018, 18, 1066–1067. [Google Scholar] [CrossRef]
  63. Mustafa, Z.U.; Saleem, M.S.; Ikram, M.N.; Salman, M.; Butt, S.A.; Khan, S.; Godman, B.; Seaton, R.A. Co-infections and antimicrobial use among hospitalized COVID-19 patients in Punjab, Pakistan: Findings from a multicenter, point prevalence survey. Pathog. Glob. Health 2022, 116, 421–427. [Google Scholar] [CrossRef] [PubMed]
  64. Ramzan, K.; Shafiq, S.; Raees, I.; Mustafa, Z.U.; Salman, M.; Khan, A.H.; Meyer, J.C.; Godman, B. Co-Infections, Secondary Infections, and Antimicrobial Use in Patients Hospitalized with COVID-19 during the First Five Waves of the Pandemic in Pakistan; Findings and Implications. Antibiotics 2022, 11, 789. [Google Scholar] [CrossRef] [PubMed]
  65. Saleem, Z.; Godman, B.; Azhar, F.; Kalungia, A.C.; Fadare, J.; Opanga, S.; Markovic-Pekovic, V.; Hoxha, I.; Saeed, A.; Al-Gethamy, M.; et al. Progress on the national action plan of Pakistan on antimicrobial resistance (AMR): A narrative review and the implications. Expert Rev. Anti-Infect. Ther. 2022, 20, 71–93. [Google Scholar] [CrossRef] [PubMed]
  66. Cox, J.A.; Vlieghe, E.; Mendelson, M.; Wertheim, H.; Ndegwa, L.; Villegas, M.V.; Gould, I.; Hara, G.L. Antibiotic stewardship in low- and middle-income countries: The same but different? Clin. Microbiol. Infect. 2017, 23, 812–818. [Google Scholar] [CrossRef] [Green Version]
  67. American College of Surgeons—ACS NSQIP Participant Use Data File. Available online: https://www.facs.org/quality-programs/data-and-registries/acs-nsqip/participant-use-data-file/ (accessed on 20 February 2023).
  68. Nusrat, N.; Haque, M.; Chowdhury, K.; Adnan, N.; Lutfor, A.B.; Karim, E.; Hassan, M.; Rabbany, A.; BeguM, D.; Hasan, M.N. Pilot Study on the Current Management of Children with COVID-19 In Hospitals in Bangladesh; Findings and Implications. Bangladesh J. Med. Sci. 2021, 20, 188–198. [Google Scholar] [CrossRef]
  69. WHO Anatomical Therapeutic Chemical (ATC) Classification. 2021. Available online: https://www.who.int/tools/atc-ddd-toolkit/atc-classification (accessed on 20 February 2023).
  70. Ariyo, P.; Zayed, B.; Riese, V.; Anton, B.; Latif, A.; Kilpatrick, C.; Allegranzi, B.; Berenholtz, S. Implementation strategies to reduce surgical site infections: A systematic review. Infect. Control Hosp. Epidemiol. 2019, 40, 287–300. [Google Scholar] [CrossRef]
  71. Franco, L.M.; Cota, G.F.; Pinto, T.S.; Ercole, F.F. Preoperative bathing of the surgical site with chlorhexidine for infection prevention: Systematic review with meta-analysis. Am. J. Infect. Control 2017, 45, 343–349. [Google Scholar] [CrossRef]
  72. Shi, D.; Yao, Y.; Yu, W. Comparison of preoperative hair removal methods for the reduction of surgical site infections: A meta-analysis. J. Clin. Nurs. 2017, 26, 2907–2914. [Google Scholar] [CrossRef]
  73. Yao, R.; Tan, T.; Tee, J.W.; Street, J. Prophylaxis of surgical site infection in adult spine surgery: A systematic review. J. Clin. Neurosci. 2018, 52, 5–25. [Google Scholar] [CrossRef]
  74. Schreiber, P.W.; Sax, H.; Wolfensberger, A.; Clack, L.; Kuster, S.P.; Swissnoso. The preventable proportion of healthcare-associated infections 2005–2016: Systematic review and meta-analysis. Infect. Control Hosp. Epidemiol. 2018, 39, 1277–1295. [Google Scholar] [CrossRef] [Green Version]
  75. Boonchan, T.; Wilasrusmee, C.; McEvoy, M.; Attia, J.; Thakkinstian, A. Network meta-analysis of antibiotic prophylaxis for prevention of surgical-site infection after groin hernia surgery. Br. J. Surg. 2017, 104, e106–e117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. De Simone, B.; Sartelli, M.; Coccolini, F.; Ball, C.G.; Brambillasca, P.; Chiarugi, M.; Campanile, F.C.; Nita, G.; Corbella, D.; Leppaniemi, A.; et al. Intraoperative surgical site infection control and prevention: A position paper and future addendum to WSES intra-abdominal infections guidelines. World J. Emerg. Surg. 2020, 15, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Godman, B.; Basu, D.; Pillay, Y.; Mwita, J.C.; Rwegerera, G.M.; Anand Paramadhas, B.D.; Tiroyakgosi, C.; Okwen, P.H.; Niba, L.L.; Nonvignon, J.; et al. Review of Ongoing Activities and Challenges to Improve the Care of Patients with Type 2 Diabetes Across Africa and the Implications for the Future. Front. Pharmacol. 2020, 11, 108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Ogunleye, O.O.; Basu, D.; Mueller, D.; Sneddon, J.; Seaton, R.A.; Yinka-Ogunleye, A.F.; Wamboga, J.; Miljkovic, N.; Mwita, J.C.; Rwegerera, G.M.; et al. Response to the Novel Co-rona Virus (COVID-19) Pandemic Across Africa: Successes, Challenges, and Implications for the Future. Front. Pharmacol. 2020, 11, 1205. [Google Scholar] [CrossRef] [PubMed]
  79. Ouedraogo, A.S.; Versporten, A.; Nagalo, A.; Pauwels, I.; Goossens, H.; Ouedraogo, A.; Poda, A. The Global Point Prevalence Survey of Antimicrobial Consumption and Resistance (Global-PPS)—Results of Antimicrobial Prescribing in Burkina Faso. 2019. Available online: https://www.global-pps.com/wp-content/uploads/2021/02/The-Global-PPS_results-of-antimicrobial-prescribing-in-Burkina-Faso.pdf (accessed on 18 February 2023).
  80. Bunduki, G.K.; Mukululi, M.P.; Masumbuko, C.K.; Uwonda, S.A. Compliance of antibiotics used for surgical site infection prophylaxis among patients undergoing surgery in a Congolese teaching hospital. Infect. Prev. Pract. 2020, 2, 100075. [Google Scholar] [CrossRef]
  81. Ashour, R.H.; Abdelkader, E.A.; Hamdy, O.; Elmetwally, M.; Laimon, W.; Abd-Elaziz, M.A. The Pattern of Antimicrobial Prescription at a Tertiary Health Center in Egypt: A Point Survey and Implications. Infect. Drug Resist. 2022, 15, 6365–6378. [Google Scholar] [CrossRef]
  82. Fentie, A.M.; Degefaw, Y.; Asfaw, G.; Shewarega, W.; Woldearegay, M.; Abebe, E.; Gebretekle, G.B. Multicentre point-prevalence survey of antibiotic use and healthcare-associated infections in Ethiopian hospitals. BMJ Open 2022, 12, e054541. [Google Scholar] [CrossRef]
  83. Bediako-Bowan, A.A.A.; Owusu, E.; Labi, A.K.; Obeng-Nkrumah, N.; Sunkwa-Mills, G.; Bjerrum, S.; Opintan, J.A.; Bannerman, C.; Mølbak, K.; Kurtzhals, J.A.L.; et al. Antibiotic use in surgical units of selected hospitals in Ghana: A multi-centre point prevalence survey. BMC Public Health 2019, 19, 797. [Google Scholar] [CrossRef]
  84. D’Arcy, N.; Ashiru-Oredope, D.; Olaoye, O.; Afriyie, D.; Akello, Z.; Ankrah, D.; Asima, D.M.; Banda, D.C.; Barrett, S.; Brandish, C.; et al. Antibiotic Prescribing Patterns in Ghana, Uganda, Zambia and Tanzania Hospitals: Results from the Global Point Prevalence Survey (G-PPS) on Antimicrobial Use and Stewardship Interventions Implemented. Antibiotics 2021, 10, 1122. [Google Scholar] [CrossRef]
  85. Okoth, C.; Opanga, S.; Okalebo, F.; Oluka, M.; Baker Kurdi, A.; Godman, B. Point prevalence survey of antibiotic use and resistance at a referral hospital in Kenya: Findings and implications. Hosp. Pract. 2018, 46, 128–136. [Google Scholar] [CrossRef] [Green Version]
  86. Momanyi, L.; Opanga, S.; Nyamu, D.; Oluka, M.; Kurdi, A.; Godman, B. Antibiotic Prescribing Patterns at a Leading Referral Hospital in Kenya: A Point Prevalence Survey. J. Res. Pharm. Pract. 2019, 8, 149–154. [Google Scholar] [PubMed]
  87. Oduyebo, O.O.; Olayinka, A.T.; Iregbu, K.C.; Versporten, A.; Goossens, H.; Nwajiobi-Princewill, P.; Jimoh, O.; Ige, T.O.; Aigbe, A.I.; Ola-Bello, O.I.; et al. A point prevalence survey of antimicrobial prescribing in four Nigerian Tertiary Hospitals. Ann. Trop. Pathol. 2017, 8, 42–46. [Google Scholar] [CrossRef]
  88. Aboderin, A.O.; Adeyemo, A.T.; Olayinka, A.A.; Oginni, A.S.; Adeyemo, A.T.; Oni, A.A.; Olabisi, O.F.; Fayomi, O.D.; Anuforo, A.C.; Egwuenu, A.; et al. Antimicrobial use among hospitalized patients: A multi-center, point prevalence survey across public healthcare facilities, Osun State, Nigeria. Germs 2021, 11, 523–535. [Google Scholar] [CrossRef] [PubMed]
  89. Ogunleye, O.O.; Oyawole, M.R.; Odunuga, P.T.; Kalejaye, F.; Yinka-Ogunleye, A.F.; Olalekan, A.; Ogundele, S.O.; Ebruke, B.E.; Richard, A.K.; Paramadhas, B.D.; et al. A multicentre point prevalence study of antibiotics utilization in hospitalized patients in an urban secondary and a tertiary healthcare facilities in Nigeria: Findings and implications. Expert Rev. Anti-Infect. Ther. 2022, 20, 297–306. [Google Scholar] [CrossRef]
  90. Nkurunziza, T.; Kateera, F.; Sonderman, K.; Gruendl, M.; Nihiwacu, E.; Ramadhan, B.; Cherian, T.; Nahimana, E.; Ntakiyiruta, G.; Habiyakare, C.; et al. Prevalence and predictors of surgical-site infection after caesarean section at a rural district hospital in Rwanda. Br. J. Surg. 2019, 106, e121–e128. [Google Scholar] [CrossRef] [Green Version]
  91. Horumpende, P.G.; Mshana, S.E.; Mouw, E.F.; Mmbaga, B.T.; Chilongola, J.O.; de Mast, Q. Point prevalence survey of antimicrobial use in three hospitals in North-Eastern Tanzania. Antimicrob. Resist. Infect. Control 2020, 9, 149. [Google Scholar] [CrossRef]
  92. Ayed, H.B.; Yaich, S.; Trigui, M.; Jemaa, M.B.; Hmida, M.B.; Karray, R.; Kassis, M.; Mejdoub, Y.; Feki, H.; Jedidi, J.; et al. Prevalence and risk factors of health care-associated infections in a limited resources country: A cross-sectional study. Am. J. Infect. Control 2019, 47, 945–950. [Google Scholar] [CrossRef]
  93. Kiggundu, R.; Wittenauer, R.; Waswa, J.P.; Nakambale, H.N.; Kitutu, F.E.; Murungi, M.; Okuna, M.; Morries, S.; Lawry, L.L.; Joshi, M.P.; et al. Point Prevalence Survey of Antibiotic Use across 13 Hospitals in Uganda. Antibiotics 2022, 11, 199. [Google Scholar] [CrossRef]
  94. Nassr, O.A.; Abd Alridha, A.M.; Naser, R.A.; Abbas, R.S. Antibiotic prescribing in the acute care in Iraq. Int. J. Pharmacol. Pharm. Sci. 2018, 12, 485–489. [Google Scholar]
  95. Kurmanji, J.M.; Hassali, A.; Versporten, A.; Younus, M.; Pauwels, I.; Goossens, H.; Alnedawi, Z. Global Point Prevalence Survey in Five Teaching Hospitals in Baghdad, Iraq. Mediterr. J. Infect. Microbes Antimicrob.-Als/Infect. Dis. Clin. Microbiol. Spec. Soc. Turk. 2021, 10, 17. [Google Scholar] [CrossRef]
  96. Abu Hammour, K.; Al-Heyari, E.; Allan, A.; Versporten, A.; Goossens, H.; Abu Hammour, G.; Manaseer, Q. Antimicrobial Consumption and Resistance in a Tertiary Care Hospital in Jordan: Results of an Internet-Based Global Point Prevalence Survey. Antibiotics 2020, 9, 598. [Google Scholar] [CrossRef] [PubMed]
  97. Skosana, P.P.; Schellack, N.; Godman, B.; Kurdi, A.; Bennie, M.; Kruger, D.; Meyer, J.C. A point prevalence survey of antimicrobial utilisation patterns and quality indices amongst hospitals in South Africa; findings and implications. Expert Rev. Anti-Infect. Ther. 2021, 19, 1353–1366. [Google Scholar] [CrossRef] [PubMed]
  98. Skosana, P.P.; Schellack, N.; Godman, B.; Kurdi, A.; Bennie, M.; Kruger, D.; Meyer, J.C. A national, multicentre, web-based point prevalence survey of antimicrobial use and quality indices among hospitalised paediatric patients across South Africa. J. Glob. Antimicrob. Resist. 2022, 29, 542–550. [Google Scholar] [CrossRef] [PubMed]
  99. Adekoya, I.; Maraj, D.; Steiner, L.; Yaphe, H.; Moja, L.; Magrini, N.; Cooke, G.; Loeb, M.; Persaud, N. Comparison of antibiotics included in national essential medicines lists of 138 countries using the WHO Access, Watch, Reserve (AWaRe) classification: A cross-sectional study. Lancet Infect. Dis. 2021, 21, 1429–1440. [Google Scholar] [CrossRef] [PubMed]
  100. Allegranzi, B.; Aiken, A.M.; Zeynep Kubilay, N.; Nthumba, P.; Barasa, J.; Okumu, G.; Mugarura, R.; Elobu, A.; Jombwe, J.; Maimbo, M.; et al. A multimodal infection control and patient safety intervention to reduce surgical site infections in Africa: A multicentre, before-after, cohort study. Lancet Infect. Dis. 2018, 18, 507–515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  101. Saied, T.; Hafez, S.F.; Kandeel, A.; El-kholy, A.; Ismail, G.; Aboushady, M.; Attia, E.; Hassaan, A.; Abdel-Atty, O.; Elfekky, E.; et al. Antimicrobial stewardship to optimize the use of antimicrobials for surgical prophylaxis in Egypt: A multicenter pilot intervention study. Am. J. Infect. Control. 2015, 43, e67–e71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  102. Shankar, R. Implementation of the WHO Surgical Safety Checklist at a teaching hospital in India and evaluation of the effects on perioperative complications. Int. J. Health Plann. Manag. 2018, 33, 836–846. [Google Scholar] [CrossRef]
  103. Mahmoudi, L.; Ghouchani, M.; Mahi-Birjand, M.; Bananzadeh, A.; Akbari, A. Optimizing compliance with surgical antimicrobial prophylaxis guidelines in patients undergoing gastrointestinal surgery at a referral teaching hospital in southern Iran: Clinical and economic impact. Infect. Drug Resist. 2019, 12, 2437–2444. [Google Scholar] [CrossRef] [Green Version]
  104. Ntumba, P.; Mwangi, C.; Barasa, J.; Aiken, A.; Kubilay, Z.; Allegranzi, B. Multimodal approach for surgical site infection prevention—Results from a pilot site in Kenya. Antimicrob. Resist. Infect. Control 2015, 4, P87. [Google Scholar] [CrossRef] [Green Version]
  105. Kim, R.Y.; Kwakye, G.; Kwok, A.C.; Baltaga, R.; Ciobanu, G.; Merry, A.F.; Funk, L.M.; Lipsitz, S.R.; Gawande, A.A.; Berry, W.R.; et al. Sustainability and long-term effectiveness of the WHO surgical safety checklist combined with pulse oximetry in a resource-limited setting: Two-year update from Moldova. JAMA Surg. 2015, 150, 473–479. [Google Scholar] [CrossRef] [Green Version]
  106. Abubakar, U.; Syed Sulaiman, S.A.; Adesiyun, A.G. Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS ONE 2019, 14, e0213395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Alam, A.; Rehman, A.U.; Waheed, D.; Khan, M.H.; Ahmad, W.; Bashir, I.; Ullah, A.; Khan, I.U. Post-operative oral antibiotics in reducing frequency of surgical site infection following non-perforated appendectomy in population of South Waziristan Agency, Pakistan. Gomal J. Med. Sci. 2021, 19, 53–57. [Google Scholar] [CrossRef]
  108. Brink, A.J.; Messina, A.P.; Feldman, C.; Richards, G.A.; van den Bergh, D. From guidelines to practice: A pharma-cist-driven prospective audit and feedback improvement model for peri-operative antibiotic prophylaxis in 34 South African hospitals. J Antimicrob. Chemother 2017, 72, 1227–1234. [Google Scholar] [CrossRef] [Green Version]
  109. Bozkurt, F.; Kaya, S.; Tekin, R.; Gulsun, S.; Deveci, O.; Dayan, S.; Hoşoglu, S. Analysis of antimicrobial consumption and cost in a teaching hospital. J. Infect. Public Health 2014, 7, 161–169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  110. Karaali, C.; Emiroglu, M.; Atalay, S.; Sert, I.; Dursun, A.; Kose, S.; Akbulut, G.; Aydın, C. A new antibiotic stewardship program approach is effective on inappropriate surgical prophylaxis and discharge prescription. J. Infect. Dev. Ctries 2019, 13, 961–967. [Google Scholar] [CrossRef]
Table
Table 1. Sociodemographic characteristics and medical conditions.
Table 1. Sociodemographic characteristics and medical conditions.
VariableFrequency (N = 583)
Demographics
Age42.2 ± 18.4
Sex
Male299 (51.3%)
Female284 (48.7%)
Comorbidities
Diabetes mellitus27 (4.6%)
Hypertension16 (2.7%)
Hepatitis 14 (2.4%)
Heart disease 5 (0.9%)
Clinical Presentation
Ward
General surgery 268 (50%)
Orthopedic214 (36.7%)
Gynecological 101 (17.3%)
Top Three Complaints on Hospital Admission
Pain 70 (12%)
Swelling 45 (7.7%)
Pus discharge 12 (2.1%)
Diagnosis
Bone Infections
Osteomyelitis160 (27.4%)
Internal Fracture54 (9.2%)
Intra-abdominal Infections
Cholelithiasis78 (13.4%)
Hernia50 (8.6%)
Appendicitis33 (5.7%)
Full term delivery80 (13.8%)
Fibroids21 (3.7%)
Skin and Soft Tissue Infections
Abscess71 (12.1%)
Diabetic foot 36 (6.1%)
Hospital Stay
Total duration in hospital (days), including pre-operatively4.9 ± 3.8
Table
Table 2. Surgical procedure performed.
Table 2. Surgical procedure performed.
Surgical ProceduresFrequency (%)
Implant Fixation Due to Removal of Dead Bone (Dirty Wound)160 (27.4)
Caesarean section (Clean Contaminated Wound)80 (13.8)
Lap Cholecystectomy (Clean Contaminated Wound)78 (13.4)
Abscess Drainage (Dirty Wound)71 (12.3)
Implant Fixation Due to Fracture (Clean Wound)54 (9.2)
Hernia Repair (Clean Wound)50 (8.6)
Amputation Due to Diabetic Foot Necrosis (Dirty Wound)36 (6.1)
Appendectomy (Contaminated Wound)33 (5.6)
Hysterectomy (Clean Contaminated Wound)21 (3.6)
Table
Table 3. Utilization pattern of antibiotics among surgical patients.
Table 3. Utilization pattern of antibiotics among surgical patients.
AntibioticsWHO AwaRe ClassificationWound TypesTotal
N (%)
Clean
N (%)		Clean/Contaminated n (%)Contaminated
n (%)		Dirty
n (%)
Penicillins
Piperacillin + Tazobactam (J01CR05)Watch2 (1)25 (7.1)2 (4)111 (20.1)140 (12.1)
Co-amoxiclav (J01CR02)Access38 (19)18 (5.1)12 (24.4)5 (0.9)73 (6.3)
Cephalosporins
Cefoperazone + Sulbactam (J01DD62)Watch20 (10)78(22.2)12 (24.4)120 (21.8)230 (20)
Ceftriaxone (J01DD04) Watch10 (5)15 (4.2)6 (12.2)61 (11)92 (8)
Cefazolin (J01DB04)Access40 (20)26 (7.4)--66 (5.7)
Cefuroxime (J01DC02)Watch10 (5)30 (8.5)-10 (1.8)50 (4.3)
Cephradine (J01DB09)Access22 (11)8 (2.2)--30 (2.6)
Cefixime (J01DD08)Watch16 (8)13 (3.7)--29 (2.5)
Fluoroquinolones
Ciprofloxacin (J01MA02)Watch16 (9)30 (8.5)8 (16.2)3 (0.5)59 (5.1)
Moxifloxacin (J01MA14)Watch4 (2)20 (5.7)3 (6.1)-27 (2.3)
Aminoglycosides
Amikacin (J01GB06)Access8 (4)26 (7.4)-120 (21.8)154 (13.4)
Others
Metronidazole (J01XD01)Access12 (6)61 (17.4)4 (8.1)95 (17.2)172 (14.9)
Vancomycin (J01XA01)Watch--2 (4)25 (4.5)27 (2.3)
Total antimicrobials200 (17.4)350 (30.4)49 (4.2)550 (47.8)1149 (100)
NB: ‘A’ = access antibiotic, ‘W’ = watch antibiotic according to the AWaRe classification (see Section 4.2 for details).
Table
Table 4. Surgical wound classifications by ACS-NSQIP *.
Table 4. Surgical wound classifications by ACS-NSQIP *.
Wound TypeDefinition
CleanUninfected operative wounds without inflammation or involvement of the respiratory, alimentary, genital or uninfected urinary tracts
Clean/ContaminatedOperative wounds in which the respiratory, alimentary, genital or urinary tract is entered under controlled conditions and without unusual contamination
ContaminatedOpen, fresh, accidental wounds; operations with major breaks in sterile technique or gross spillage from the gastrointestinal tract; and incisions in which acute, non-purulent inflammation is encountered
DirtyOld traumatic wounds with retained devitalized tissue and involvement of existing clinical infection or perforated viscera
NB: * American College of Surgeons National Surgical Quality Improvement Program.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Saleem, Z.; Ahsan, U.; Haseeb, A.; Altaf, U.; Batool, N.; Rani, H.; Jaffer, J.; Shahid, F.; Hussain, M.; Amir, A.; et al. Antibiotic Utilization Patterns for Different Wound Types among Surgical Patients: Findings and Implications. Antibiotics 2023, 12, 678. https://doi.org/10.3390/antibiotics12040678

AMA Style

Saleem Z, Ahsan U, Haseeb A, Altaf U, Batool N, Rani H, Jaffer J, Shahid F, Hussain M, Amir A, et al. Antibiotic Utilization Patterns for Different Wound Types among Surgical Patients: Findings and Implications. Antibiotics. 2023; 12(4):678. https://doi.org/10.3390/antibiotics12040678

Chicago/Turabian Style

Saleem, Zikria, Umar Ahsan, Abdul Haseeb, Ummara Altaf, Narjis Batool, Hira Rani, Javeria Jaffer, Fatima Shahid, Mujahid Hussain, Afreenish Amir, and et al. 2023. "Antibiotic Utilization Patterns for Different Wound Types among Surgical Patients: Findings and Implications" Antibiotics 12, no. 4: 678. https://doi.org/10.3390/antibiotics12040678

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