Next Article in Journal
Use of Geospatial Surveillance and Response Systems for Vector-Borne Diseases in the Elimination Phase
Previous Article in Journal
Cross-Generational Effects of Heat Stress on Fitness and Wolbachia Density in Aedes aegypti Mosquitoes

Trop. Med. Infect. Dis. 2019, 4(1), 14; https://doi.org/10.3390/tropicalmed4010014

Review
Nosocomial Pathogens: An In-Depth Analysis of the Vectorial Potential of Cockroaches
Department of Medical Microbiology, University of Ghana, Accra, Ghana
Received: 13 December 2018 / Accepted: 15 January 2019 / Published: 17 January 2019

Abstract

:
Nosocomial or healthcare-associated infections are regarded as the most frequent adverse event that threatens patients’ safety and has serious economic and social consequences. Cockroach infestation is common in many hospitals, especially in the developing world. Common nosocomial pathogens isolated from cockroaches include Staphylococcus aureus, Pseudomonas aeruginosa, Escherichia coli, and Klebsiella pneumoniae. Cockroaches also harbor epidemiologically significant antibiotic-resistant organisms, such as carbapenem-resistant Enterobacteriaceae, which complicate nosocomial infections. Therefore, cockroaches constitute an important vector for nosocomial pathogens, and there should be zero tolerance for their presence in healthcare facilities. This paper aims to elucidate the possible role of cockroaches in nosocomial infections by reviewing the relevant research publications.
Keywords:
Staphylococcus aureus; nosocomial infections; antibiotic resistance; cockroach

1. Introduction

Cockroaches are adapted to live in various environmental conditions and, consequently, they are found in every part of the world. There exist about 4000 species of cockroach [1], but only 30 are associated with human habitations, including the species Periplaneta americana, Blatella germanica, and Blatta orientalis [2]. Cockroaches are one of the most significant and objectionable pests. They are common in many human habitations, particularly in places where food is stored or handled. Apart from that, cockroaches are also frequently detected in hospital environments, such as wards and laboratory rooms. In a study of hospital rooms in Poland, B. germanica and B. orientalis were found in 70% and 40% of hospitals, respectively [3]. Another study at a hospital in Switzerland enumerated about 30 cockroaches (Ectobius vittiventris) in a single day, which were found hiding in oxygen masks in the intensive care unit [4]. Cockroaches feed readily on faeces, sputum, skin scrapings, and other human detritus, as well as on a variety of foodstuffs. The filthy behavior of cockroaches coupled with their nocturnal lifestyle make them potential vectors for a wide range of pathogenic microorganisms. The role of cockroaches in human infections had been inconclusive and an issue of debate for several years. Recently, there has been a plethora of research information that contributes significantly to our understanding of this subject. Unfortunately, there are hardly any review papers synthesizing the research data on a single platform to provide a global understanding of the role cockroaches may play in human infections. In this review article, the author aims to describe the significance and possible role of cockroaches in nosocomial infections.

2. Brief Overview of Nosocomial Infections

Nosocomial or healthcare-associated infections are regarded as the most frequent, adverse event that threatens patients’ safety [5,6,7]. For every 100 hospitalized patients at any given time, 7 in developed countries and 10 in developing countries will acquire at least one healthcare-associated infection [8]. The brunt of nosocomial infections appears to be borne by neonates, and the infections are responsible for 4–56% of all deaths caused in this age group [8,9,10]. Based on the anatomical site of infection, the main types of nosocomial infections are urinary tract infections, pneumonia, surgical site infection, and blood stream infections. While urinary tract infections are the most common nosocomial infection in developed countries, surgical site infections are the most common in developing countries, affecting up to one-third of operated patients, and this is up to nine times higher than in developed countries [8,9,10]. A wide range of microbial pathogens including bacteria, parasites, and viruses are implicated in nosocomial infections, though the majority of the infections are associated with bacteria [11,12,13,14]. Nosocomial pathogens tend to differ depending on patient populations, medical facilities, and even differences in the environment in which patient care is administered. Epidemiological evidence indicates that principal nosocomial pathogens include Staphylococcus aureus, Pseudomonas aeruginosa, Escherichia coli, Acinetobacter baumanii, and coagulase-negative staphylococcus [8,10,14]. There is also evidence of emerging nosocomial pathogens such as Cryptosporidium parvum, Helicobacter pylori, and hepatitis C virus [15]. The success of nosocomial pathogens is partly related to their persistence on surfaces in the hospital environment. Relevant nosocomial pathogens such as S. aureus and E. coli could persist on dry inanimate surfaces for several months [16]. The longer a nosocomial pathogen persists on a surface, the longer it may be a source of transmission in the hospital. Generally, a high inoculum of the nosocomial pathogen, high relative humidity (>70%), and low temperature (around 4 °C) will provide the best chance for long persistence [16,17].
Antibiotic resistance has emerged as a major problem in nosocomial infections and has very serious negative implications for the treatment of such infections, especially in the developing world [18,19,20]. Highly antibiotic-resistant strains frequently encountered in healthcare infections include methicillin-resistant S. aureus (MRSA), vancomycin-resistant Enterococci (VRE), carbapenem-resistant Enterobacteriaceae (CRE), and extended-spectrum beta-lactamase producing E. coli [21]. These bacterial strains account for the majority of outbreaks and mortality cases of healthcare infections. The most studied of these antibiotic-resistant strains appears to be MRSA, which is endemic in many hospitals worldwide, particularly in Europe, the United States, and Asia. In the United States, the annual incidence of invasive MRSA infections in hospitals is estimated to be 94,360, resulting in 18,650 deaths [22,23]. Data from 31 European countries showed that between 2007 and 2008, there were 27,711 episodes of MRSA blood stream infections with 5503 deaths [24]. Though MRSA is considered a nosocomial pathogen traditionally, it has emerged in the community in the last two decades and is responsible for several types of community-acquired infections [25,26,27,28]. Characteristically, healthcare-associated MRSA (HA-MRSA) and community-associated MRSA (CA-MRSA) are considered to be different from each other in terms of their epidemiology, genetic traits, and types of infections [29,30]. Only a few of the known HA-MRSA clones are responsible for the majority of infection, and different clones dominate in different geographical regions. For example, the ST239-SCCmecIII clone predominates in South American, Asia, and Africa [31,32]. The predominant clone in the United States is CC5-SCCmecII (USA100) [33,34], while in Europe it is CC22-SCCmecIV (EMRSA-15) [35,36,37,38,39,40]. It is important to note that replacement of these clones keep occurring in several geographical regions [41,42]. Studies on the evolution of the major HA-MRSA clones indicate strong evidence for a wide range of antibiotic-resistant mutations and mobile genetic elements that are associated with the emergence of these clones in hospital epidemics [43,44].
Healthcare infections have serious economic and social consequences. These infections take a heavy toll on patients and their families by causing prolonged hospital stays, potential disabilities, and mortality. According to the Centre for Disease Control in the United States, the cost of events related to healthcare-associated infections was, on average, $2100 and varied from $680 for urinary tract infections to $5683 for respiratory tract infections [45]. In the United Kingdom, healthcare-associated infections cost about £1 billion a year; £56 million is estimated to incur after patients are discharged from hospital [46]. In the developing world, information on costs related to healthcare-associated infections is limited and available only in a few countries. A study from Thailand reported that the extra costs associated with surgical site infections was U.S. $1091 [47], while another study in Turkey showed that extra cost for a patient with a nosocomial infection was U.S. $2026 [48]. The huge public health impact of nosocomial infections coupled with the associated financial costs underscores the need for effective prevention of these infections. This requires good hygienic practices including hand-washing of healthcare workers and disinfection of surfaces in the hospitals, microbiological surveillance of nosocomial pathogens using standard laboratory protocols, applying barrier precautions to high-risk patients, judicious use of antibiotics in the hospital, limiting the duration of use of intravascular catheters [17,21,45].

3. Evidence for the Role of Cockroaches in Human Infections

Compelling evidence incriminating cockroaches as vectors of human infections comes from a study by Tarshis [49] in the 1950s, which reported a correlation between lack of cockroach control and incidence of infectious hepatitis in Los Angeles, Southern California. Between 1956 and 1959, the Carmelitos Housing Project had 20 to 39% of hepatitis A cases in Los Angeles. However, in 1960, the incidence of hepatitis A at the housing project dropped to 6.6%, then further to 3.6% in 1961, and to 0.0% in 1962. It was observed that the drop in the incidence of hepatitis A occurred concurrently with about a 70% drop in the infestations of B. germanica, B. orientalis, and Supella longipalpa cockroaches at the Carmelitos Housing Project, which was the consequence of a concentrated pest control program. Around the same time, the incidence of the infection had been rising everywhere else in Los Angeles County that was not receiving the pest control service. The association of cockroaches with the hepatitis A epidemic in Los Angeles is interesting and demonstrates the huge extent of these insects as vectors of infectious agents implicated in human infections. The hepatitis A virus is present in the faeces of infected persons and is most often transmitted through consumption of contaminated water or food. The association of cockroaches with faeces and food makes their transmission of hepatitis A virus highly plausible. In the hepatitis A epidemic in Los Angeles, cockroaches traversing between the sewage system and the houses were pinpointed as the source of the epidemic.
Major experimental evidence supporting the role of cockroaches as vectors of microbial pathogens was found in a study by Kopanic et al. [50] in 1993. In that study, experiments were conducted to find out if individual cockroaches could acquire a naladixic acid-resistant strain of Salmonella Typhimurium from a contaminated food source and then transfer this microbe to uninfected cockroaches, food (eggs), and water. Cockroaches, food, and water were sampled after 24, 48, 72, and 96 hours and tested for S. Typhimurium. All three types of samples were positive for S. Typhimurium at each 24 h sampling period. The highest frequency of S. Typhimurium cross-contamination between infected and uninfected cockroaches occurred within 24 h and declined thereafter. Water sites were heavily contaminated throughout the 96 h test period. Eggs that had been exposed for 24 h to infected cockroaches contained a minimum of 75 S. Typhimurium cells per egg. These findings clearly show the vectorial potential of cockroaches in the contamination of food and water and their role as important agents of human infection.
In 2003, Imamura et al. [51], using H. pylori, provided an additional piece of experimental evidence implicating cockroaches as vectors of microbial pathogens. After a three-day fast, cockroaches were divided into two groups; one group was transferred onto agar plates of freshly grown H. pylori (challenge group), while the other was placed on sterile agar plates without H. pylori (control group). After 24 h, the cockroaches were transferred to disinfected containers and provided with sterile food and water. The external surfaces and excreta of the cockroaches were sampled for microbiological examination by culture, rapid urease test, and polymerase chain reaction. The investigators detected H. pylori in both excreta and external surfaces of the challenged group, though at higher levels in the excreta. In the excreta of the challenged group, H. pylori was culturable for a 24 h post-challenge, the urease test was positive for up to day 3, and the PCR analysis was positive for up to day 7. All of the controlled cockroach samples were negative for H. pylori.

4. Cockroaches and Nosocomial Pathogens

Cockroaches pose a concern in the hospital environment because they may serve as reservoirs and vectors for nosocomial pathogens. Microbial carriage of cockroaches in hospitals has been reported by several studies (Table 1) [52,53,54,55,56,57,58,59,60,61,62]. Generally, these studies seem to have focused on bacteria and, to some extent, parasites and fungi, while very little has been done on viruses. A study reported 19.7% carriage of rotavirus among cockroaches collected at a tertiary hospital in Ghana [61]. Rotavirus is the most common cause of severe and fatal diarrhea in young children worldwide and accounts for about half of the diarrheal disease hospitalizations of children under five years of age in developing countries [61,63,64,65,66,67]. Moreover, nosocomial rotavirus infection seems to be responsible for about 25% of all rotavirus-related hospitalizations, especially in immune-compromised children [68,69]. Thus, the occurrence of cockroaches in hospitals and homes could have serious health implications for children. As shown in Table 1, parasites carried by cockroaches that were sampled in hospitals are predominantly those implicated in gastroenteritis. Some of these gastrointestinal parasites are also implicated in nosocomial infections, suggesting that cockroaches could play a role in nosocomial parasitosis. For instance, Entamoeba histolytica is frequently implicated in parasitic nosocomial epidemics involving diarrhea [70,71,72], while Entamoeba coli and Endolimax nana are detected most frequently in nosocomial parasitosis involving transplantation [72]. Nosocomial invasive fungal infections are usually caused by Candida and Aspergillus [73,74]. Both fungi were reported to be carried by cockroaches sampled in the hospital environment [56,58]. This indicates that cockroaches may also have some relevance in nosocomial mycoses. A wide range of bacteria have been isolated from cockroaches in hospitals (Table 1). In one study, as many as 174 bacteria were isolated [60]. This highlights the close association of cockroaches and bacteria, which is not surprising given the broad habitat range of cockroaches and the ubiquitous nature of bacteria. As shown in Table 1, the bacterial florae isolated from cockroaches in different countries in the developed and developing world, appear to be similar. This suggests that the type of bacterial flora carried by cockroaches may be independent of geographical location or socio-economic factors. Several of these bacterial agents including S. aureus, E. coli, P.s aeruginosa, and Klebsiella pneumoniae are recognized nosocomial pathogens. For example, K. pneumoniae and S. aureus are leading causes of nosocomial pneumonia, while E. coli is the commonest cause of nosocomial urinary tract infection [11,14,21].

5. Cockroaches and Antibiotic Resistance

In many instances, cockroaches have been reported to carry highly antibiotic-resistant bacteria, therefore, it is important to highlight these studies. A study in Ethiopia showed that 64.1% of bacteria isolated from cockroaches were multidrug-resistant (resistance to three or more classes of antibiotics); Salmonella spp. were the most prevalent multidrug-resistant isolates (100%) followed by Enterobacter (90.5%) and Shigella spp. (76.9%) [57]. Interestingly, in that study the bacteria isolated from cockroaches in the hospital environment had a higher prevalence of multidrug resistance (67%) compared to those from the community (61.3%) [57]. The risk of cockroaches as reservoirs of antibiotic-resistant bacteria in the hospital environment has been elucidated by another study carried out at the neonatal intensive care unit of a hospital in Ethiopia [62]. In that study, the key nosocomial pathogens implicated in neonatal sepsis at the study hospital, including K. pneumoniae and Klebsiella oxytoca, were isolated from the cockroaches, and these organisms were predominantly multidrug-resistant [72]. A study in a hospital in Iraq showed that about 42.8% of cockroach bacterial isolates were found to express the extended-spectrum beta-lactamases (ESβLs) trait, while 19% expressed the metallo-β-lactamases (MβLs) trait [75]; both ESβLs and MβLs are enzymes that confer resistance to a broad range of β-lactam drugs. Studies in Ghana and Algeria showed that household and hospital cockroaches could serve as reservoirs of the CTX-M-15, OXA-48, and NDM-1 genes that share beta-lactam resistance determinants with humans [76,77]. The cockroach brain has antimicrobial properties, and this is thought to be an important factor that accounts for the carriage of antibiotic-resistant organisms among cockroaches [78]. In hospitals, cockroaches that carry antibiotic-resistant bacteria could easily disseminate these organisms on hospital equipment and, therefore, facilitate their transmission to patients. This implies that cockroaches could play a significant role in outbreaks of nosocomial pathogens in hospitals, though little attention has been given to this. In an outbreak of K. pneumoniae in a neonatal unit infested with cockroaches in South Africa, the organisms isolated from cockroaches and those colonizing infants or causing clinical disease were indistinguishable by pulsed-field gel electrophoresis [79]. This suggests the possibility of some transmission events between cockroaches and humans, though the investigators needed whole-genome sequencing analysis to confirm this. Antibiotic resistance is considered one of the greatest threats to public health in recent times, and, therefore, cockroach infestation should be of a serious concern, given the possible role of cockroaches as reservoirs of antibiotic-resistant bacteria.

6. Conclusions and Further Research

Cockroaches could harbor and disseminate many microbial pathogens including bacteria, fungi, viruses, and parasites. Since many of these microorganisms are implicated in healthcare-associated infections, the presence of cockroaches in the hospital environment constitutes an important reservoir of vectors of nosocomial pathogens. In addition, cockroaches tend to serve as reservoirs of antibiotic-resistant organisms, which complicates healthcare-associated infections.
Despite cockroaches being reservoirs and vectors of nosocomial pathogens, their involvement in the actual transmission of these pathogens to patients in hospitals has not been proven. The era of whole-genome sequencing provides us with the opportunity to address this research gap. In hospitals, whole-genome sequencing of nosocomial pathogens isolated from cockroaches, patients, healthcare workers, hospital equipment, and other fomites could provide insights into the transmission of nosocomial pathogens involving cockroaches. There is also the need for further studies to describe cockroach carriage of epidemiologically significant antibiotic-resistant organisms, such as MRSA and VRE, which have not been previously reported. In addition, studies are required to elucidate the possible mechanisms of host–pathogen relationships that may exist between cockroaches and microbial pathogens.
Considering the microbial risk to human health associated with cockroaches, there should be zero tolerance for their presence in healthcare facilities. Control of cockroaches in healthcare facilities could involve proper sanitation of equipment and facilities to remove dirt and food debris, as well as the application of insecticides to hiding places of cockroaches [80,81,82]. There is also the need to discard cardboard and to keep food in tightly fitted containers. It is believed that the effective control of cockroaches will substantially minimize the spread of infectious diseases in our environment [83].

Funding

This research received no external funding.

Acknowledgments

I thank authors of the various papers that were used in developing this review article.

Conflicts of Interest

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be constructed as a potential conflict of interest.

References

  1. Cornwell, P.B. The Cockroach; Hutchinson: London, UK, 1968; Volume 1. [Google Scholar]
  2. Roth, L.M.; Willis, E.R. The Biotic Associations of Cockroaches; The Smithsonian Institution: Washington, DC, USA, 1960; Volume 141, p. 470. [Google Scholar]
  3. Gliniewicz, A.; Sawicka, B.; Czajka, E. Occurrence of insect pests in hospitals in Poland. Przegl. Epidemiol. 2003, 57, 329–334. [Google Scholar] [PubMed]
  4. Uçkay, I.; Sax, H.; Longet-Di Pietro, S.; Baur, H.; Boulc’h, M.F.; Akakpo, C.; Chevrolet, J.C.; Pittet, D. Cockroaches (Ectobius vittiventris) in an intensive care unit, Switzerland. Emerg. Infect. Dis. 2009, 15, 496–497. [Google Scholar] [CrossRef] [PubMed]
  5. Burke, J.P. Infection control: A problem for patient safety. N. Engl. J. Med. 2003, 348, 651–656. [Google Scholar] [CrossRef] [PubMed]
  6. Bates, D.W.; Larizgoitia, I.; Prasopa-Plaizier, N.; Jha, A.K. Global priorities for patient safety research. BMJ 2009, 338, b1775. [Google Scholar] [CrossRef] [PubMed]
  7. Pittet, D.; Donaldson, L. Clean Care is Safer Care: A worldwide priority. Lancet 2005, 336, 1246–1247. [Google Scholar] [CrossRef]
  8. Report on the Endemic Burden of Healthcare-Associated Infection Worldwide; World Health Organization: Geneva, Switzerland, 2011; Available online: http://apps.who.int/iris/bitstream/10665/80135/1/9789241501507_eng.pdf (accessed on 18 October 2016).
  9. Nejad, S.B.; Syed, S.B.; Ellis, B.; Pittet, D. Health-care-associated infection in Africa: A systematic review. Bull. World Health Organ. 2011, 89, 757–765. [Google Scholar] [CrossRef]
  10. Allegranzi, B.; Bagheri Nejad, S.; Combescure, C.; Graafmans, W.; Attar, H.; Donaldson, L.; Pittet, D. Burden of endemic health-care-associated infection in developing countries: Systematic review and meta-analysis. Lancet 2011, 377, 228–241. [Google Scholar] [CrossRef]
  11. Trilla, A. Epidemiology of nosocomial infections in adult intensive care units. Intensive Care Med. 1994, 20 (Suppl. 3), S1–S4. [Google Scholar] [CrossRef] [PubMed]
  12. Eggimann, P.; Pittet, D. Infection control in the ICU. Chest 2001, 120, 2059–2093. [Google Scholar] [CrossRef]
  13. Zhanel, G.G.; DeCorby, M.; Laing, N.; Weshnoweski, B.; Vashisht, R.; Tailor, F.; Nichol, K.A.; Wierzbowski, A.; Baudry, P.J.; Karlowsky, J.A.; et al. Antimicrobial-resistant pathogens in intensive care units in Canada: Results of the Canadian National Intensive Care Unit (CAN-ICU) study, 2005–2006. Antimicrob. Agents Chemother. 2008, 52, 1430–1437. [Google Scholar] [CrossRef]
  14. Becker, K.; Heilmann, C.; Peters, G. Coagulase-Negative Staphylococci. Clin. Microbiol. Rev. 2014, 27, 870–926. [Google Scholar] [CrossRef] [PubMed][Green Version]
  15. Weber, D.J.; Rutala, W.A. The emerging nosocomial pathogens Cryptosporidium, Escherichia coli O157:H7, Helicobacter pylori, and hepatitis C: Epidemiology, environmental survival, efficacy of disinfection, and control measures. Infect. Control Hosp. Epidemiol. 2001, 22, 306–315. [Google Scholar] [CrossRef] [PubMed]
  16. Mbithi, J.N.; Springthorpe, V.S.; Sattar, S.A. Effect of relative humidity and air temperature on survival of hepatitis A virus on environmental surfaces. Applied Environ. Microbiol. 1991, 57, 1394–1399. [Google Scholar]
  17. Kramer, A.; Schwebke, I.; Kampf, G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 2006, 6, 130. [Google Scholar] [CrossRef] [PubMed][Green Version]
  18. Ayukekbong, J.A.; Ntemgwa, M.; Atabe, A.N. The threat of antimicrobial resistance in developing countries: Causes and control strategies. Antimicrob. Resist. Infect. Control. 2017, 6, 47. [Google Scholar] [CrossRef] [PubMed]
  19. Codjoe, F.S.; Donkor, E.S. Carbapenem Resistance: A Review. Med. Sci. 2017, 6, 1. [Google Scholar] [CrossRef]
  20. Labi, A.K.; Obeng-Nkrumah, N.; Addison, N.; Donkor, E.S. Salmonella blood stream infections in a tertiary care setting in Ghana. BMC Infect. Dis. 2015, 15, 263. [Google Scholar] [CrossRef]
  21. Emily, R.M.; Sydnor, T.M.P. Hospital epidemiology and infection control in acute-care settings. Clin. Microbiol. Rev. 2011, 24, 141–173. [Google Scholar]
  22. Klevens, R.M.; Morrison, M.A.; Nadle, J.; Petit, S.; Gershman, K.; Ray, S.; Harrison, L.H.; Lynfield, R.; Dumyati, G.; Townes, J.M.; et al. Active Bacterial Core surveillance (ABCs) MRSA Investigators. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 2007, 298, 1763–1771. [Google Scholar] [CrossRef] [PubMed]
  23. Elixhauser, A.; Steiner, C. Infections with Methicillin-Resistant Staphylococcus aureus (MRSA) in U.S. Hospitals, 1993–2005: Statistical Brief #35; Agency for Health Care Policy and Research: Rockville, MD, USA, 2007.
  24. De Kraker, M.E.; Wolkewitz, M.; Davey, P.G.; Koller, W.; Berger, J.; Nagler, J.; Icket, C.; Kalenic, S.; Horvatic, J.; Seifert, H.; et al. Clinical impact of antimicrobial resistance in European hospitals: Excess mortality and length of hospital stay related to methicillin-resistant Staphylococcus aureus bloodstream infections. Antimicrob. Agents Chemother. 2011, 55, 1598–1605. [Google Scholar] [CrossRef]
  25. Durai, R.; Ng, P.C.; Hoque, H. Methicillin-resistant Staphylococcus aureus: An update. AORN J. 2010, 91, 599–606. [Google Scholar] [CrossRef] [PubMed]
  26. Boyce, J.M. Are the epidemiology and microbiology of methicillin-resistant Staphylococcus aureus changing? JAMA 1998, 279, 623–624. [Google Scholar] [CrossRef] [PubMed]
  27. Lindenmayer, J.M.; Schoenfeld, S.; O’Grady, R.; Carney, J.K. Methicillin-resistant Staphylococcus aureus in a high school wrestling team and the surrounding community. Arch. Intern. Med. 1998, 158, 895–899. [Google Scholar] [CrossRef] [PubMed]
  28. Akram, J.; Glatt, A. True community-acquired methicillin-resistant Staphylococcus aureus bacteremia. Infect. Control Hosp. Epidemiol. 1998, 19, 106–107. [Google Scholar] [CrossRef] [PubMed]
  29. Popovich, K.J.; Weinstein, R.A.; Hota, B. Are community associated methicillin resistant Staphylococcus aureus (MRSA) strains replacing traditional nosocomial MRSA strains? Clin. Infect. Dis. 2008, 46, 787–794. [Google Scholar] [CrossRef] [PubMed]
  30. Bassetti, M.; Nicco, E.; Mikulska, M. Why is community-associated MRSA spreading across the world and how will it change clinical practice? Int. J. Antimicrob. Agents 2009, 34, 15–19. [Google Scholar] [CrossRef]
  31. Feil, E.J.; Nickerson, E.K.; Chantratita, N.; Wuthiekanun, V.; Srisomang, P.; Cousins, R.; Pan, W.; Zhang, G.; Xu, B.; Day, N.P.J. Rapid detection of the pandemic methicillin-resistant Staphylococcus aureus clone ST 239, a dominant strain in Asian hospitals. J. Clin. Microbiol. 2008, 46, 1520–1522. [Google Scholar] [CrossRef] [PubMed]
  32. Abdulgader, S.M.; Shittu, A.O.; Nicol, M.P.; Kaba, M. Molecular epidemiology of Methicillin-resistant Staphylococcus aureus in Africa: A systematic review. Front. Microbiol. 2015, 6, 348. [Google Scholar] [CrossRef] [PubMed]
  33. Roberts, R.B.; Chung, M.; de Lencastre, H.; Hargrave, J.; Tomasz, A.; Nicolau, D.P.; John, J.F., Jr.; Korzeniowski, O.; Tri-State MRSA Collaborative Study Group. Distribution of methicillin-resistant Staphylococcus aureus clones among health care facilities in Connecticut, New Jersey, and Pennsylvania. Microb. Drug Resist. 2000, 6, 245–251. [Google Scholar] [CrossRef] [PubMed]
  34. Pardos de la Gandara, M.; Curry, M.; Berger, J.; Burstein, D.; Della-Latta, P.; Kopetz, V.; Quale, J.; Spitzer, E.; Tan, R.; Urban, C.; et al. MRSA Causing Infections in Hospitals in Greater Metropolitan New York: Major Shift in the Dominant Clonal Type between 1996 and 2014. PLoS ONE 2016, 11, e0156924. [Google Scholar] [CrossRef] [PubMed]
  35. Denis, O.; Deplano, A.; Nonhoff, C.; De Ryck, R.; de Mendonça, R.; Rottiers, S.; Vanhoof, R.; Struelens, M.J. National surveillance of methicillin-resistant Staphylococcus aureus in Belgian hospitals indicates rapid diversification of epidemic clones. Antimicrob. Agents Chemother. 2004, 48, 3625–3629. [Google Scholar] [CrossRef] [PubMed]
  36. Strommenger, B.; Cuny, C.; Werner, G.; Witte, W. Obvious lack of association between dynamics of epidemic methicillin-resistant Staphylococcus aureus in Central Europe and agr specificity groups. Eur. J. Clin. Microbiol. Infect. Dis. 2004, 23, 15–19. [Google Scholar] [PubMed]
  37. Melter, O.; Urbaskova, P.; Jakubu, V.; Macková, B.; Zemlicková, H.; Czech participants in EARSS. Emergence of EMRSA-15 clone in hospitals throughout the Czech Republic. Euro Surveill. 2006, 11, E060803–E060806. [Google Scholar] [CrossRef] [PubMed]
  38. Conceiçao, T.; Aires-de-Sousa, M.; Fuzi, M.; Toth, A.; Paszti, J.; Ungvári, E.; van Leeuwen, W.B.; van Belkum, A.; Grundmann, H.; de Lencastre, H. Replacement of methicillin-resistant Staphylococcus aureus clones in Hungary over time: A 10-year surveillance study. Clin. Microbiol. Infect. 2007, 13, 971–979. [Google Scholar] [CrossRef] [PubMed]
  39. Perez-Roth, E.; Lorenza-Diaz, F.; Batista, N.; Moreno, A.; Mendez-Alvarez, S. Tracking methicillin-resistant Staphylococcus aureus clones during a 5-year period (1998 to 2002) in a Spanish hospital. J. Clin. Microbiol. 2004, 42, 4649–4656. [Google Scholar] [CrossRef] [PubMed]
  40. Aires-de-Sousa, M.; Correia, B.; de Lencastre, H. The Multilaboratory Project Collaborators (2008) Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: Surveillance over a 16-year period. J. Clin. Microbiol. 2008, 46, 2912–2917. [Google Scholar] [CrossRef] [PubMed]
  41. Laurent, F.; Lelièvre, H.; Cornu, M.; Vandenesch, F.; Carret, G.; Etienne, J.; Flandrois, J.P. Fitness and competitive growth advantage of new gentamicin-susceptible MRSA clones spreading in French hospitals. J. Antimicrob. Chemother. 2001, 47, 277–283. [Google Scholar] [CrossRef] [PubMed][Green Version]
  42. Knight, G.M.; Budd, E.L.; Whitney, L.; Thornley, A.; Al-Ghusein, H.; Planche, T.; Lindsay, J.A. Shift in dominant hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) clones over time. J. Antimicrob. Chemother. 2012, 67, 2514–2522. [Google Scholar] [CrossRef] [PubMed][Green Version]
  43. Hsu, L.Y.; Harris, S.R.; Chlebowicz, M.A.; Lindsay, J.A.; Koh, T.H.; Krishnan, P.; Tan, T.Y.; Hon, P.Y.; Grubb, W.B.; Bentley, S.D.; et al. Evolutionary dynamics of methicillin-resistant Staphylococcus aureus within a healthcare system. Genome Biol. 2015, 16, 81. [Google Scholar] [CrossRef] [PubMed]
  44. DeLeo, F.R.; Chambers, H.F. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Investig. 2009, 119, 2464–2474. [Google Scholar] [CrossRef] [PubMed][Green Version]
  45. Centers for Disease Control and Prevention. Public health focus: Surveillance, prevention and control of nosocomial infections. Morb. Mortal. Wkly. Rep. (MMWR) 1992, 41, 783–787. [Google Scholar]
  46. National Audit Office. Reducing Healthcare Associated Infections in Hospitals in England. HC 560 Session 2008–2009. London: The Stationery Office. 2009. Available online: http://www.nao.org.uk/publications/0809/reducing_healthcare_associated.aspx (accessed on 30 September 2018).
  47. Esatoglu, A.E.; Agirbas, I.; Onder, O.R.; Celik, Y. Additional cost of hospital-acquired infection to the patient: A case study in Turkey. Health Serv. Manag. Res. 2006, 19, 137–143. [Google Scholar] [CrossRef] [PubMed]
  48. Kasatpibal, N.; Thongpiyapoom, S.; Narong, M.; Suwalak, N.; Jamulitrat, S. Extra charge and extra length of postoperative stay attributable to surgical site infection in six selected operations. J. Med. Assoc. Thail. 2005, 88, 1083–1091. [Google Scholar]
  49. Tarshis, I.B. The cockroach—A new suspect in the spread of infectious hepatitis. Am. J. Trop. Med. Hyg. 1962, 11, 705–711. [Google Scholar] [CrossRef] [PubMed]
  50. Kopanic, R.J., Jr.; Sheldon, B.W.; Wright, C.G. Cockroaches as vectors of salmonella: Laboratory and field trials. J. Food Protect. 1994, 57, 125–132. [Google Scholar] [CrossRef]
  51. Imamura, S.; Kita, M.; Yamaoka, Y.; Yamamoto, T.; Ishimaru, A.; Konishi, H.; Wakabayashi, N.; Mitsufuji, S.; Okanoue, T.; Imanishi, J. Vector potential of cockroaches for Helicobacter pylori infection. Am. J. Gastroenterol. 2003, 98, 1500–1503. [Google Scholar] [CrossRef] [PubMed]
  52. Fotedar, R.; Nayar, E.; Samantray, J.C.; Shriniwas Banerjee, U.; Dogra, V.; Kumar, A. Cockroaches as vectors of pathogenic bacteria. J. Commun. Dis. 1989, 21, 318–322. [Google Scholar] [PubMed]
  53. Tachbele, E.; Erku, W.; Gebre-Michael, T.; Ashenafi, M. Cockroach-associated food-borne bacterial pathogens from some hospitals and restaurants in Addis Ababa, Ethiopia: Distribution and antibiograms. J. Rural Trop. Public Health 2006, 5, 34–41. [Google Scholar]
  54. Oothuman, P.; Jeffery, J.; Aziz, A.H.; Abu Bakar, E.; Jegathesan, M. Bacterial pathogens isolated from cockroaches trapped from paediatric wards in peninsular Malaysia. Trans. R. Soc. Trop. Med. Hyg. 1989, 83, 133–135. [Google Scholar] [CrossRef]
  55. Le Guyader, A.; Rivault, C.; Chaperon, J. Microbial organisms carried by brown banded cockroaches in relation to their spatial distribution in a hospital. Epidemiol. Infect. 1989, 102, 485–492. [Google Scholar] [CrossRef] [PubMed]
  56. Fotedar, R.; Shriniwas, U.B.; Verma, A. Cockroaches (Blattella germanica) as carriers of microorganisms of medical importance in hospitals. Epidemiol. Infect. 1991, 107, 181–187. [Google Scholar] [CrossRef] [PubMed]
  57. Moges, F.; Eshetie, S.; Endris, M.; Huruy, K.; Muluye, D.; Feleke, T.; G/Silassie, F.; Ayalew, G.; Nagappan, R. Cockroaches as a Source of High Bacterial Pathogens with Multidrug Resistant Strains in Gondar Town, Ethiopia. Biomed. Res. Int. 2016, 2016, 2825056. [Google Scholar] [CrossRef] [PubMed]
  58. Salehzadeh, A.; Tavacol, P.; Mahjub, H. Bacterial, fungal and parasitic contamination of cockroaches in public hospitals of Hamadan, Iran. J. Vector Borne Dis. 2007, 44, 105–110. [Google Scholar] [PubMed]
  59. Naher, A.; Afroz, S.; Hamid, S. Cockroach associated foodborne pathogens: Distribution and antibiogram. Bangladesh Med. Res. Counc. Bull. 2018, 44, 30–38. [Google Scholar] [CrossRef]
  60. Menasria, T.; Moussa, F.; El-Hamza, S.; Tine, S.; Megri, R.; Chenchouni, H. Bacterial load of German cockroach (Blattella germanica) found in hospital environment. Pathog. Glob. Health 2014, 108, 141–147. [Google Scholar] [CrossRef] [PubMed]
  61. Tetteh-Quarcoo, P.B.; Donkor, E.S.; Attah, S.K.; Duedu, K.O.; Afutu, E.; Boamah, I.; Olu-Taiwo, M.; Anim-Baidoo, I.; Ayeh-Kumi, P.F. Microbial carriage of cockroaches at a tertiary care hospital in Ghana. Environ. Health Insights 2013, 7, 59–66. [Google Scholar] [CrossRef] [PubMed]
  62. Tilahun, B.; Worku, B.; Tachbele, E.; Terefe, S.; Kloos, H.; Legesse, W. High load of multi-drug resistant nosocomial neonatal pathogens carried by cockroaches in a neonatal intensive care unit at Tikur Anbessa specialized hospital, Addis Ababa, Ethiopia. Antimicrob. Resist. Infect. Control 2012, 1, 12. [Google Scholar] [CrossRef] [PubMed][Green Version]
  63. Becker-Dreps, S.; Bucardo, F.; Vilchez, S.; Zambrana, L.E.; Liu, L.; Weber, D.J.; Peña, R.; Barclay, L.; Vinjé, J.; Hudgens, M.G.; et al. Etiology of childhood diarrhea following rotavirus vaccine introduction: A prospective, population-based study in Nicaragua. Pediatr. Infect. Dis. J. 2014, 33, 1156–1163. [Google Scholar] [CrossRef] [PubMed]
  64. Revelas, A. Acute gastroenteritis among children in the developing world. S. Afr. J. Epidemiol. Infect. 2012, 27, 156–162. [Google Scholar] [CrossRef][Green Version]
  65. Elliott, E.J. Acute gastroenteritis in children. BMJ Open 2007, 334, 35–40. [Google Scholar] [CrossRef] [PubMed][Green Version]
  66. World Health Organization Rotavirus Vaccines. WHO position paper—January 2013. Wkly. Epidemiol. Rec. 2013, 88, 49–64. [Google Scholar]
  67. Damanka, S.; Adiku, T.K.; Armah, G.E.; Rodrigues, O.; Donkor, E.S.; Nortey, D.; Asmah, R. Rotavirus Infection in Children with Diarrhea at Korle-Bu Teaching Hospital, Ghana. Jpn. J. Infect. Dis. 2016, 69, 331–334. [Google Scholar] [CrossRef] [PubMed]
  68. Fischer, T.K.; Bresee, J.S.; Glass, R.I. Rotavirus vaccines and the prevention of hospital-acquired diarrhea in children. Vaccine 2004, 22, S49–S54. [Google Scholar] [CrossRef] [PubMed]
  69. Clark, H.F.; Offit, P.A.; Glass, R.I.; Ward, R.L. Rotavirus vaccines. In Vaccines, 4th ed.; Plotkin, S., Orenstein, W., Offit, P., Eds.; Elsevier: Philadelphia, PA, USA, 2013; pp. 1327–1345. [Google Scholar]
  70. Aygun, G.; Yilmaz, M.; Yasar, H.; Aslan, M.; Polat, E.; Midilli, K.; Ozturk, R.; Altas, K. Parasites in nosocomial diarrhea: Are they underestimated? J. Hosp. Infect. 2005, 60, 283–285. [Google Scholar] [CrossRef] [PubMed]
  71. Sandokji, A.M.; Murshid, K.R.; El-Badry, A.A.; Ali-Ali, K.H.; Halaby, S.A. Infectious nosocomial diarrhea in the surgical wards: Role of parasites and microbes imply stool analysis. J. Taibah Univ. Med. Sci. 2009, 4, 73–81. [Google Scholar]
  72. Góralska, K.; Kurnatowski, P. Parasites as etiological factors of nosocomial infections. Ann. Parasitol. 2013, 59, 3–11. [Google Scholar] [PubMed]
  73. Perlroth, J.; Choi, B.; Spellberg, B. Nosocomial fungal infections: Epidemiology, diagnosis, and treatment. Med. Mycol. 2007, 45, 321–346. [Google Scholar] [CrossRef] [PubMed]
  74. Delaloye, J.; Calandra, T. Invasive candidiasis as a cause of sepsis in the critically ill patient. Virulence 2014, 5, 161–169. [Google Scholar] [CrossRef] [PubMed]
  75. ALMarjani, M.F.; Abdulra, R.A.; Zahraa, A.K.; Reyam, I.D.; Khiaria, J.T. Cockroaches (Periplaneta americana): Reservoirs of metallo Β lactamase and extended spectrum Β-lactamaseproducing bacteria in medical city hospital in Baghdad, Iraq. Pak. J. Biotechnol. 2017, 14, 317–321. [Google Scholar]
  76. Obeng-Nkrumah, N.; Labi, A.; Blankson, H.; Awuah-Mensah, G.; Oduro-Mensah, D.; Anum, J.; Teye, J.; Kwashie, S.; Bako, E.; Ayeh-Kumi, P.F.; et al. Household cockroaches carry CTX-M-15, OXA-48 and NDM-1, and share beta-lactam resistance determinants with humans. bioRxiv 2018. [Google Scholar] [CrossRef]
  77. Loucif, L.; Gacemi-Kirane, D.; Cherak, Z.; Chamlal, N.; Grainat, N.; Rolain, J.M. First Report of German Cockroaches (Blattella germanica) as Reservoirs of CTX-M-15 Extended-Spectrum-β-Lactamase- and OXA-48 Carbapenemase-Producing Enterobacteriaceae in Batna University Hospital, Algeria. Antimicrob. Agents Chemother. 2016, 60, 6377–6380. [Google Scholar] [CrossRef] [PubMed][Green Version]
  78. Lee, S.; Atkins, H.; Duce, I.; Khan, N.A. Cockroach and locust: physicians’ answer to infectious diseases. Int. J. Antimicrob. Agents 2011, 37, 279–280. [Google Scholar] [CrossRef] [PubMed]
  79. Cotton, M.F.; Wasserman, E.; Pieper, C.H.; Theron, D.C.; van Tubbergh, D.; Campbell, G.; Fang, F.C.; Barnes, AJ. Invasive disease due to extended spectrum beta-lactamase-producing Klebsiella pneumoniae in a neonatal unit: The possible role of cockroaches. J. Hosp. Infect. 2000, 44, 13–17. [Google Scholar] [CrossRef] [PubMed]
  80. Potter, M.F. The perfect storm: An extension view on bed bugs. Am. Entomol. 2006, 52, 102–104. [Google Scholar] [CrossRef]
  81. Goddard, J. Public Health Entomology; CRC Press: Boca Raton, FL, USA, 2012. [Google Scholar]
  82. Fakoorziba, M.R.; Eghbal FHassanzadeh, J.; Moemenbellah-Fard, M.D. Cockroaches (Periplaneta americana and Blattella germanica) as potential vectors of the pathogenic bacteria found in nosocomial infections. Ann. Trop. Med. Parasitol. 2010, 104, 521–528. [Google Scholar] [CrossRef] [PubMed]
  83. El-Sherbini, G.T.; El-Sherbini, E.T. The role of cockroaches and flies in mechanical transmission of medical important parasites. J. Entomol. Nematol. 2011, 3, 98–104. [Google Scholar]
Table 1. Microbial Carriage of Cockroaches in Healthcare Institutions.
Table 1. Microbial Carriage of Cockroaches in Healthcare Institutions.
StudyCountryNOrganisms Isolated
Fotedar et al. [52]India96Pseudomonas aeruginosa, Staphylococcus aureus, Streptococcus faecalis, Micrococcus spp.
Tachbele et al. [53]Ethiopia600Salmonella spp., Shigella flexneri, Escherichia coli O157, Staphylococcus aureus and Bacillus cereus.
Oothuman et al. [54]Malaysia104Shigella boydii, Shigella dysenteriae, Salmonella Typhimurium, Klebseilla oxytoca, Klebsiella ozaena, Serratia marcescens.
Guyader et al. [55]France532Citrobacter freundii, Enterobacter cloacae, Klebsiella oxytoca, Klebsiella pneumoniae, Enterobacter agglomerans, Escherichia adecarboxylata, Serratia marcescens, Serratia liquefaciens, Acinetobacter spp., Pseudomonas fluorescens, Pseudomonas putida, Pseudomonas aeruginosa, Escherichia coli, Staphylococcus aureus.
Fotedar et al. [56]India279Bacteria: Klebsiella spp., Escherichia coli, Enterobacter spp., Pseudomonas aeruginosa, Proteus spp., Staphylococcus aureus, Streptococcus epidermidis, Streptococcus faecalis, Streptococcus viridans, Micrococcus, Bacillus spp.
Parasites: Endolimax nana, Entamoeba coli, Entamoeba histolytica.
Fungi: Candida spp., Rhizopus spp. Mucor spp., Alternaria spp. Aspergillus niger, Aspergillus flavus, Aspergillus spp.
Moges et al. [57]Ethiopia60Klebsiella pneumoniae, Escherichia coli, Citrobacter spp., Salmonella spp., Enterobacter spp. Shigella spp., Providencia spp., Serratia spp., Proteus spp., Staphylococcus aureus, Escherichia coli.
Salehzadeh et al. [58]Iran133Bacteria: Enterobacter spp., Klebsiella spp., Enterococcus spp., Staphylococcus spp., Escherichia coli, Streptococcus spp., Pseudomonas spp. Shigella spp, Haemophilus and group A beta-hemolytic Streptococcus spp.
Fungi: Candida spp., Mucor spp., Rhizopus spp., Penicillium spp., Aspergillus fumigans. Aspergillus niger.
Naher et al. [59]Bangladesh Escherichia coli, Pseudomonas aeruginosa, Salmonella spp., Shigella spp., Klebsiella spp., Proteus spp., Staphylococcus aureus.
Mensaria et al. [60]Algeria Citrobacter freundii, Enterobacter cloacae, Serratia marcescens, Klebsiella pneumoniae, Pantoea spp., Enterobacter aerogenes, Enterobacter spp.
Tetteh-Quarcoo et al. [61]Ghana61Bacteria: Klebsiella pneumoniae, Escherichia coli, Proteus vulgaris, Citrobacter ferundii, Enterobacter cloacae, Enterococcus faecalis, Pseudomonas aeruginosa, Klebsiella oxytoca.
Parasites: Ancylostoma duodenale, Hymenolepis nana, Taenia spp.
Viruses: Rotavirus.
Tilahun et al. [62]Ethiopia400Klebsiella oxytoca, Klebsiella pneumoniae, Klebsiella ozaenae, Citrobacter spp., Citrobacter diversus, Enterobacter cloacae, Pseudomonas aeruginosa, Enterobacter aeruginosa, Providencia rettgeri, Salmonella spp., Streptococcus spp. Staphylococcus aureus, Escherichia coli, Acinetobacter spp. and Shigella flexneri
N, number of cockroach samples.

© 2019 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Back to TopTop