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20 May 2020 Cockroaches and Food-borne Pathogens
Eric S Donkor
Author Affiliations +
Abstract

Food-borne disease is a widespread and escalating public health problem globally. About a quarter of the microorganisms isolated from cockroaches are food-borne pathogens including Escherichia coli O157:H7, Staphylococcus aureus, Bacillus cereus, Shigella dysenteriae, Salmonella enterica subsp. enterica serovar Typhi, Rotavirus, Aspergillus fumigatus, and Cryptosporidium parvum. Thus, cockroaches could be an important reservoir and mechanical vector of food-borne pathogens. Generally, the role of cockroaches in human infections is poorly understood and has been an issue of debate for several years. This article aims to elucidate the possible role of cockroaches in food-borne infections by reviewing the relevant research publications.

Introduction

Food is an important vehicle for the transmission of infectious pathogens to humans. The high incidence of food-borne diseases coupled with the emergence and re-emergence of food-borne pathogens, have placed food safety high on the agenda of public health issues. Cockroaches appear to be suitable mechanical transmitters for a wide range of food-borne pathogenic microorganisms due to their filthy behaviour and occurrence in places where food is stored or handled.1,2 Microorganisms may be carried externally on the cuticle of cockroaches,3,4 or may be ingested and then later excreted or regurgitated.3,4 In this way, cockroaches can easily contaminate food when they come into contact with it. Although there exist about 4000 species of cockroaches, only 30 are associated with human habitations.2 The most common cockroach species found in human habitations or environments are Periplaneta Americana, Blattella germanica, Blatta orientalis, Periplaneta australasiae, and Supella longipalpa.3 Generally, the role of cockroaches in human infections is poorly understood and has been an issue of debate for several years. In the last 2 decades, there has been an accumulation of adequate research data that contributes significantly to our understanding of this subject.4 In this regard, the scientific community could benefit from a review of available research data that can provide a global understanding of the role of cockroaches in transmission of human infections. Therefore, in this review article, the author aims to elucidate the possible role of cockroaches in the transmission of food-borne pathogens by reviewing the relevant research publications.

Brief Overview of Food-borne Infections

The World Health Organization5 estimates that food-borne diseases cause about 600 million illness episodes, 420 000 deaths and 33 million healthy life years lost (disability-adjusted life years, DALYs) annually. Food-borne disease is most prevalent in Africa and South-East Asia, where more than a third of all food-borne illness occurs.5 Food-borne pathogens account for the vast majority of food-borne diseases, and diarrhoeal agents are responsible for more than half of the global burden of food-borne infections.5,6 Although all human beings are at risk, the impact of food-borne infections is most severe in very young and elderly people, as well as immune-compromised individuals. Food-borne illness is associated with huge economic costs. For example, in the United States, food-borne illnesses cost the economy between US$10 and US$83 billion.7 In Australia, the cost of food-borne illness has been estimated at US$1.289 billion per year,8 whereas in New Zealand, it costs US$86 million.9 The cost of food-borne illness in Sweden was estimated to be as high as US$171 million.10 Generally, data on the financial costs of food-borne illness in the developing world are lacking, though the majority of food-borne cases occur in these countries.

The pathogens implicated in food-borne infections cover a wide spectrum of microbes including bacteria, parasites, viruses, and fungi.11-15 Some of the common food-borne pathogens and types of food they affect are shown in Table 1. The incidence/prevalence of food-borne diseases caused by different pathogens has changed in the last few decades. For example, in the United Kingdom, in 2010, Campylobacter displaced Salmonella as the prime cause of food-borne disease while the incidence of Listeria monocytogenes rose between 2001 and 2009.16 Viruses are implicated in an increasing number of food-borne cases in the United Kingdom currently, while toxin-producing Escherichia coli such as E coli 0157:H7 remain less common, but serious pathogens due to their clinical impact.16 In the next decades of years, new food-borne pathogens are likely to emerge globally driven by factors such as microbial evolution and changes in food production processes.17-19 In addition, food-borne infections due to existing pathogens can be expected to increase, especially in developing countries, partly because of environmental and demographic changes, as well as massive consumption of risky foods.19,20

Table 1.

Potentially contaminated foods and the microbial pathogens implicated.

10.1177_1178630220913365-table1.tif

The many food-borne pathogens can be classified into 3 main groups depending on their reservoirs. The first group are pathogens that are sustained in human reservoirs and contaminate food through the faeces of infected humans. This group contains pathogens such as Norovirus.21,22 The second group are pathogens such as Campylobacter spp. and Salmonella enteritidis, which are sustained in animal reservoirs and contaminate animal source food of humans such as meat, milk, and eggs.22,23 They could also occur in the faeces of infected animals and contaminate human food. The third group are pathogens that persist in the environment and can contaminate food usually through poor environmental hygiene. This group includes a wide range of pathogens such as Clostridium perfringens and Bacillus cereus.24-27

The diseases caused by food-borne pathogens can be classified into 2 forms: food-borne infection and food-borne intoxication.27 In food-borne infection (eg, L. monocytogenes food poisoning), live cells of the food-borne pathogen are ingested, while in food-borne intoxication (eg, Clostridium botulinum food poisoning), toxins are ingested. Some food-borne diseases involve both ingestion of live cells and toxins (eg, C. perfringens food poisoning). For successful gastrointestinal infection, pathogens must gain access to the host in adequate numbers to initiate infection. Infective dose, which is the number of cells required to successfully infect a host, varies significantly among food-borne pathogens. For instance, the infective dose of Yersinia enterocolitica is about 106 cells while that of Shigella flexneri is 101 to 102 cells.26 Once inside the host, the pathogens establish colonization, and this is facilitated by adhesion factors, invasion factors, chemotaxis, and sometime immune evasion. Most food-borne microorganisms such as Staphylococcus aureus cause localized infection but some such as L. monocytogenes spread to deeper tissues to induce systemic infection.

Cockroaches and Food-borne Pathogens

In the 1950s, Tarshis28 provided a compelling evidence incriminating cockroaches as possible vectors of human infections, through a study that reported a correlation between the incidence of hepatitis A and the lack of cockroach control. From 1956 to 1959, the Carmelitos Housing Project had 20% to 39% of the hepatitis A cases in Los Angeles. However, through a concentrated pest control programme, there was a sharp decline in the incidence of endemic infectious hepatitis: in 1960, the hepatitis A incidence at the housing project reduced to 6.6%, then further to 3.6% in 1961, and to 0.0% in 1962. Meanwhile, around the same period, every other place in Los Angeles County that was not receiving the pest control service experienced increasing incidence of the infection. It was observed that the decline in hepatitis A incidence occurred simultaneously with a significant reduction (about 70%) in cockroach infestation due to the pest control programme. The hepatitis A virus occurs in the faeces of infected persons and is usually 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. Although the study of Tarshis28 was not supported with experimental data, it provides evidence supporting the theory that cockroaches play a role in the transmission of food-borne pathogens. Experimental evidence supporting the possible role of cockroaches in the transmission of food-borne pathogens has been provided by several investigators. A study done by Ash and Greenberg29 in 1980 reported that exposure of cockroaches to Salmonella enterica subsp. enterica serovar Typhimurium resulted in occurrence of the pathogen in the excreta of the cockroaches in a dose-related fashion with outputs of 8 × 101 to 2 × 107 cells/defecation over a range of 3 to 20 days. The investigators observed that S. Typhimurium was recoverable about 10 days longer in the cockroach gut compared with the faeces, and persistence of the organism occurred primarily in the hindgut. In another experiment by Kopanic et al30 in 1993, it was shown that cockroaches could be infected with a naladixic acid-resistant strain of S. Typhimurium from a contaminated food source. The investigators also showed that the infected cockroaches could transmit the naladixic acid-resistant strain of S. Typhimurium to uninfected cockroaches, food (eggs), and water. A study by Zurek and Schal31 in 2004 investigated the vectorial potential of German cockroaches for verotoxigenic E. coli F18, an important porcine bacterial pathogen. Forty adult cockroaches were divided into 2 groups of 20 each; 1 group of cockroaches was exposed to E. coli F18 (5.0 × 105 CFUs mL) in 10 mL of phosphate buffer solution (PBS), while the second group (control) received 10 mL of sterile PBS. After 5 hours, the PBS was replaced with sterile tap water, and sterile piglet feed ration (collected from the swine farm) was supplied to both cockroach groups. Viable and virulent E. coli F18 cells were detectable in cockroach faeces for up to 8 days after the initial exposure, and the number of bacterial cells decreased over time. In the control group, no E. coli F18 organisms were detected in cockroach faeces. The average number of faecal coliforms in cockroach faeces was high (4.4 × 105 g1) and not significantly different from that found in piglet faeces (1.9 ± 0.8 × 106 g1). Using non-food-borne pathogens such as Helicobacter pylori32 and Mycobacterium avium subsp. paratuberculosis,33 other investigators have also demonstrated the vectorial potential of cockroaches through controlled laboratory studies.

Several observational studies on microbial carriage of cockroaches have been carried out in many parts of the world.34-45 As shown in Table 2, these studies report many different microorganisms including bacteria, parasites, fungi, and viruses. This is not surprising given the broad habitat range of cockroaches and the ubiquitous nature of microorganisms. Approximately, a quarter of the microorganisms reported in Table 2 are food-borne pathogens and will be discussed in detail.

Table 2.

Microbial carriage of cockroaches.

10.1177_1178630220913365-table2.tif

Food-borne bacterial pathogens isolated from cockroaches include Shigella boydii, Shigella dysenteriae, Shigella flexneri, Salmonella enterica subsp. enterica serovar Typhi, Salmonella Typhimurium, Escherichia coli O157:H7, Staphylococcus aureus, and Bacillus cereus. It is important to note the several species of Shigella and Salmonella that have been isolated from cockroaches, which probably indicates that cockroaches are an important reservoir for these bacteria.34-36,39 As Shigella spp. and S. Typhi are mainly sustained in humans,46-49 their occurrence in food is thought to be associated with food handlers. However, these organisms could be disseminated by cockroaches in food environments. Shigella spp. have a very low infective dose (101-102 cells) and cause bacillary dysentery (shigellosis), a highly invasive intestinal infection characterized by fever, violent abdominal cramps, rectal urgencies, and complications such as intestinal perforations, septicaemia, and toxic megacolon.46,47 In particular, a strain of S. dysenteriae (one of the Shigella spp. isolated from cockroaches) is implicated in severe epidemics of bacillary dysentery through the production of shiga toxins46,47. S. Typhi causes typhoid fever, which is a serious disease as it could lead to complications such as liver damage, inflammation of the heart, holes in the gut, and internal bleeding.48,49 The association of cockroaches with S. Typhi should be viewed with seriousness in developing countries where typhoid fever is most prevalent and lack of food hygiene is also of serious concern. S. Typhimurium causes a mild gastroenteritis and is often transmitted from animals through consumption of raw or undercooked animal source food such as meat.50,51 Compared with Shigella, Salmonella has a relatively high infective dose of 105 to 106 cells. The isolation of E. coli O157:H7 from cockroaches is interesting, as this organism emerged as a food-borne pathogen only in the 1990s.52 The organism resides in the intestinal tract of live animals and is shed in their faeces, which may contaminate food, water, and the environment.52-55 It has unusual persistence features in the environment and survives at low temperatures and under acidic conditions.52,55 The infective dose of E. coli O157:H7 is very small (10-100 cells) and is implicated in severe clinical conditions including, haemorrhagic colitis leading to bloody diarrhoea, haemolytic uremic syndrome and kidney damage.52-55 S. aureus and B. cereus, also isolated from cockroaches, are among the predominant food-borne pathogens globally. Both pathogens have an infective dose of 105 to 106 cells and produce toxins, which mediate the food-borne disease; S. aureus produces enteroxins, which cause diarrhoea,56 while B. cereus produces an emetic and enterotoxin responsible for vomiting and diarrhoea, respectively.57,58 B. cereus is a spore-forming bacteria and can therefore survive for a very long period in the environment, which enhances its chances of contaminating cockroaches.59,60

Compared with bacteria, the other types of food-borne microbes tend to be carried by cockroaches to a lesser extent. Four main food-borne parasites are reported to be carried by cockroaches: Cryptosporidium parvum, Cyclospora cayetanensis, Entamoeba histolytica, and Giardia duodenalis (Table 2). These pathogens are transmitted faecal-orally from ingestion of their oocyst/cysts, which can persist and survive for long periods in the environment, water, and on foods.61-64 Animals are known to be a reservoir of human infection for C. parvum and G. duodenalis, but not C. cayetanensis and E. histolytica.63,64 Among food-borne viruses, rotavirus and hepatitis A virus have been reported to be associated with cockroaches.28,43 Rotavirus is the leading cause of severe diarrhoea in young children globally, and is responsible for about 50% of paediatric diarrheal disease hospitalizations in developing countries.65-69 In this regard, the presence of cockroaches in homes could have serious implications for paediatric health. Hepatitis A is the most common form of acute viral hepatitis worldwide and therefore its association with cockroaches is a cause for concern, especially in the developing world where the infection is mostly prevalent.70 Several fungi implicated in food-borne infections have been isolated from cockroaches and include Aspergillus spp., Candida spp., Mucor spp., and Alternaria spp. (Table 2). Among these fungal pathogens, Aspergillus spp. poses the biggest threat to humans through the production of aflatoxins, which are extremely potent liver carcinogens.71,72 The most pathogenic species of Aspergillus is A. fumigatus, followed by A. flavus, both of which have been isolated from cockroaches.73-75

Conclusions and Further Research

Cockroaches could harbour and disseminate many food-borne microbial pathogens including bacteria, fungi, viruses, and parasites. These food-borne pathogens vary widely in their biological characteristics, host associations, virulence determinants, and transmissions. This implies that cockroaches could play a very broad role in food-borne infections. Given the association between cockroaches and food-borne pathogens, it is important to consider them in food-borne outbreak investigations, which has not been the case hitherto.

Further studies are needed to describe cockroach carriage of the several other food-borne pathogens that have not been reported previously. These include important food-borne pathogens such as C. perfringens, C. botulinum, Campylobacter spp., norovirus, and hepatitis A. In addition, there is the need for a better understanding regarding host–microbe relationships that occur between cockroaches and food-borne microbial pathogens. Microbiome studies could provide invaluable insights in this regard.

Considering the food-borne risks associated with cockroaches, their presence should not be tolerated in the food industry. Similarly, cockroaches should not be tolerated in the hospital setting as they might spread nosocomial pathogens such as S. aureus and E. coli. Efforts to control cockroaches should involve good hygiene and sanitation of facilities and also the application of proper insecticides to cockroach hiding spots.4,76,77 It is also important to remove hiding places of cockroaches such as cardboard, as this will prevent future infestations.

Author Contributions

ESD conceived the idea for this paper, undertook literature review and wrote the manuscript.

REFERENCES

1.

Cochran DG. Cockroaches.Geneva, Switzerland: World Health Organization; 1982. Google Scholar

2.

Cornwell PB. The Cockroach (Vol. 1).London, UK: Hutchinson; 1968. Google Scholar

3.

Roth LM , Willis ER. The biotic associations of cockroaches. Smithson Miscellaneous Collect. 1960;141:1—470. Google Scholar

4.

Donkor ES. Nosocomial pathogens: an in-depth analysis of the vectorial potential of cockroaches. Trop Med Infect Dis. 2019;4:14. Google Scholar

5.

World Health Organization. The World Health Organization estimates of the global burden of foodborne diseases: FERG project report. http://www.who.int/foodsafety/areas_work/foodborne-diseases/ferg/en/. Updated 2015. Google Scholar

6.

Kirk MD , Angulo FJ , Havelaar AH , Black RE. Diarrhoeal disease in children due to contaminated food. Bull World Health Organ. 2017;95:233—234. Google Scholar

7.

Nyachuba DG. Foodborne illness: is it on the rise? Nutr Rev. 2010;68:257—269. Google Scholar

8.

McPherson M , Kirk MD , Raupach J , Combs B , Butler JR. Economic costs of Shiga toxin-producing Escherichia coli infection in Australia. Foodborne Pathog Dis. 2011;8:55—62. Google Scholar

9.

Lake RJ , Cressey PJ , Campbell DM , Oakley E. Risk ranking for foodborne microbial hazards in New Zealand: burden of disease estimates. Risk Anal. 2010;30:743—752. Google Scholar

10.

Toljander J , Dovarn A , Andersson Y , Ivarsson S , Lindqvist R. Public health burden due to infections by verocytotoxin-producing Escherichia coli (VTEC) and Campylobacter spp. as estimated by cost of illness and different approaches to model disability-adjusted life years. Scand J Public Health. 2012;40:294—302. Google Scholar

11.

Centers for Disease Control and Prevention. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-10 states, 2007. MMWR Morb Mortal Wkly Rep. 2008;57:366—370. Google Scholar

12.

Viray MA , Hofmeister MG , Johnston DI , et al. Public health investigation and response to a hepatitis a outbreak from imported scallops consumed raw-Hawaii, 2016 [published online ahead of print October 17, 2018]. Epidemiol Infect. doi: https://doi.org/10.1017/S0950268818002844. Google Scholar

13.

Lake RJ , Cressey PJ , Campbell DM , Oakley E. Risk ranking for foodborne microbial hazards in New Zealand: burden of disease estimates. Risk Anal. 2010;30:743—752. Google Scholar

14.

Scallan E , Hoekstra RM , Mahon BE , Jones TF , Griffin PM. An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol Infect. 2015;143:2795—2804. Google Scholar

15.

Redel H. Foodborne infections and intoxications, 4th edition. Emerg Infect Dis. 2013;19:2067. Google Scholar

16.

Adak GK , Long SM , O’Brien SJ. Trends in indigenous foodborne disease and deaths, England and Wales: 1992 to 2000. Gut. 2002;51:832—841. Google Scholar

17.

Braden CR , Tauxe RV. Emerging trends in foodborne diseases. Infect Dis Clin North Am. 2013;27:517—533. Google Scholar

18.

Tauxe RV. Emerging foodborne pathogens. Int J Food Microbiol. 2002;78:31—41. Google Scholar

19.

Lindahl JF , Grace D. The consequences of human actions on risks for infectious diseases: a review. Infect Ecol Epidemiol. 2015;5:30048. Google Scholar

20.

Grace D. Food safety in low and middle income countries. Int J Environ Res Public Health. 2015;12:10490—10507. Google Scholar

21.

Glass RI , Parashar UD , Estes MK. Norovirus gastroenteritis. N Engl J Med. 2009;361:1776—1785. Google Scholar

22.

Behravesh CB , Williams IT , Tauxe RV. Improving Food Safety through a One Health Approach: Workshop Summary Institute of Medicine (US).Washington, DC: National Academies Press; 2012. Google Scholar

23.

Patrick ME , Mahon BE , Zansky SM , Hurd S , Scallan E. Riding in shopping carts and exposure to raw meat and poultry products: prevalence of, and factors associated with, this risk factor for Salmonella and Campylobacter infection in children younger than 3 years. J Food Prot. 2010;73:1097—1100. Google Scholar

24.

Brynestad S , Granum PE. Clostridium perfringens and foodborne infections. Int J Food Microbiol. 2002;74:195—202. Google Scholar

25.

Tewari A , Abdullah S. Bacillus cereus food poisoning: international and Indian perspective. J Food Sci Technol. 2015;52:2500—2511. Google Scholar

26.

Kothary MH , Babu US. Infective dose of foodborne pathogens in volunteers: a review. J Food Saf. 2001;21:49—73. Google Scholar

27.

Sinell HJ. Control of foodborne infections and intoxications. Int J Food Microbiol. 1995;25:209—217. Google Scholar

28.

Tarshis IB. The cockroach: a new suspect in the spread of infectious hepatitis. Am J Trop Med Hyg. 1962;11:705—711. Google Scholar

29.

Ash N , Greenberg B. Vector potential of the German cockroach (Dictyoptera: Blattellidae) in dissemination of Salmonella enteritidis serotype Typhimurium. J Med Entomol. 1980;17:417—423. Google Scholar

30.

Kopanic RJJr Sheldon BW , Wright CG. Cockroaches as vectors of salmonella: laboratory and field trials. J Food Prot. 1994;57:125—135. Google Scholar

31.

Zurek L , Schal C. Evaluation of the German cockroach (Blattella germanica) as a vector for verotoxigenic Escherichia coli F18 in confined swine production. Vet Microbiol. 2004;101:263—267. Google Scholar

32.

Imamura S , Kita M , Yamaoka Y , et al. Vector potential of cockroaches for Helicobacter pylori infection. Am J Gastroenterol. 2003;98:1500—1503. Google Scholar

33.

Fischer OA , Matlova L , Dvorska L , Svastova P , Pavlik I. Nymphs of the Oriental cockroach (Blatta orientalis) as passive vectors of causal agents of avian tuberculosis and paratuberculosis. Med Vet Entomol. 2003;17:145—150. Google Scholar

34.

Fotedar R , Nayar E , Samantray JC , et al. Cockroaches as vectors of pathogenic bacteria. J Commun Dis. 1989;21:318—322. Google Scholar

35.

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

36.

Oothuman P , Jeffery J , Aziz AH , 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

37.

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

38.

Fotedar R , Shriniwas UB , Verma A. Cockroaches (Blattella germanica) as carriers of microorganisms of medical importance in hospitals. Epidemiol Infect. 1991;107:181—187. Google Scholar

39.

Moges F , Eshetie S , Endris M , et al. Cockroaches as a source of high bacterial pathogens with multidrug resistant strains in Gondar Town, Ethiopia. Biomed Res Int. 2016;2016:2825056. Google Scholar

40.

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

41.

Naher A , Afroz S , Hamid S. Cockroach associated foodborne pathogens: distribution and antibiogram. Bangladesh Med Res Counc Bull. 2018;44:30—38. Google Scholar

42.

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

43.

Tetteh-Quarcoo PB , Donkor ES , Attah SK , et al. Microbial carriage of cockroaches at a tertiary care hospital in Ghana. Environ Health Insights. 2013;7:59—66. Google Scholar

44.

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

45.

Oyeyemi OT , Agbaje MO , Okelue UB. Food-borne human parasitic pathogens associated with household cockroaches and houseflies in Nigeria. Parasite Epidemiol Cont. 2016;1:10—13. Google Scholar

46.

Khalil IA , Troeger C , Blacker BF , et al. Morbidity and mortality due to shigella and enterotoxigenic Escherichia coli diarrhoea: the Global Burden of Disease Study 1990-2016. Lancet Infect Dis. 2018;18:1229—1240. Google Scholar

47.

Lanata CF , Black RE. Estimating the true burden of an enteric pathogen: enterotoxigenic Escherichia coli and Shigella spp. Lancet Infect Dis. 2018;18:1165—1166. Google Scholar

48.

Butler T , Knight J , Nath SK , Speelman P , Roy SK , Azad MAK , . Typhoid fever complicated by intestinal perforation: a persisting fatal disease requiring surgical management. Rev Infect Dis. 1985;7:244—256. Google Scholar

49.

Edelman R , Levine MM. Summary of an international workshop on typhoid fever. Rev Infect Dis. 1986;8:329—349. Google Scholar

50.

Helms M , Ethelberg S , Molbak K. International Salmonella typhimurium DT104 infections, 1992-2001. Emerg Infect Dis. 2005;11:859—867. Google Scholar

51.

Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis. 2001;15:263—269. Google Scholar

52.

Doyle MP. Escherichia coli O157:H7 and its significance in foods. Int J Food Microbiol. 1991;12:289—301. Google Scholar

53.

Bystrom PV , Beck RJ , Prahlow JA , . Hemolytic uremic syndrome caused by E. coli O157 infection. Forensic Sci Med Pathol. 2017;13:240—244. Google Scholar

54.

Donkor ES , Lanyo R , Akyeh ML , Kayang BB , Quaye DA. Monitoring enterohaemorrhagic Escherichia coli O157:H7 in the vegetable food chain in Ghana. Res J Microbiol. 2008;3:423—428. Google Scholar

55.

Chekabab SM , Paquin-Veillette J , Dozois CM , Harel J. The ecological habitat and transmission of Escherichia coli O157:H7. FEMS Microbiol Lett. 2013;341:1—12. Google Scholar

56.

Argudín MÁ , Mendoza MC , Rodicio MR , . Food poisoning and Staphylococcus aureus enterotoxins. Toxins. 2010;2:1751—1773. Google Scholar

57.

Granum PE , Brynestad S , Kramer JM. Analysis of enterotoxin production by Bacillus cereus from dairy products, food poisoning incidents and non-gastrointestinal infections. Int J Food Microbiol. 1993;17:269—279. Google Scholar

58.

Tewari A , Singh SP , Singh R. Incidence and enterotoxigenic profile of Bacillus cereus in meat and meat products of Uttarakhand, India. J Food Sci Technol. 2015;52:1796—1801. Google Scholar

59.

Andersson A , Ronner U , Granum PE. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int J Food Microbiol. 1995;28:145—155. Google Scholar

60.

Setlow P. Spore resistance properties. Microbiol Spectr. 2014;2:1—14. Google Scholar

61.

Anim-Baidoo I , Narh CA , Oddei D , Brown CA , Enweronu-Laryea C , Bandoh B , Sampane-Donkor E , Armah G , Adjei AA , Adjei DN , Ayeh-Kumi PF , Gyan BA , . Giardia lamblia infections in children in Ghana. Pan Afr Med J. 2016; 24:217. Google Scholar

62.

Jokipii L , Jokipii AM. Timing of symptoms and oocyst excretion in human cryptosporidiosis. New Engl J Med. 1986;315:1643—1647. Google Scholar

63.

Rose JB , Slifko TR. Giardia, Cryptosporidium, and Cyclospora and their impact on foods: review. J Food Protect. 1999;62:1059—1070. Google Scholar

64.

Ravdin J , , ed. Amoebiasis: Human Infection by Entamoeba Histolytica.New York, NY: John Wiley and Sons; 1988. Google Scholar

65.

Tate JE , Burton AH , Boschi-Pinto C , Steele AD , Duque J , Parashar UD. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12:136—141. Google Scholar

66.

Revelas A. Acute gastroenteritis among children in the developing world. South Afr J Epidemiol Infect. 2012;27:156—162. Google Scholar

67.

Elliott EJ. Acute gastroenteritis in children. BMJ Open. 2007;334:35—40. Google Scholar

68.

World Health Organization. Rotavirus vaccines WHO position paper: January 2013. Weekly Epidemiol Rec Health Sect Secr Leag Nations. 2013;88:49—64. Google Scholar

69.

Damanka S , Adiku TK , Armah GE , et al. Rotavirus infection in children with diarrhea at Korle-Bu teaching hospital, Ghana. Jpn J Infect Dis. 2016;69:331—334. Google Scholar

70.

Franco E , Meleleo C , Serino L , Sorbara D , Zaratti L. Hepatitis A: Epidemiology and prevention in developing countries. World J Hepatol. 2012;4:68—73. Google Scholar

71.

Benedict K , Chiller TM , Mody RK. Invasive fungal infections acquired from contaminated food or nutritional supplements: a review of the literature. Foodborne Pathog Dis. 2016;13:343—349. Google Scholar

72.

Takatori K , Aihara M , Sugita-Konishi Y. Hazardous food-borne fungi and present and future approaches to the mycotoxin regulations in Japan. Kokuritsu Iyakuhin Shokuhin Eisei Kenkyusho Hokoku. 2006;124:21—29. Google Scholar

73.

Raper KB , Fennel DI. The Genus Aspergillus.Baltimore, MD: Williams and Wilkins; 1965. Google Scholar

74.

Araujo R , Rodrigues AG. Variability of germinative potential among pathogenic species of Aspergillus. J Clin Microbiol. 2004;42:4335—4337. Google Scholar

75.

Paulussen C , Hallsworth JE , Álvarez-Pérez S , et al. Ecology of aspergillosis: insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species. Microb Biotechnol. 2017;10:296—322. Google Scholar

76.

Potter MF. The perfect storm: an extension view on bed bugs. Am Entomol. 2006;52:102—104. Google Scholar

77.

Goddard J. Public Health Entomology.Boca Raton, FL: CRC Press; 2012. Google Scholar
© The Author(s) 2020 This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
Eric S Donkor "Cockroaches and Food-borne Pathogens," Environmental Health Insights 14(1), (20 May 2020). https://doi.org/10.1177/1178630220913365
Received: 23 January 2020; Accepted: 19 March 2020; Published: 20 May 2020
KEYWORDS
Antibiotic resistance
cockroach
Escherichia coli O157:H7
food-borne pathogens
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