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      Role of Flies as Vectors of Foodborne Pathogens in Rural Areas


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          This study aims to evaluate flies as a vector for foodborne pathogens. For this purpose, several flies were collected from different sites from rural areas. These flies were then analyzed for the presence of Enterobacteriaceae, Escherichia coli, Staphylococcus coagulase positive, and Listeria monocytogenes. Another aim of this study was to evaluate some virulence factors of the collected pathogens: susceptibility to some antibiotics and the presence of enterotoxigenic S. aureus. The results showed that flies in the presence of animals demonstrated a significantly higher prevalence of the studied pathogens than those collected in the kitchens, and kitchens situated in the closest proximity to the animal husbandry had a higher count than the kitchens in private houses. Enterobacteriaceae was the indicator organism with the highest microbial counts followed by E. coli and S. aureus. Listeria monocytogenes was not detected from any of the collected flies. The antimicrobial susceptibility test showed that the bacteria carried by the flies possessed multiantibiotic resistance profiles, and enterotoxin A was produced by 17.9% of the confirmed S. aureus isolates. These results demonstrate that flies can transmit foodborne pathogens and their associated toxin and resistance and the areas of higher risk are those in closer proximity to animal production sites.

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          Fly Transmission of Campylobacter

          An annual increase in Campylobacter infection in England and Wales begins in May and reaches a maximum in early June. This increase occurs in all age groups and is seen in all geographic areas. Examination of risk factors that might explain this seasonal increase identifies flies as a potential source of infection. The observed pattern of infection is hypothesized to reflect an annual epidemic caused by direct or indirect contamination of people by small quantities of infected material carried by flies that have been in contact with feces. The local pattern of human illness appears random, while having a defined geographic and temporal distribution that is a function of the growth kinetics of one or more fly species. The hypothesis provides an explanation for the seasonal distribution of Campylobacter infections seen around the world. Campylobacter spp. are the most common bacterial causes of diarrhea in England and Wales (1). The epidemiologic features of Campylobacter infection have proved difficult to discover, and extensive strain typing has failed to clarify the main transmission routes. Testable hypotheses must be established to explain available evidence, particularly the reason for the observed seasonality. Relatively few outbreaks of Campylobacter gastroenteritis occur (2), and most cases are sporadic. In case-control and case-case studies of sporadic Campylobacter infections, most cases remain unexplained by recognized risk factors (3,4). The annual increase in Campylobacter infections in England and Wales begins at approximately day 130 (May 9) and reaches a maximum at approximately day 160 (June 8) (Figure 1). Although this seasonal rise is seen in all ages, it is more marked in children (5). Cases in towns and cities across England and Wales show broadly similar seasonal changes in distribution (Figure 2). The relative geographic uniformity of the increase seen in May of most years has the temporal appearance of an annual national epidemic. Because person-to-person infection within the community is uncommon, it is likely that the epidemic is caused by a single main driver for human Campylobacter infection. The possible seasonal drivers were examined, and only vector transmission by flies appears to provide a convincing explanation for the observed seasonal trends (Table). Figure 1 Distribution of Campylobacter cases per day. When averaged for 1989 to 2002, the epidemic begins at approximately day 130, peaks at approximately day 160, and gradually declines through the rest of the year. Figure 2 Cases of Campylobacter infection in England and Wales based on the patient specimen date. Figure shows broadly similar changes in patterns of infection across the country as measured by laboratory reporting per town or city (cases as a percentage of the annual total) by day of year. Laboratories were ordered by the total number of cases reported over the 14-year period (Appendix). Table Risk factors that might affect Campylobacter seasonality* Risk factor Outbreaks Evidence of seasonality Credibility as the main seasonal driver Barbecuing Yes Medium Low Birds Yes Strong Low Bottled water No None Low Chicken Yes Medium Medium Cross-contamination Yes None None Domestic catering No None None Farm visit Yes None None Farm animals Yes Weak Low Flies No Strong High Food handlers Yes None None Food packaging No None None Immunologic response No Weak None Mains supply drinking water Yes None None Nosocomial Yes None None Pets No Weak Low Pools, lakes, streams No None None Private drinking water supplies Yes Weak None Protozoa No None Low Salads and fruit Yes Weak Low Stir-fried food Yes None None The countryside No Weak Medium Transmission in families Yes None None Travel abroad No None None Unpasteurized milk Yes Weak None Weather/climate No Medium Medium *Evidence base provided in Appendix. The seasonal increase in Campylobacter infections in May and June in England and Wales is hypothesized to reflect an annual epidemic caused by direct or indirect exposure of humans to contaminated material carried by several fly species that have been in contact with human, bird, or animal feces or contaminated raw foods. Flies have been shown to carry Campylobacter and can infect both humans and animals (6–8). Intervention studies have demonstrated diarrheal disease reduction linked to control of flies (9–11), and deaths from diarrheal diseases have been linked to measurements of fly abundance (12). The local pattern of human Campylobacter infection appears random, while having a defined geographic and temporal distribution. This distribution is predicted to be linked to the growth kinetics of 1 or more fly species and their access to environmental sources of Campylobacter in feces or food. The seasonal increase in fly populations results from rainy weather and an increase in temperature that causes the development from egg to fly to occur in days rather than months. Individual flies can lay hundreds of eggs, which can result in a large increase in fly numbers in a short period. Fly numbers fluctuate through the summer and decline in October, but the decline is less dramatic and defined than the spring increase. Disease transmission is hypothesized to occur through small quantities of contaminated material carried on the feet, proboscis, legs, and body hairs or from material regurgitated or defecated by flies. The variety, numbers, virulence and viability of organisms in the contaminated material will differ, and some contamination will include Campylobacter while others will not. Contamination will be distributed over a variety of food types. Contamination of food by flies could occur at any stage of the food supply chain, but Campylobacter counts within the contaminated material on foods will decrease over time; consequently, most infection will result from contamination close to consumption (e.g., in the domestic or catering environment). Because whether a fly has visited contaminated feces is unknown and how a person becomes infected is uncertain, epidemiologic investigation is difficult. A number of synanthropic fly species could be involved, including houseflies (e.g., Musca spp., Fannia spp.), blowflies (e.g., Calliphora spp., Lucilia spp.), and other dung-related flies (e.g., Sarcophaga spp., Drosophila spp.) (13). These flies have individual behavioral patterns, ecology, physiology, and temporal and geographic distributions that will influence the likelihood of their being in kitchens, on human or animal feces, and on food. Although Musca domestica is the species most likely to be involved because it is commonly found in houses and food-processing establishments, larger flies (e.g., Calliphora spp.) may be able to transmit larger numbers of Campylobacter. Flies contaminated through fecal contact will carry heterogeneous mixtures of organisms, including any pathogens that are present within the feces, and may be able to cause a variety of human infections, including infection by different Campylobacter species and types. This fact partially explains the lack of a clear epidemiologic picture arising from Campylobacter typing work. Gastrointestinal disease caused by flies is more likely to involve pathogens with a low infectious dose (e.g., Shigella, Campylobacter, Cryptosporidium, Giardia, Cyclospora, Escherichia coli O157), and some of these could have a seasonal component related to flies. Where high fly populations and poor hygiene conditions prevail, as in disasters or famines, or where pathogens can grow within fly-contaminated food, the potential exists for transmitting pathogens with a high infectious dose (e.g., Vibrio cholerae, Salmonella spp.). The access that flies have to human and animal feces will influence the degree to which they are contaminated with different enteric pathogens. Contamination of a range of foods by flies will result in a pattern of infection that will not be amenable to identifying specific vehicles through standard case-control, case-case, or cohort studies, unless specific objective or subjective assessments of fly numbers can be obtained. Fly monitoring will need to be undertaken. An alternative approach could use estimates of fly population numbers based on climatic conditions to compare with data on human Campylobacter infections. This approach has the advantage of being able to use historical climatic and disease surveillance data. The broad relationship between Campylobacter cases and ambient temperature has not been explained in terms of disease causation. The time taken for the larvae of M. domestica to develop (13) was applied to temperature data for England and Wales and has been used to show a strong relationship between Campylobacter cases per week and M. domestica larval development time for 1989 to 1999 (Figure 3). Periods when Campylobacter cases exceed a 7-day average of 170 cases per day occurred when M. domestica larval development time was <3 weeks. Figure 3 Campylobacter cases by week and Musca domestica larval growth times. Campylobacter cases per day are plotted against the minimum M. domestica growth times for the 14 days before the date for weeks from January 1989 to December 1999. The time taken for M. domestica larvae to develop was based on understood growth temperatures (145 days divided by the number of degrees above 12°C, up to an optimum of 36°C) (8). The temperatures were based on a maximum temperature in 47 temperature sampling sites across England and Wales in the 2 weeks before (Appendix). The hypothesis predicts that the Campylobacter infection rates will be higher in persons living close to animal production and lower in urban settings because fly numbers will be lower. Some evidence from the United Kingdom (1,14) and Norway (15) supports this hypothesis. Seasonal changes in Campylobacter incidence that are seen around the world may result from changes in fly populations and flies' access to human and animal feces. Much emphasis on foodborne disease reduction has rightly been on kitchen hygiene, since the low infectious dose of Campylobacter makes cross-transmission from raw meats to ready-to-eat foods a substantial risk in domestic and catering environments. Fly transmission may be the most important source of infection in kitchen transmission routes, and establishments that sell ready-to-eat foods may be sources of Campylobacter, if effective fly control is not in operation. Flies may also be important in transmitting Campylobacter in poultry flocks (16) and between other agricultural animals. While flies are regarded as important mechanical vectors of diarrheal disease in developing countries, control has largely concentrated on improving drinking water and sewage disposal. In the industrialized world, flies are thought to play a minor role in the transmission of human diarrheal diseases. Immediately intervening in the transmission of Campylobacter gastroenteritis should be possible through increased public awareness and more effective fly control. Appendix Supplementary Information Temperature Data Temperature data were acquired from the British Atmospheric Data Centre (BADC), the Natural Environment Research Council's (NERC) Designated Data Centre for the Atmospheric Sciences based at the Rutherford Appleton Laboratory in Oxfordshire, part of the Central Laboratory of the Research Councils. Data are available on-line through a World Wide Web interface ( http://badc.nerc.ac.uk ) by prearranged agreement. Data were collated for the period 1989–1999, with 5 locations selected for each region to provide overall coverage of the region (except London, which had only 2 centers with data available for the given time period). Location of temperature stations is shown in the Figure A1. There were a total of 47 sites. Some of the data series were missing data points. The maximum, minimum, and average temperatures were determined for all days between January 1, 1989, and December 31, 1999. Maximum temperatures across all sites were used to calculate the presumptive minimum Musca domestica larval development times. Methods The data represent patients who had fecal specimens examined by a microbiology laboratory in England and Wales between 1989 and 2003 where Campylobacter was isolated from the sample. Data were acquired through well-described surveillance processes, and analysis was conducted in Microsoft Access and Excel (Microsoft Corp., Redmond, WA, USA). Daily cases were based on the patient specimen date, and a 7-day rolling mean was used to eliminate the weekly cycles that reflect reduced patient sampling on weekends. Hypothesis generation was performed through a systematic review of known and suggested causes of Campylobacter infection, particularly reflecting on changes in these risks over the period of May and June and assessing their credibility as biological drivers for the observed seasonality. Cities and Towns Included in Figure A1 S1, London; S2, Birmingham; S3, Bristol; S4, Nottingham; S5, Sheffield; S6, Manchester; S7, Leeds; S8, Leicester; S9, Reading; S10, Plymouth; S11, Portsmouth; S12, Colchester; S13, Bradford; S14, Southampton; S15, Poole; S16, Preston; S17, Cardiff; S18, Chelmsford; S19, Norwich; S20, Ipswich; S21, Truro; S22, Oxford; S23, Shrewsbury; S24, Dudley; S25, Taunton; S26, Newport; S27, Cambridge; S28, Newcastle; S29, Chester; S30, Gloucester; S31, Swindon; S32, Chertsey; S33, Coventry; S34, Welwyn; S35, Frimley Park; S36, High Wycombe; S37, Slough; S38, Exeter; S39, Swansea; S40, Luton; S41, Torquay; S42, Derby; S43, York; S44, Worcester; S45, Northampton; S46, Bishops Stortford; S47, Hull; S48, Basildon; S49, Stoke-on-Trent; S50, Worthing; S51, Stafford; S52, Harrogate; S53, Hereford; S54, Halifax; S55, Sunderland; S56, Chesterfield and N Derbyshire; S57, Lincoln; S58, Ashford Kent; S59, Stockport; S60, Blackpool; S61, Maidstone; S62, Liverpool; S63, Bangor; S64, Llandough; S65, Lancaster; S66, Sutton Coldfield; S67, Aylesbury; S68, Grimsby; S69, Doncaster; S70, Peterborough; S71, Brighton; S72, Gateshead; S73, Kettering; S74, Southend; S75, Rhyl; S76, Cheltenham; S77, Epsom; S78, Chichester; S79, Carlisle; S80, Milton Keynes; S81, Dorchester; S82, Durham; S83, Bury; S84, Great Yarmouth; S85, Bury St Edmunds; S86, Warwick; S87, Salisbury; S88, Wolverhampton; S89, Scarborough; S90, Pontefract; S91, Bath; S92, Winchester; S93, Bishop Auckland; S94, Watford; S95, Bolton; S96, Eastbourne; S97, Oldham; S98, North Shields; S99, Burnley; S100, Ashford Middlesex; S101, Kings Lynn; S102, Warrington; S103, Wakefield; S104, Keighley; S105, Crawley; S106, Barnstaple; S107, Abergavenney; S108, Boston; S109, Nuneaton; S110, Northallerton; S111, Wrexham; S112, Macclesfield; S113, Darlington; S114, Bedford; S115, Basingstoke; S116, Weston Supermare; S117, Middlesborough; S118, Dewsbury; S119, Sutton-in-Ashfield; S120, Rochdale; S121, Guildford; S122, Worksop; S123, Wigan; S124, Stevenage; S125, Bridgend; S126, Rotherham; S127, West Bromwich; S128, Solihull; S129, Burton-upon-Trent; S130, Haverford West; S131, Carmarthen; S132, Hemel Hempstead; S133, Stockton-on-Tees; S134, Huddersfield; S135, South Shields; S136, Barnsley; S137, Whitehaven; S138, Chatham; S139, Blackburn; S140, Redditch; S141, St Leonards-on-Sea; S142, Grantham and Kesteven; S143, Ormskirk; S144, Scunthorpe; S145, Canterbury; S146, Kidderminster; S147, Dartford; S148, Aberystwyth; S149, Hexham; S150, Barrow-in Furness; S151, Redhill; S152, Margate; S153, Walsall; S154, Ashington; S155, Salford; S156, Merthyr Tydfil; S157, Stourbridge; S158, Haywards Heath; S159, Banbury; S160, Hartlepool; S161, Prescot; S162, Otley; S163, Southport; S164, Yeovil; S165, Llanelli. 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            • Abstract: found
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            Isolation of Salmonella enterica serovar Enteritidis from houseflies (Musca domestica) found in rooms containing Salmonella serovar Enteritidis-challenged hens.

            Houseflies (Musca domestica) released into rooms containing hens challenged with Salmonella enterica serovar Enteritidis (Salmonella serovar Enteritidis) rapidly became contaminated with Salmonella serovar Enteritidis. Forty to 50% of the flies were contaminated at 48 h, and the percentage increased to 50 to 70% at 4 and 7 days postexposure and then decreased to 30% at day 15. Initial attempts at recovering surface organisms for culture using an aqueous rinse were largely unsuccessful, while cultures of internal contents readily recovered Salmonella serovar Enteritidis. However, when 0.5% detergent was incorporated into the rinse, high recovery levels of bacteria were observed from both external and internal culture regimens, indicating equal distribution of the organism on and in the fly and a tighter interaction of the organism with the host than previously thought. Salmonella serovar Enteritidis was isolated routinely from the fly gut, on rare occasions from the crop, and never from the salivary gland. Feeding contaminated flies to hens resulted in gut colonization of a third of the birds, but release of contaminated flies in a room containing previously unchallenged hens failed to result in colonization of any of the subject birds. These results indicate that flies exposed to an environment containing Salmonella serovar Enteritidis can become colonized with the organism and might serve as a source for transmission of Salmonella serovar Enteritidis within a flock situation.
              • Record: found
              • Abstract: found
              • Article: not found

              Ecology of antibiotic resistance genes: characterization of enterococci from houseflies collected in food settings.

              In this project, enterococci from the digestive tracts of 260 houseflies (Musca domestica L.) collected from five restaurants were characterized. Houseflies frequently (97% of the flies were positive) carried enterococci (mean, 3.1 x 10(3) CFU/fly). Using multiplex PCR, 205 of 355 randomly selected enterococcal isolates were identified and characterized. The majority of these isolates were Enterococcus faecalis (88.2%); in addition, 6.8% were E. faecium, and 4.9% were E. casseliflavus. E. faecalis isolates were phenotypically resistant to tetracycline (66.3%), erythromycin (23.8%), streptomycin (11.6%), ciprofloxacin (9.9%), and kanamycin (8.3%). Tetracycline resistance in E. faecalis was encoded by tet(M) (65.8%), tet(O) (1.7%), and tet(W) (0.8%). The majority (78.3%) of the erythromycin-resistant E. faecalis isolates carried erm(B). The conjugative transposon Tn916 and members of the Tn916/Tn1545 family were detected in 30.2% and 34.6% of the identified isolates, respectively. E. faecalis carried virulence genes, including a gelatinase gene (gelE; 70.7%), an aggregation substance gene (asa1; 33.2%), an enterococcus surface protein gene (esp; 8.8%), and a cytolysin gene (cylA; 8.8%). Phenotypic assays showed that 91.4% of the isolates with the gelE gene were gelatinolytic and that 46.7% of the isolates with the asa1 gene aggregated. All isolates with the cylA gene were hemolytic on human blood. This study showed that houseflies in food-handling and -serving facilities carry antibiotic-resistant and potentially virulent enterococci that have the capacity for horizontal transfer of antibiotic resistance genes to other bacteria.

                Author and article information

                ISRN Microbiol
                ISRN Microbiol
                ISRN Microbiology
                Hindawi Publishing Corporation
                4 August 2013
                : 2013
                : 718780
                CBQF-Centro de Biotecnologia e Química Fina, Laboratório Associado, Escola Superior de Biotecnologia, Universidade Católica Portuguesa/Porto, Rua Dr. António Bernardino Almeida, 4200-072 Porto, Portugal
                Author notes

                Academic Editors: J.-F. Cavin, R. E. Levin, and A. Sunna

                Author information
                Copyright © 2013 Cláudia Barreiro et al.

                This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                : 17 June 2013
                : 13 July 2013
                Research Article


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