1921
Volume 98, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Consumption of contaminated stored food can cause childhood diarrhea. Flies carry enteropathogens, although their contribution to food contamination remains unclear. We investigated the role of flies in contaminating stored food by collecting food and flies from the same households in rural Bangladesh. We selected 182 households with children ≤ 24 months old that had stored foods for later feeding at room temperature for ≥ 3 hours. We collected food samples and captured flies with fly tapes hung by the kitchen. We used the IDEXX Quanti-Tray System (Colilert-18 media; IDEXX Laboratories, Inc., Westbrook, ME) to enumerate with the most probable number (MPN) method. –positive IDEXX wells were analyzed by polymerase chain reaction for pathogenic genes (, , , , , , , , , and ). was detected in 61% (111/182) of food samples, with a mean of 1.1 log MPN/dry g. Fifteen samples (8%) contained pathogenic ; seven (4%) had enteropathogenic (EPEC) genes ( and/or ); and 10 (5%) had enteroaggregative genes ( and/or ). Of flies captured in 68 (37%) households, was detected in 41 (60%, mean 2.9 log MPN/fly), and one fly (1%) had an EPEC gene (). For paired fly-food samples, each log MPN increase in flies was associated with a 0.31 log MPN increase in stored food (95% confidence interval: 0.07, 0.55). In rural Bangladesh, flies possibly a likely route for fecal contamination of stored food. Controlling fly populations may reduce contamination of food stored for young children.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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2018-10-16
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References

  1. WHO, 2009. Global Strategy for Infant and Young Child Feeding. Geneva, Switzerland: World Health Organization.
  2. Przyrembel H, , 2012. Timing of introduction of complementary food: short-and long-term health consequences. Ann Nutr Metab 60: 820.
  3. Islam MS, Mahmud ZH, Gope PS, Zaman RU, Hossain Z, Islam MS, Mondal D, Sharker MAY, Islam K, Jahan H, , 2013. Hygiene intervention reduces contamination of weaning food in Bangladesh. Trop Med Int Health 18: 250258.
  4. Islam MA, Ahmed T, Faruque ASG, Rahman S, Das SK, Ahmed D, Fattori V, Clarke R, Endtz HP, Cravioto A, , 2012. Microbiological quality of complementary foods and its association with diarrhoeal morbidity and nutritional status of Bangladeshi children. Eur J Clin Nutr 66: 12421246.
  5. Henry FJ, Patwary Y, Huttly SRA, Aziz KMA, , 1990. Bacterial contamination of weaning foods and drinking water in rural Bangladesh. Epidemiol Infect 104: 7985.
  6. Kung’u JK, Boor KJ, Ame SM, Ali NS, Jackson AE, Stoltzfus RJ, , 2009. Bacterial populations in complementary foods and drinking-water in households with children aged 10–15 months in Zanzibar, Tanzania. J Health Popul Nutr 27: 4152.
  7. Afifi ZE, Nasser SS, Shalaby S, Atlam SA, , 1998. Contamination of weaning foods: organisms, channels, and sequelae. J Trop Pediatr 44: 335337.
  8. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, , 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209222.
  9. Oo K, Sebastian A, Aye T, , 1989. Carriage of enteric bacterial pathogens by house flies in Yangon, Myanmar. J Diarrhoeal Dis Res 7: 8184.
  10. De Jesüs AJ, Olsen AR, Bryce JR, Whiting RC, , 2004. Quantitative contamination and transfer of Escherichia coli from foods by houseflies, Musca domestica L. (Diptera: Muscidae). Int J Food Microbiol 93: 259262.
  11. Khalil K, Lindblom GB, Mazhar K, Kaijser B, , 1994. Flies and water as reservoirs for bacterial enteropathogens in urban and rural areas in and around Lahore, Pakistan. Epidemiol Infect 113: 435444.
  12. Butler JF, Garcia-Maruniak A, Meek F, Maruniak JE, , 2010. Wild Florida house flies (Musca domestica) as carriers of pathogenic bacteria. Fla Entomol 93: 218223.
  13. Echeverria P, Harrison BA, Tirapat C, McFarland A, , 1983. Flies as a source of enteric pathogens in a rural village in Thailand. Appl Environ Microbiol 46: 3236.
  14. Szalanski AL, Owens CB, McKay T, Steelman CD, , 2004. Detection of Campylobacter and Escherichia coli O157: H7 from filth flies by polymerase chain reaction. Med Vet Entomol 18: 241246.
  15. Nazni WA, Seleena B, Lee HL, Jeffery J, Rogayah TAR, Sofian MA, , 2005. Bacteria fauna from the house fly, Musca domestica (L.). Trop Biomed 22: 225231.
  16. Farag TH, Faruque AS, Wu Y, Das SK, Hossain A, Ahmed S, Ahmed D, Nasrin D, Kotloff KL, Panchilangam S, , 2013. Housefly population density correlates with shigellosis among children in Mirzapur, Bangladesh: a time series analysis. PLoS Negl Trop Dis 7: e2280.
  17. Collinet-Adler S, Babji S, Francis M, Kattula D, Premkumar PS, Sarkar R, Mohan VR, Ward H, Kang G, Balraj V, , 2015. Environmental factors associated with high fly densities and diarrhea in Vellore, India. Appl Environ Microbiol 81: 60536058.
  18. Graczyk TK, Knight R, Gilman RH, Cranfield MR, , 2001. The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 3: 231235.
  19. Kuhns DM, Anderson TG, , 1944. A fly-borne bacillary dysentery epidemic in a large military organization. Am J Public Health Nations Health 34: 750755.
  20. Irish S, Aiemjoy K, Torondel B, Abdelahi F, Ensink JHJ, , 2013. Characteristics of latrines in central Tanzania and their relation to fly catches. PLoS One 8: e67951.
  21. Meyer J, Shultz T, , 1990. Stable fly and house fly breeding sites on dairies. Calif Agric 44: 2829.
  22. Nash J, , 1909. House flies as carriers of disease. Epidemiol Infect 9: 141169.
  23. West LS, , 1951. The House Fly its Natural History, Medical Importance, and Control. New York, NY: Comstock Publishing Company.
  24. Olsen AR, , 1998. Regulatory action criteria for filth and other extraneous materials. III. Review of flies and foodborne enteric disease. Regul Toxicol Pharmacol 28: 199211.
  25. Wolff H, Van Zijl W, , 1969. Houseflies, the availability of water, and diarrhoeal diseases. Bull World Health Organ 41: 952959.
  26. Wright EP, , 1983. The isolation of Campylobacter jejuni from flies. J Hyg (Lond) 91: 223226.
  27. Alam MJ, Zurek L, , 2004. Association of Escherichia coli O157: H7 with houseflies on a cattle farm. Appl Environ Microbiol 70: 75787580.
  28. Shane SM, Montrose MS, Harrington KS, , 1985. Transmission of Campylobacter jejuni by the housefly (Musca domestica). Avian Dis 29: 384391.
  29. Kobayashi M, Sasaki T, Agui N, , 2002. Possible food contamination with the excreta of housefly with enterohemorrhagic Escherichia coli O157: H7. Jap J Sanit Zool 53: 8387.
  30. Kobayashi M, Sasaki T, Saito N, Tamura K, Suzuki K, Watanabe H, Agui N, , 1999. Houseflies: not simple mechanical vectors of enterohemorrhagic Escherichia coli O157: H7. Am J Trop Med Hyg 61: 625629.
  31. Nayduch D, Pittman Noblet G, Stutzenberger F, , 2002. Vector potential of houseflies for the bacterium Aeromonas caviae. Med Vet Entomol 16: 193198.
  32. Sasaki T, Kobayashi M, Agui N, , 2000. Epidemiological potential of excretion and regurgitation by Musca domestica (Diptera: Muscidae) in the dissemination of Escherichia coli O157: H7 to food. J Med Entomol 37: 945949.
  33. Cohen D, Green M, Block C, Slepon R, Ambar R, Wasserman SS, Levine MM, , 1991. Reduction of transmission of shigellosis by control of houseflies (Musca domestica). Lancet 337: 993997.
  34. Fotedar R, , 2001. Vector potential of houseflies (Musca domestica) in the transmission of Vibrio cholerae in India. Acta Trop 78: 3134.
  35. Hald B, Skovgård H, Bang DD, Pedersen K, Dybdahl J, Jespersen JB, Madsen M, , 2004. Flies and Campylobacter infection of broiler flocks. Emerg Infect Dis 10: 14901492.
  36. Holt PS, Geden CJ, Moore RW, Gast RK, , 2007. Isolation of Salmonella enterica serovar Enteritidis from houseflies (Musca domestica) found in rooms containing Salmonella serovar Enteritidis-challenged hens. Appl Environ Microbiol 73: 60306035.
  37. Chavasse DC, Shier RP, Murphy OA, Huttly SRA, Cousens SN, Akhtar T, , 1999. Impact of fly control on childhood diarrhoea in Pakistan: community-randomised trial. Lancet 353: 2225.
  38. Fukushima H, Ito Y, Saito K, Tsubokura M, Otsuki K, , 1979. Role of the fly in the transport of Yersinia enterocolitica. Appl Environ Microbiol 38: 10091010.
  39. Lindeberg YL, Egedal K, Hossain ZZ, Phelps M, Tulsiani S, Farhana I, Begum A, Jensen PKM, , 2017. Can E. coli fly? The role of flies as transmitters of Escherichia coli to food in an urban slum in Bangladesh. Trop Med Int Health 23: 29.
  40. Arnold BF, Null C, Luby SP, Unicomb L, Stewart CP, Dewey KG, Ahmed T, Ashraf S, Christensen G, Clasen T, , 2013. Cluster-randomised controlled trials of individual and combined water, sanitation, hygiene and nutritional interventions in rural Bangladesh and Kenya: the WASH benefits study design and rationale. BMJ Open 3: e003476.
  41. Simon AK, Hollander GA, McMichael A, , 2015. Evolution of the immune system in humans from infancy to old age. Proc Biol Sci 282: 20143085.
  42. Guerrant RL, DeBoer MD, Moore SR, Scharf RJ, Lima AA, , 2013. The impoverished gut—a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol 10: 220229.
  43. Mashreky SR, Rahman A, Chowdhury S, Giashuddin S, Svanström L, Linnan M, Shafinaz S, Uhaa I, Rahman F, , 2008. Epidemiology of childhood burn: yield of largest community based injury survey in Bangladesh. Burns 34: 856862.
  44. Senior-White R, Aubertin D, Smart J, , 1940. The Fauna of British India, Including the Remainder of the Oriental Region: Diptera. Family Calliphoridae, Vol. 6. New Delhi, India: Today & Tomorrow’s Printers & Publisher.
  45. Van Emden FI, , 1965. The fauna of India and the adjacent countries. Diptera 7: 493541.
  46. Nandi BC, , 2002. The Fauna of India and the Adjacent Countries: Diptera. Sarcophagidae, Vol. 10. Calcutta, India: Zoological Survey of India.
  47. Gilbert R, De Louvois J, Donovan T, Little C, Nye K, Ribeiro C, Richards J, Roberts D, Bolton F, , 2000. Guidelines for the microbiological quality of some ready-to-eat foods sampled at the point of sale. PHLS Advisory Committee for Food and Dairy Products. Commun Dis Public Health 3: 163167.
  48. Mickey RM, Greenland S, , 1989. The impact of confounder selection criteria on effect estimation. Am J Epidemiol 129: 125137.
  49. Kusumaningrum H, Riboldi G, Hazeleger W, Beumer R, , 2003. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol 85: 227236.
  50. Joosten H, Lardeau A, , 2004. Enhanced microbiological safety of acidified infant formulas tested in vitro. South Afr J Clin Nutr 17: 8792.
  51. Isobe KO, Tarao M, Chiem NH, Minh LY, Takada H, , 2004. Effect of environmental factors on the relationship between concentrations of coprostanol and fecal indicator bacteria in tropical (Mekong Delta) and temperate (Tokyo) freshwaters. Appl Environ Microbiol 70: 814821.
  52. Rochelle-Newall E, Nguyen TMH, Le TPQ, Sengtaheuanghoung O, Ribolzi O, , 2015. A short review of fecal indicator bacteria in tropical aquatic ecosystems: knowledge gaps and future directions. Front Microbiol 6: 308.
  53. Lanata CF, , 2003. Studies of food hygiene and diarrhoeal disease. Int J Environ Health Res 13 (Suppl 1): S175S183.
  54. Kusumaningrum HD, van Asselt ED, Beumer RR, Zwietering MH, , 2004. A quantitative analysis of cross-contamination of Salmonella and Campylobacter spp. via domestic kitchen surfaces. J Food Prot 67: 18921903.
  55. Gorman R, Bloomfield S, Adley CC, , 2002. A study of cross-contamination of food-borne pathogens in the domestic kitchen in the Republic of Ireland. Int J Food Microbiol 76: 143150.
  56. Curtis V, Cairncross S, Yonli R, , 2000. Domestic hygiene and diarrhoea—pinpointing the problem. Trop Med Int Health 5: 2232.
  57. Pickering AJ, Julian TR, Marks SJ, Mattioli MC, Boehm AB, Schwab KJ, Davis J, , 2012. Fecal contamination and diarrheal pathogens on surfaces and in soils among Tanzanian households with and without improved sanitation. Environ Sci Technol 46: 57365743.
  58. Van Donsel DJ, Geldreich EE, Clarke NA, , 1967. Seasonal variations in survival of indicator bacteria in soil and their contribution to storm-water pollution. Appl Microbiol 15: 13621370.
  59. Mattick K, Durham K, Domingue G, Jorgensen F, Sen M, Schaffner DW, Humphrey T, , 2003. The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food. Int J Food Microbiol 85: 213226.
  60. Talukdar PK, Rahman M, Rahman M, Nabi A, Islam Z, Hoque MM, Endtz HP, Islam MA, , 2013. Antimicrobial resistance, virulence factors and genetic diversity of Escherichia coli isolates from household water supply in Dhaka, Bangladesh. PLoS One 8: e61090.
  61. Harris AR, Pickering AJ, Harris M, Doza S, Islam MS, Unicomb L, Luby S, Davis J, Boehm AB, , 2016. Ruminants contribute fecal contamination to the urban household environment in Dhaka, Bangladesh. Environ Sci Technol 50: 46424649.
  62. Lindsay DR, Stewart WH, Watt J, , 1953. Effect of fly control on diarrheal disease in an area of moderate morbidity. Public Health Rep 68: 361367.
  63. Rahman MJ, Nizame FA, Nuruzzaman M, Akand F, Islam MA, Parvez SM, Stewart CP, Unicomb L, Luby SP, Winch PJ, , 2016. Toward a scalable and sustainable intervention for complementary food safety. Food Nutr Bull 37: 186201.
  64. Touré O, Coulibaly S, Arby A, Maiga F, Cairncross S, , 2011. Improving microbiological food safety in peri-urban Mali; an experimental study. Food Control 22: 15651572.
  65. Parvez SM, Kwong L, Rahman MJ, Ercumen A, Pickering AJ, Ghosh PK, Rahman M, Das KK, Luby SP, Unicomb L, , 2017. Escherichia coli contamination of child complementary foods and association with domestic hygiene in rural Bangladesh. Trop Med Int Health 22: 547557.
  66. Halder AK, Tronchet C, Akhter S, Bhuiya A, Johnston R, Luby SP, , 2010. Observed hand cleanliness and other measures of handwashing behavior in rural Bangladesh. BMC Public Health 10: 545.
  67. Curtis VA, Danquah LO, Aunger RV, , 2009. Planned, motivated and habitual hygiene behaviour: an eleven country review. Health Educ Res 24: 655673.
  68. Freeman MC, Stocks ME, Cumming O, Jeandron A, Higgins J, Wolf J, Prüss-Ustün A, Bonjour S, Hunter PR, Fewtrell L, , 2014. Systematic review: hygiene and health: systematic review of handwashing practices worldwide and update of health effects. Trop Med Int Health 19: 906916.
  69. Ehiri JE, Azubuike MC, Ubbaonu CN, Anyanwu EC, Ibe KM, Ogbonna MO, , 2001. Critical control points of complementary food preparation and handling in eastern Nigeria. Bull World Health Organ 79: 423433.
  70. Gilman RH, Skillicorn P, , 1985. Boiling of drinking-water: can a fuel-scarce community afford it? Bull World Health Organ 63: 157.
  71. Geden CJ, , 2005. Methods for monitoring outdoor populations of house flies, Musca domestica L. (Diptera: Muscidae). J Vector Ecol 30: 244.
  72. Geden CJ, Szumlas DE, Walker TW, , 2009. Evaluation of commercial and field-expedient baited traps for house flies, Musca domestica L. (Diptera: Muscidae). J Vector Ecol 34: 99103.
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  • Received : 25 May 2017
  • Accepted : 20 Dec 2017

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