Environmental factors associated with high fly densities and Diarrhea in Vellore, India

Applied and Environmental Microbiology

Volumn 81, Issue 17, 2015, Pages 6053-6058

  Collinet Adler, Stefan ^a   Babji, Sudhir ^b   Francis, Mark ^b   Kattula, Deepthi ^b   Premkumar, Prasanna Samuel ^b   Sarkar, Rajiv ^b   Mohan, Venkat Ragava ^b   Ward, Honorine ^a,b   Kang, Gagandeep ^b   Balraj, Vinohar ^b   Naumova, Elena N ^b,c  

^a TUFTS MEDICAL CENTER   (United States)

^b CHRISTIAN MEDICAL COLLEGE   (India)

^c TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; PROTOZOA; REGRESSION ANALYSIS; SURVEYS; URBAN GROWTH; VIRUSES;

CONFIDENCE INTERVAL; ENTERIC PATHOGENS; ENVIRONMENTAL FACTORS; FOODBORNE INFECTIONS; HUMAN-ANIMAL INTERACTIONS; LIVING CONDITIONS; RURAL HOUSEHOLDS; WET AND DRY SEASONS;

PATHOGENS;

ABUNDANCE; CHILD HEALTH; DIARRHEAL DISEASE; DISEASE VECTOR; ENVIRONMENTAL FACTOR; FLY; HEALTH RISK; HOST-PATHOGEN INTERACTION; POPULATION DENSITY; RURAL POPULATION; SEASONAL VARIATION;

INDIA; TAMIL NADU; VELLORE;

ANIMALIA; CRYPTOSPORIDIUM; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GIARDIA; NOROVIRUS; PROTOZOA; ROTAVIRUS; SALMONELLA; SHIGELLA; VIBRIO;

ANIMAL; BACTERIUM; CLASSIFICATION; DIARRHEA; DIPTERA; ENVIRONMENT; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; INDIA; INFANT; INSECT VECTOR; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; NEWBORN; PARASITOLOGY; POPULATION DENSITY; PRESCHOOL CHILD; SEASON; VIROLOGY; VIRUS;

ANIMALS; BACTERIA; CHILD, PRESCHOOL; DIARRHEA; DIPTERA; ENVIRONMENT; FEMALE; HUMANS; INDIA; INFANT; INFANT, NEWBORN; INSECT VECTORS; MALE; POPULATION DENSITY; SEASONS; VIRUSES;

EID: 84938785530     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01236-15     Document Type: Article

References (45)

1. Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, Cousens S, Mathers C, Black RE. 2015. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 385:430-440. http://dx.doi.org/10.1016/S0140-6736(14)61698-6.
2. Collinet-Adler S, Ward HD. 2010. Cryptosporidiosis: environmental, therapeutic, and preventive challenges. Eur J Clin Microbiol Infect Dis 29:927-935. http://dx.doi.org/10.1007/s10096-010-0960-9.
3. Graczyk TK, Grimes BH, Knight R, Da Silva AJ, Pieniazek NJ, Veal DA. 2003. Detection of Cryptosporidium parvum and Giardia lamblia carried by synanthropic flies by combined fluorescent in situ hybridization and a monoclonal antibody. Am J Trop Med Hyg 68:228-232.
4. Graczyk TK, Knight R, Gilman RH, Cranfield MR. 2001. The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 3:231-235. http://dx.doi.org/10.1016/S1286-4579(01)01371-5.
5. 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 113:435-444. http://dx.doi.org/10.1017/S0950268800068448.
6. Rosef O, Kapperud G. 1983. House flies (Musca domestica) as possible vectors of Campylobacter fetus subsp. jejuni. Appl Environ Microbiol 45:381-383.
7. Nmorsi OP, Agbozele G, Ukwandu NC. 2007. Some aspects of epidemiology of filth flies: Musca domestica, Musca domestica vicina, Drosophila melanogaster and associated bacteria pathogens in Ekpoma, Nigeria. Vector Borne Zoonotic Dis 7:107-117. http://dx.doi.org/10.1089/vbz.2006.0539.
8. Butler JF, Garcia-Maruniak A, Meek F, Maruniak JE. 2010. Wild Florida house flies (Musca domestica) as carriers of pathogenic bacteria. Fla Entomol 93:218-223. http://dx.doi.org/10.1653/024.093.0211.
9. 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 46:32-36.
10. Levine OS, Levine MM. 1991. Houseflies (Musca domestica) as mechanical vectors of shigellosis. Rev Infect Dis 13:688-696. http://dx.doi.org/10.1093/clinids/13.4.688.
11. De Jesus 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 93:259-262. http://dx.doi.org/10.1016/j.ijfoodmicro.2003.12.003.
12. 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 61:625-629.
13. 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 37:945-949. http://dx.doi.org/10.1603/0022-2585-37.6.945.
14. Graczyk TK, Cranfield MR, Fayer R, Bixler H. 1999. House flies (Musca domestica) as transport hosts of Cryptosporidium parvum. Am J Trop Med Hyg 61:500-504.
15. Graczyk TK, Fayer R, Cranfield MR, Mhangami-Ruwende B, Knight R, Trout JM, Bixler H. 1999. Filth flies are transport hosts of Cryptosporidium parvum. Emerg Infect Dis 5:726-727. http://dx.doi.org/10.3201/eid0505.990520.
16. Graczyk TK, Grimes BH, Knight R, Szostakowska B, Kruminis-Lozowska W, Racewicz M, Tamang L, Dasilva AJ, Myjak P. 2004. Mechanical transmission of Cryptosporidium parvum oocysts by flies. Wiad Parazytol 50:243-247.
17. Tan SW, Yap KL, Lee HL. 1997. Mechanical transport of rotavirus by the legs and wings of Musca domestica (Diptera: Muscidae). J Med Entomol 34:527-531. http://dx.doi.org/10.1093/jmedent/34.5.527.
18. Graczyk TK, Fayer R, Knight R, Mhangami-Ruwende B, Trout JM, Da Silva AJ, Pieniazek NJ. 2000. Mechanical transport and transmission of Cryptosporidium parvum oocysts by wild filth flies. Am J Trop Med Hyg 63:178-183.
19. Motarjemi Y, Kaferstein F, Moy G, Quevedo F. 1993. Contaminated weaning food: a major risk factor for diarrhoea and associated malnutrition. Bull World Health Organ 71:79-92.
20. Bidawid SP, Edeson JF, Ibrahim J, Matossian RM. 1978. The role of non-biting flies in the transmission of enteric pathogens (Salmonella species and Shigella species) in Beirut, Lebanon. Ann Trop Med Parasitol 72:117-121.
21. Chavasse DC, Shier RP, Murphy OA, Huttly SR, Cousens SN, Akhtar T. 1999. Impact of fly control on childhood diarrhoea in Pakistan: community-randomised trial. Lancet 353:22-25. http://dx.doi.org/10.1016/S0140-6736(98)03366-2.
22. 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 337:993-997. http://dx.doi.org/10.1016/0140-6736(91)92657-N.
23. Lindsay DR, Stewart WH, Watt J. 1953. Effect of fly control on diarrheal disease in an area of moderate morbidity. Public Health Rep 68:361-367. http://dx.doi.org/10.2307/4588424.
24. Sukontason K, Bunchoo M, Khantawa B, Piangjai S, Sukontason K, Methanitikorn R, Rongsriyam Y. 2000. Mechanical carrier of bacterial enteric pathogens by Chrysomya megacephala (Diptera: Calliphoridae) in Chiang Mai, Thailand. Southeast Asian J Trop Med Public Health 31(Suppl 1):S157-S161.
25. Sukontason K, Bunchoo M, Khantawa B, Sukontason K, Piangjai S, Choochote W. 2000. Musca domestica as a mechanical carrier of bacteria in Chiang Mai, north Thailand. J Vector Ecol 25:114-117.
26. Sukontason KL, Bunchoo M, Khantawa B, Piangjai S, Rongsriyam Y, Sukontason K. 2007. Comparison between Musca domestica and Chrysomya megacephala as carriers of bacteria in northern Thailand. Southeast Asian J Trop Med Public Health 38:38-44.
27. Szostakowska B, Kruminis-Lozowska W, Racewicz M, Knight R, Tamang L, Myjak P, Graczyk TK. 2004. Cryptosporidium parvum and Giardia lamblia recovered from flies on a cattle farm and in a landfill. Appl Environ Microbiol 70:3742-3744. http://dx.doi.org/10.1128/AEM.70.6.3742-3744.2004.
28. Watt J, Lindsay DR. 1948. Diarrheal disease control studies; effect of fly control in a high morbidity area. Public Health Rep 63:1319-1333. http://dx.doi.org/10.2307/4586723.
29. 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 73:6030-6035. http://dx.doi.org/10.1128/AEM.00803-07.
30. Farag TH, Faruque AS, Wu Y, Das SK, Hossain A, Ahmed S, Ahmed D, Nasrin D, Kotloff KL, Panchilangam S, Nataro JP, Cohen D, Blackwelder WC, Levine MM. 2013. Housefly population density correlates with shigellosis among children in Mirzapur, Bangladesh: a time series analysis. PLoS Negl Trop Dis 7:e2280. http://dx.doi.org/10.1371/journal.pntd.0002280.
31. Kattula D, Francis MR, Kulinkina A, Sarkar R, Mohan VR, Babji S, Ward HD, Kang G, Balraj V, Naumova EN. 18 February 2015. Environmental drivers of diarrheal infection in rural and urban communities in southern India in children and adults. Epidemiol Infect http://dx.doi.org/10.1017/S0950268814003562.
32. Ajjampur SS, Rajendran P, Ramani S, Banerjee I, Monica B, Sankaran P, Rosario V, Arumugam R, Sarkar R, Ward H, Kang G. 2008. Closing the diarrhoea diagnostic gap in Indian children by the application of molecular techniques. J Med Microbiol 57:1364-1368. http://dx.doi.org/10.1099/jmm.0.2008/003319-0.
33. Borror DJ, DeLong DM. 1964. An introduction to the study of insects. Holt, Rinehart, and Winston, Austin, TX.
34. Gomez-Duarte OG, Bai J, Newell E. 2009. Detection of Escherichia coli, Salmonella spp., Shigella spp., Yersinia enterocolitica, Vibrio cholerae, and Campylobacter spp. enteropathogens by 3-reaction multiplex polymerase chain reaction. Diagn Microbiol Infect Dis 63:1-9. http://dx.doi.org/10.1016/j.diagmicrobio.2008.09.006.
35. Girish R, Broor S, Dar L, Ghosh D. 2002. Foodborne outbreak caused by a Norwalk-like virus in India. J Med Virol 67:603-607. http://dx.doi.org/10.1002/jmv.10145.
36. Iturriza Gomara M, Wong C, Blome S, Desselberger U, Gray J. 2002. Molecular characterization of VP6 genes of human rotavirus isolates: correlation of genogroups with subgroups and evidence of independent segregation. J Virol 76:6596-6601. http://dx.doi.org/10.1128/JVI.76.13.6596-6601.2002.
37. Nguyen TV, Le Van P, Le Huy C, Gia KN, Weintraub A. 2005. Detection and characterization of diarrheagenic Escherichia coli from young children in Hanoi, Vietnam. J Clin Microbiol 43:755-760. http://dx.doi.org/10.1128/JCM.43.2.755-760.2005.
38. Xiao L, Morgan UM, Limor J, Escalante A, Arrowood M, Shulaw W, Thompson RC, Fayer R, Lal AA. 1999. Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Appl Environ Microbiol 65:3386-3391.
39. Greenberg B. 1964. Experimental transmission of Salmonella Typhimurium by houseflies to man. Am J Hyg (Lond) 80:149-156.
40. Greenberg B. 1973. Flies and disease. Vol II. Biology and disease transmission. Princeton University Press, Princeton, NJ.
41. Khin Nwe O, Sebastian AA, Aye T. 1989. Carriage of enteric bacterial pathogens by house flies in Yangon, Myanmar. J Diarrhoeal Dis Res 7:81-84.
42. Levine MM, Cohen D, Green M, Levine OS, Mintz ED. 1999. Fly control and shigellosis. Lancet 353:1020.
43. Manun'ebo MN, Haggerty PA, Kalengaie M, Ashworth A, Kirkwood BR. 1994. Influence of demographic, socioeconomic and environmental variables on childhood diarrhoea in a rural area of Zaire. J Trop Med Hyg 97:31-38.
44. Hashizume M, Wagatsuma Y, Faruque AS, Hayashi T, Hunter PR, Armstrong B, Sack DA. 2008. Factors determining vulnerability to diarrhoea during and after severe floods in Bangladesh. J Water Health 6:323-332. http://dx.doi.org/10.2166/wh.2008.062.
45. U KM, Khin M, Wai NN, Hman NW, Myint TT, Butler T. 1992. Risk factors for the development of persistent diarrhoea and malnutrition in Burmese children. Int J Epidemiol 21:1021-1029. http://dx.doi.org/10.1093/ije/21.5.1021.