Volume 91, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



The risk factors for acquisition of cryptosporidial infection in resource-poor settings are poorly understood. A nested case-control study was conducted to assess factors associated with childhood cryptosporidiosis (detected by stool polymerase chain reaction) in an endemic, Indian slum community using data from two community-based studies with 580 children followed prospectively until their second birthday. Factors were assessed for overall cryptosporidiosis ( = 406), and for multiple ( = 208), asymptomatic ( = 243), and symptomatic ( = 163) infections, respectively. Presence of older siblings (odds ratio [OR] = 1.88, = 0.002) and stunting at 6 months of age (OR = 1.74, = 0.019) were important risk factors for childhood cryptosporidiosis. Always boiling drinking water before consumption, the use of a toilet by all members of the family, and maternal age ≥ 23 years were protective. These results provide insights into acquisition of childhood cryptosporidiosis in settings with poor environmental sanitation, contaminated public water supply systems, and close human–animal contact. Disease control strategies will require a multifaceted approach.


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  1. Fayer R, Morgan U, Upton SJ, , 2000. Epidemiology of Cryptosporidium: transmission, detection and identification. Int J Parasitol 30: 13051322.[Crossref] [Google Scholar]
  2. Tzipori S, Ward H, , 2002. Cryptosporidiosis: biology, pathogenesis and disease. Microbes Infect 4: 10471058.[Crossref] [Google Scholar]
  3. Dillingham RA, Lima AA, Guerrant RL, , 2002. Cryptosporidiosis: epidemiology and impact. Microbes Infect 4: 10591066.[Crossref] [Google Scholar]
  4. Kosek M, Alcantara C, Lima AA, Guerrant RL, , 2001. Cryptosporidiosis: an update. Lancet Infect Dis 1: 262269.[Crossref] [Google Scholar]
  5. Desai NT, Sarkar R, Kang G, , 2012. Cryptosporidiosis: an under-recognized public health problem. Trop Parasitol 2: 9198.[Crossref] [Google Scholar]
  6. Leav BA, Mackay M, Ward HD, , 2003. Cryptosporidium species: new insights and old challenges. Clin Infect Dis 36: 903908.[Crossref] [Google Scholar]
  7. Shirley DA, Moonah SN, Kotloff KL, , 2012. Burden of disease from cryptosporidiosis. Curr Opin Infect Dis 25: 555563.[Crossref] [Google Scholar]
  8. Snelling WJ, Xiao L, Ortega-Pierres G, Lowery CJ, Moore JE, Rao JR, Smyth S, Millar BC, Rooney PJ, Matsuda M, Kenny F, Xu J, Dooley JS, , 2007. Cryptosporidiosis in developing countries. J Infect Dev Ctries 1: 242256. [Google Scholar]
  9. Checkley W, Epstein LD, Gilman RH, Black RE, Cabrera L, Sterling CR, , 1998. Effects of Cryptosporidium parvum infection in Peruvian children: growth faltering and subsequent catch-up growth. Am J Epidemiol 148: 497506.[Crossref] [Google Scholar]
  10. Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL, , 1999. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am J Trop Med Hyg 61: 707713. [Google Scholar]
  11. Molbak K, Hojlyng N, Gottschau A, Sa JC, Ingholt L, da Silva AP, Aaby P, , 1993. Cryptosporidiosis in infancy and childhood mortality in Guinea Bissau, West Africa. BMJ 307: 417420.[Crossref] [Google Scholar]
  12. Collinet-Adler S, Ward HD, , 2010. Cryptosporidiosis: environmental, therapeutic, and preventive challenges. Eur J Clin Microbiol Infect Dis 29: 927935.[Crossref] [Google Scholar]
  13. Cruz JR, Cano F, Caceres P, Chew F, Pareja G, , 1988. Infection and diarrhea caused by Cryptosporidium sp. among Guatemalan infants. J Clin Microbiol 26: 8891. [Google Scholar]
  14. Molbak K, Aaby P, Hojlyng N, da Silva AP, , 1994. Risk factors for Cryptosporidium diarrhea in early childhood: a case-control study from Guinea-Bissau, West Africa. Am J Epidemiol 139: 734740.[Crossref] [Google Scholar]
  15. Javier Enriquez F, Avila CR, Ignacio Santos J, Tanaka-Kido J, Vallejo O, Sterling CR, , 1997. Cryptosporidium infections in Mexican children: clinical, nutritional, enteropathogenic, and diagnostic evaluations. Am J Trop Med Hyg 56: 254257. [Google Scholar]
  16. Newman RD, Sears CL, Moore SR, Nataro JP, Wuhib T, Agnew DA, Guerrant RL, Lima AA, , 1999. Longitudinal study of Cryptosporidium infection in children in northeastern Brazil. J Infect Dis 180: 167175.[Crossref] [Google Scholar]
  17. Bhattacharya MK, Teka T, Faruque AS, Fuchs GJ, , 1997. Cryptosporidium infection in children in urban Bangladesh. J Trop Pediatr 43: 282286.[Crossref] [Google Scholar]
  18. Katsumata T, Hosea D, Wasito EB, Kohno S, Hara K, Soeparto P, Ranuh IG, , 1998. Cryptosporidiosis in Indonesia: a hospital-based study and a community-based survey. Am J Trop Med Hyg 59: 628632. [Google Scholar]
  19. Bern C, Ortega Y, Checkley W, Roberts JM, Lescano AG, Cabrera L, Verastegui M, Black RE, Sterling C, Gilman RH, , 2002. Epidemiologic differences between cyclosporiasis and cryptosporidiosis in Peruvian children. Emerg Infect Dis 8: 581585.[Crossref] [Google Scholar]
  20. Nchito M, Kelly P, Sianongo S, Luo NP, Feldman R, Farthing M, Baboo KS, , 1998. Cryptosporidiosis in urban Zambian children: an analysis of risk factors. Am J Trop Med Hyg 59: 435437. [Google Scholar]
  21. Leach CT, Koo FC, Kuhls TL, Hilsenbeck SG, Jenson HB, , 2000. Prevalence of Cryptosporidium parvum infection in children along the Texas-Mexico border and associated risk factors. Am J Trop Med Hyg 62: 656661. [Google Scholar]
  22. Pereira MD, Atwill ER, Barbosa AP, Silva SA, Garcia-Zapata MT, , 2002. Intra-familial and extra-familial risk factors associated with Cryptosporidium parvum infection among children hospitalized for diarrhea in Goiania, Goias, Brazil. Am J Trop Med Hyg 66: 787793. [Google Scholar]
  23. Roy SL, DeLong SM, Stenzel SA, Shiferaw B, Roberts JM, Khalakdina A, Marcus R, Segler SD, Shah DD, Thomas S, Vugia DJ, Zansky SM, Dietz V, Beach MJ, , 2004. Risk factors for sporadic cryptosporidiosis among immunocompetent persons in the United States from 1999 to 2001. J Clin Microbiol 42: 29442951.[Crossref] [Google Scholar]
  24. Solorzano-Santos F, Penagos-Paniagua M, Meneses-Esquivel R, Miranda-Novales MG, Leanos-Miranda B, Angulo-Gonzalez D, Fajardo-Gutierrez A, , 2000. Cryptosporidium parvum infection in malnourished and non-malnourished children without diarrhea in a Mexican rural population. Rev Invest Clin 52: 625631. [Google Scholar]
  25. Lake IR, Harrison FC, Chalmers RM, Bentham G, Nichols G, Hunter PR, Kovats RS, Grundy C, , 2007. Case-control study of environmental and social factors influencing cryptosporidiosis. Eur J Epidemiol 22: 805811.[Crossref] [Google Scholar]
  26. Hunter PR, Hughes S, Woodhouse S, Syed Q, Verlander NQ, Chalmers RM, Morgan K, Nichols G, Beeching N, Osborn K, , 2004. Sporadic cryptosporidiosis case-control study with genotyping. Emerg Infect Dis 10: 12411249.[Crossref] [Google Scholar]
  27. Al-Mekhlafi HM, Mahdy MA, Azlin MY, Fatmah MS, Norhayati M, , 2011. Childhood Cryptosporidium infection among aboriginal communities in Peninsular Malaysia. Ann Trop Med Parasitol 105: 135143.[Crossref] [Google Scholar]
  28. Khalili B, Mardani M, , 2009. Frequency of Cryptosporidium and risk factors related to cryptosporidiosis in under-5 year old hospitalized children due to diarrhea. Iranian Journal of Clinical Infectious Diseases 4: 151155. [Google Scholar]
  29. Molloy SF, Tanner CJ, Kirwan P, Asaolu SO, Smith HV, Nichols RA, Connelly L, Holland CV, , 2011. Sporadic Cryptosporidium infection in Nigerian children: risk factors with species identification. Epidemiol Infect 139: 946954.[Crossref] [Google Scholar]
  30. Chacin-Bonilla L, Barrios F, Sanchez Y, , 2008. Environmental risk factors for Cryptosporidium infection in an island from western Venezuela. Mem Inst Oswaldo Cruz 103: 4549.[Crossref] [Google Scholar]
  31. Ajjampur SS, Gladstone BP, Selvapandian D, Muliyil JP, Ward H, Kang G, , 2007. Molecular and spatial epidemiology of cryptosporidiosis in children in a semiurban community in south India. J Clin Microbiol 45: 915920.[Crossref] [Google Scholar]
  32. Ajjampur SS, Sarkar R, Sankaran P, Kannan A, Menon VK, Muliyil J, Ward H, Kang G, , 2010. Symptomatic and asymptomatic Cryptosporidium infections in children in a semi-urban slum community in southern India. Am J Trop Med Hyg 83: 11101115.[Crossref] [Google Scholar]
  33. Sarkar R, Sivarathinaswamy P, Thangaraj B, Sindhu KN, Ajjampur SS, Muliyil J, Balraj V, Naumova EN, Ward H, Kang G, , 2013. Burden of childhood diseases and malnutrition in a semi-urban slum in southern India. BMC Public Health 13: 87.[Crossref] [Google Scholar]
  34. Sarkar R, Ajjampur SS, Prabakaran AD, Geetha JC, Sowmyanarayanan TV, Kane A, Duara J, Muliyil J, Balraj V, Naumova EN, Ward H, Kang G, , 2013. Cryptosporidiosis among children in an endemic semiurban community in southern India: does a protected drinking water source decrease infection? Clin Infect Dis 57: 398406.[Crossref] [Google Scholar]
  35. Kattula D, Sarkar R, Sivarathinaswamy P, Velusamy V, Venugopal S, Naumova EN, Muliyil J, Ward H, Kang G, , 2014. The first 1000 days of life: prenatal and postnatal risk factors for morbidity and growth in a birth cohort in southern India. BMJ Open 4: e005404. doi:10.1136/bmjopen-2014-005404.[Crossref] [Google Scholar]
  36. WHO, 1995. The Treatment of Diarrhea: A Manual for Physicians and Other Senior Health Workers. Geneva: World Health Organization. [Google Scholar]
  37. Xiao L, Escalante L, Yang C, Sulaiman I, Escalante AA, Montali RJ, Fayer R, Lal AA, , 1999. Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65: 15781583. [Google Scholar]
  38. WHO, 2006. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Geneva: World Health Organization. [Google Scholar]
  39. Brick T, Primrose B, Chandrasekhar R, Roy S, Muliyil J, Kang G, , 2004. Water contamination in urban south India: household storage practices and their implications for water safety and enteric infections. Int J Hyg Environ Health 207: 473480.[Crossref] [Google Scholar]
  40. Gladstone BP, Muliyil JP, Jaffar S, Wheeler JG, Le Fevre A, Iturriza-Gomara M, Gray JJ, Bose A, Estes MK, Brown DW, Kang G, , 2008. Infant morbidity in an Indian slum birth cohort. Arch Dis Child 93: 479484.[Crossref] [Google Scholar]
  41. Greenland S, Drescher K, , 1993. Maximum likelihood estimation of the attributable fraction from logistic models. Biometrics 49: 865872.[Crossref] [Google Scholar]
  42. Gordis L, , 2004. Epidemiology. Philadelphia, PA: Elsevier Saunders. [Google Scholar]
  43. Osewe P, Addiss DG, Blair KA, Hightower A, Kamb ML, Davis JP, , 1996. Cryptosporidiosis in Wisconsin: a case-control study of post-outbreak transmission. Epidemiol Infect 117: 297304.[Crossref] [Google Scholar]
  44. Bushen OY, Kohli A, Pinkerton RC, Dupnik K, Newman RD, Sears CL, Fayer R, Lima AA, Guerrant RL, , 2007. Heavy cryptosporidial infections in children in northeast Brazil: comparison of Cryptosporidium hominis and Cryptosporidium parvum . Trans R Soc Trop Med Hyg 101: 378384.[Crossref] [Google Scholar]
  45. Molbak K, Andersen M, Aaby P, Hojlyng N, Jakobsen M, Sodemann M, da Silva AP, , 1997. Cryptosporidium infection in infancy as a cause of malnutrition: a community study from Guinea-Bissau, West Africa. Am J Clin Nutr 65: 149152. [Google Scholar]
  46. Macfarlane DE, Horner-Bryce J, , 1987. Cryptosporidiosis in well-nourished and malnourished children. Acta Paediatr Scand 76: 474477.[Crossref] [Google Scholar]
  47. Sallon S, Deckelbaum RJ, Schmid II, Harlap S, Baras M, Spira DT, , 1988. Cryptosporidium, malnutrition, and chronic diarrhea in children. Am J Dis Child 142: 312315. [Google Scholar]
  48. Mor SM, Tzipori S, , 2008. Cryptosporidiosis in children in sub-Saharan Africa: a lingering challenge. Clin Infect Dis 47: 915921.[Crossref] [Google Scholar]
  49. Masangwi SJ, Ferguson NS, Grimason AM, Morse TD, Zawdie G, Kazembe LN, , 2010. Household and community variations and nested risk factors for diarrhea prevalence in southern Malawi: a binary logistic multi-level analysis. Int J Environ Health Res 20: 141158.[Crossref] [Google Scholar]
  50. Fraser D, Dagan R, Porat N, el-On J, Alkrinawi S, Deckelbaum RJ, Naggan L, , 1998. Persistent diarrhea in a cohort of Israeli Bedouin infants: role of enteric pathogens and family and environmental factors. J Infect Dis 178: 10811088.[Crossref] [Google Scholar]
  51. Rauh VA, Wasserman GA, Brunelli SA, , 1990. Determinants of maternal child-rearing attitudes. J Am Acad Child Adolesc Psychiatry 29: 375381.[Crossref] [Google Scholar]
  52. Gualberto FA, Heller L, , 2006. Endemic Cryptosporidium infection and drinking water source: a systematic review and meta-analyses. Water Sci Technol 54: 231238.[Crossref] [Google Scholar]
  53. Chalmers RM, Giles M, , 2010. Zoonotic cryptosporidiosis in the UK: challenges for control. J Appl Microbiol 109: 14871497.[Crossref] [Google Scholar]
  54. Hunter PR, Thompson RC, , 2005. The zoonotic transmission of Giardia and Cryptosporidium . Int J Parasitol 35: 11811190.[Crossref] [Google Scholar]
  55. Nundy S, Gilman RH, Xiao L, Cabrera L, Cama R, Ortega YR, Kahn G, Cama VA, , 2011. Wealth and its associations with enteric parasitic infections in a low-income community in Peru: use of principal component analysis. Am J Trop Med Hyg 84: 3842.[Crossref] [Google Scholar]

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  • Received : 16 May 2014
  • Accepted : 01 Jul 2014
  • Published online : 03 Dec 2014

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