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.


Article metrics loading...

Loading full text...

Full text loading...



  1. Fayer R, Morgan U, Upton SJ, , 2000. Epidemiology of Cryptosporidium: transmission, detection and identification. Int J Parasitol 30: 13051322.[Crossref]
  2. Tzipori S, Ward H, , 2002. Cryptosporidiosis: biology, pathogenesis and disease. Microbes Infect 4: 10471058.[Crossref]
  3. Dillingham RA, Lima AA, Guerrant RL, , 2002. Cryptosporidiosis: epidemiology and impact. Microbes Infect 4: 10591066.[Crossref]
  4. Kosek M, Alcantara C, Lima AA, Guerrant RL, , 2001. Cryptosporidiosis: an update. Lancet Infect Dis 1: 262269.[Crossref]
  5. Desai NT, Sarkar R, Kang G, , 2012. Cryptosporidiosis: an under-recognized public health problem. Trop Parasitol 2: 9198.[Crossref]
  6. Leav BA, Mackay M, Ward HD, , 2003. Cryptosporidium species: new insights and old challenges. Clin Infect Dis 36: 903908.[Crossref]
  7. Shirley DA, Moonah SN, Kotloff KL, , 2012. Burden of disease from cryptosporidiosis. Curr Opin Infect Dis 25: 555563.[Crossref]
  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.
  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]
  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.
  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]
  12. Collinet-Adler S, Ward HD, , 2010. Cryptosporidiosis: environmental, therapeutic, and preventive challenges. Eur J Clin Microbiol Infect Dis 29: 927935.[Crossref]
  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.
  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]
  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.
  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]
  17. Bhattacharya MK, Teka T, Faruque AS, Fuchs GJ, , 1997. Cryptosporidium infection in children in urban Bangladesh. J Trop Pediatr 43: 282286.[Crossref]
  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.
  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]
  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.
  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.
  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.
  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]
  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.
  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]
  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]
  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]
  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.
  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]
  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]
  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]
  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]
  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]
  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]
  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]
  36. WHO, 1995. The Treatment of Diarrhea: A Manual for Physicians and Other Senior Health Workers. Geneva: World Health Organization.
  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.
  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.
  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]
  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]
  41. Greenland S, Drescher K, , 1993. Maximum likelihood estimation of the attributable fraction from logistic models. Biometrics 49: 865872.[Crossref]
  42. Gordis L, , 2004. Epidemiology. Philadelphia, PA: Elsevier Saunders.
  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]
  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]
  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.
  46. Macfarlane DE, Horner-Bryce J, , 1987. Cryptosporidiosis in well-nourished and malnourished children. Acta Paediatr Scand 76: 474477.[Crossref]
  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.
  48. Mor SM, Tzipori S, , 2008. Cryptosporidiosis in children in sub-Saharan Africa: a lingering challenge. Clin Infect Dis 47: 915921.[Crossref]
  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]
  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]
  51. Rauh VA, Wasserman GA, Brunelli SA, , 1990. Determinants of maternal child-rearing attitudes. J Am Acad Child Adolesc Psychiatry 29: 375381.[Crossref]
  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]
  53. Chalmers RM, Giles M, , 2010. Zoonotic cryptosporidiosis in the UK: challenges for control. J Appl Microbiol 109: 14871497.[Crossref]
  54. Hunter PR, Thompson RC, , 2005. The zoonotic transmission of Giardia and Cryptosporidium . Int J Parasitol 35: 11811190.[Crossref]
  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]

Data & Media loading...

  • Received : 16 May 2014
  • Accepted : 01 Jul 2014

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error