Cryptosporidiosis in HIV/AIDS Patients in Kenya: Clinical Features, Epidemiology, Molecular Characterization and Antibody Responses

Jane W. Wanyiri Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Henry Kanyi Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Samuel Maina Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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David E. Wang Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Aaron Steen Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Paul Ngugi Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Timothy Kamau Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Tabitha Waithera Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Roberta O'Connor Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Kimani Gachuhi Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Claire N. Wamae Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Mkaya Mwamburi Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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Honorine D. Ward Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts; Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, Massachusetts; Center of Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya; Center of Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya; Kenyatta National Hospital, Nairobi, Kenya

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We investigated the epidemiological and clinical features of cryptosporidiosis, the molecular characteristics of infecting species and serum antibody responses to three Cryptosporidium-specific antigens in human immunodeficiency virus (HIV)/acquired immunodeficiency syndrome (AIDS) patients in Kenya. Cryptosporidium was the most prevalent enteric pathogen and was identified in 56 of 164 (34%) of HIV/AIDS patients, including 25 of 70 (36%) with diarrhea and 31 of 94 (33%) without diarrhea. Diarrhea in patients exclusively infected with Cryptosporidium was significantly associated with the number of children per household, contact with animals, and water treatment. Cryptosporidium hominis was the most prevalent species and the most prevalent subtype family was Ib. Patients without diarrhea had significantly higher serum IgG levels to Chgp15, Chgp40 and Cp23, and higher fecal IgA levels to Chgp15 and Chgp40 than those with diarrhea suggesting that antibody responses to these antigens may be associated with protection from diarrhea and supporting further investigation of these antigens as vaccine candidates.

Author Notes

* Address correspondence to Jane W. Wanyiri, Department of Medicine, Johns Hopkins University School of Medicine, CRB2 Bldg., Suite 1M.02, 1550 Orleans Street, Baltimore, MD 21287, E-mail: jwanyir1@jhmi.edu or Honorine D. Ward, Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Box 041, 800 Washington Street, Boston, MA 02111, E-mail: hward@tuftsmedicalcenter.org.

Financial support: This study was supported by the NIH Fogarty International Clinical Research Fellows Program (R24 TW007988) to JWW and in part by NIH R01 AI072222 and R01 AI52786 to HDW and the Tufts-Brown Center for AIDS Research 5P30AI042853.

Authors' addresses: Jane W. Wanyiri, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, E-mail: jwanyir1@jhmi.edu. Henry Kanyi, Eastern and Southern Africa Centre of International Parasite Control (ESACIPAC), Kenya Medical Research Institute, Nairobi, Kenya, E-mail: hkanyi@kemri.org. Samuel Maina, International Emerging Infections Program, KEMRI/CDC Research and Public Health Collaboration, Kisumu, Kenya, E-mail: Smaina@ke.cdc.gov. David E. Wang, Roberta O'Connor, and Honorine D. Ward, Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, MA, E-mails: d.wang@alumni.tufts.edu, Roconnor@tuftsmedicalcenter.org, and hward@tuftsmedicalcenter.org. Aaron Steen, Geisel School of Medicine at Dartmouth, White River Junction, VT, E-mail: Aaron.j.steen.dm@dartmouth.edu. Paul Ngugi, Comprehensive Care Center, Kenyatta National Hospital, Nairobi, Kenya, E-mail: ngugi.paul7@gmail.com. Timothy Kamau and Kimani Gachuhi, Center for Biotechnology, Research and Development, Kenya Medical Research Institute, Nairobi, Kenya, E-mails: Tkamau@kemri.org and Kgachuhi@kemri.org. Tabitha Waithera and Claire N. Wamae, Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya, E-mails: tiringu@kemri.org and nwamae@kemri.org. Mkaya Mwamburi, Department of Public Health and Community Medicine, Tufts University School of Medicine, Boston, MA, E-mail: Mkaya.Mwamburi@tufts.edu.

  • 1.

    O'Connor RM, Shaffie R, Kang G, Ward HD, 2011. Cryptosporidiosis in patients with HIV/AIDS. AIDS 25: 549560.

  • 2.

    Abubakar I, Aliyu SH, Arumugam C, Hunter PR, Usman NK, 2007. Prevention and treatment of cryptosporidiosis in immunocompromised patients. Cochrane Database Syst Rev CD004932.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Abubakar I, Aliyu SH, Arumugam C, Usman NK, Hunter PR, 2007. Treatment of cryptosporidiosis in immunocompromised individuals: systematic review and meta-analysis. Br J Clin Pharmacol 63: 387393.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    UNAIDS, 2012. The Kenya AIDS Epidemic, Update 2011. Geneva Joint Nations Programme on HIV/AIDS. Available at: http://www.unaids.org/en/dataanalysis/knowyourresponse/countryprogressreports/2012countries/ce_KE_Narrative_Report.pdf. Accessed October 24, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    NACC, 2009. Kenya Aids Indicator Survey 2007 (KAIS 2007) Final Report.

  • 6.

    Mwachari C, Batchelor BI, Paul J, Waiyaki PG, Gilks CF, 1998. Chronic diarrhea among HIV-infected adult patients in Nairobi, Kenya. J Infect 37: 4853.

  • 7.

    Mwachari CW, Meier AS, Muyodi J, Gatei W, Waiyaki P, Cohen CR, 2003. Chronic diarrhea in HIV-1-infected adults in Nairobi, Kenya: evaluation of risk factors and the WHO treatment algorithm. AIDS 17: 21242126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Batchelor BI, Kimari JN, Brindle RJ, 1996. Microbiology of HIV associated bacteremia and diarrhea in adults from Nairobi, Kenya. Epidemiol Infect 117: 139144.

  • 9.

    Estambale BB, Bwibo CR, Kang'ethe S, Chitayi PM, 1989. The occurrence of Cryptosporidium oocysts in fecal samples submitted for routine examination at Kenyatta National Hospital. East Afr Med J 66: 792795.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Gatei W, Wamae CN, Mbae C, Waruru A, Mulinge E, Waithera T, Gatika SM, Kamwati SK, Revathi G, Hart CA, 2006. Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in Kenya. Am J Trop Med Hyg 75: 7882.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Mirza NB, Bhatt KM, Bhatt SM, Kanja C, 1994. Cryptosporidiosis in HIV positive patients at Kenyatta National Hospital, Nairobi, Kenya. East Afr Med J 71: 334335.

  • 12.

    Borad A, Ward H, 2010. Human immune responses in cryptosporidiosis. Future Microbiol 5: 507519.

  • 13.

    Pozio E, Rezza G, Boschini A, Pezzotti P, Tamburrini A, Rossi P, Di Fine M, Smacchia C, Schiesari A, Gattei E, Zucconi R, Ballarini P, 1997. Clinical cryptosporidiosis and human immunodeficiency virus (HIV)-induced immunosuppression: findings from a longitudinal study of HIV-positive and HIV-negative former injection drug users. J Infect Dis 176: 969975.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Schmidt W, Wahnschaffe U, Schafer M, Zippel T, Arvand M, Meyerhans A, Riecken EO, Ullrich R, 2001. Rapid increase of mucosal CD4 T cells followed by clearance of intestinal cryptosporidiosis in an AIDS patient receiving highly active antiretroviral therapy. Gastroenterology 120: 984987.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Leitch GJ, He Q, 2012. Cryptosporidiosis-an overview. J Biomed Res 25: 116.

  • 16.

    Riggs MW, 2002. Recent advances in cryptosporidiosis: the immune response. Microbes Infect 4: 10671080.

  • 17.

    Chappell CL, Okhuysen PC, Sterling CR, Wang C, Jakubowski W, Dupont HL, 1999. Infectivity of Cryptosporidium parvum in healthy adults with pre-existing anti-C. parvum serum immunoglobulin G. Am J Trop Med Hyg 60: 157164.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Frost FJ, Muller T, Craun GF, Lockwood WB, Calderon RL, 2002. Serological evidence of endemic waterborne Cryptosporidium infections. Ann Epidemiol 12: 222227.

  • 19.

    Egorov A, Frost F, Muller T, Naumova E, Tereschenko A, Ford T, 2004. Serological evidence of Cryptosporidium infections in a Russian city and evaluation of risk factors for infections. Ann Epidemiol 14: 129136.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Moss DM, Chappell CL, Okhuysen PC, DuPont HL, Arrowood MJ, Hightower AW, Lammie PJ, 1998. The antibody response to 27-, 17-, and 15-kDa Cryptosporidium antigens following experimental infection in humans. J Infect Dis 178: 827833.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Wanyiri J, Ward H, 2006. Molecular basis of Cryptosporidium-host cell interactions: recent advances and future prospects. Future Microbiol 1: 201208.

  • 22.

    Frost FJ, Roberts M, Kunde TR, Craun G, Tollestrup K, Harter L, Muller T, 2005. How clean must our drinking water be: the importance of protective immunity. J Infect Dis 191: 809814.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Frost FJ, Tollestrup K, Craun GF, Fairley CK, Sinclair MI, Kunde TR, 2005. Protective immunity associated with a strong serological response to a Cryptosporidium-specific antigen group, in HIV-infected individuals. J Infect Dis 192: 618621.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Priest JW, Bern C, Roberts JM, Kwon JP, Lescano AG, Checkley W, Cabrera L, Moss DM, Arrowood MJ, Sterling CR, Gilman RH, Lammie PJ, 2005. Changes in serum immunoglobulin G levels as a marker for Cryptosporidium sp. infection in Peruvian children. J Clin Microbiol 43: 52985300.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Priest JW, Bern C, Xiao L, Roberts JM, Kwon JP, Lescano AG, Checkley W, Cabrera L, Moss DM, Arrowood MJ, Sterling CR, Gilman RH, Lammie PJ, 2006. Longitudinal analysis of Cryptosporidium species-specific immunoglobulin G antibody responses in Peruvian children. Clin Vaccine Immunol 13: 123131.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Wanyiri JW, Kanyi H, Maina S, Wang DE, Ngugi P, O'Connor R, Kamau T, Waithera T, Kimani G, Wamae CN, Mwamburi M, Ward HD, 2013. Infectious diarrhea in antiretroviral therapy-naive HIV/AIDS patients in Kenya. Trans R Soc Trop Med Hyg 107: 631638.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Vidal M, Kruger E, Duran C, Lagos R, Levine M, Prado V, Toro C, Vidal R, 2005. Single multiplex PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. J Clin Microbiol 43: 53625365.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Xiao L, 2010. Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124: 8089.

  • 30.

    Cohen S, Dalle F, Gallay A, Di Palma M, Bonnin A, Ward HD, 2006. Identification of Cpgp40/15 Type Ib as the predominant allele in isolates of Cryptosporidium spp. from a waterborne outbreak of gastroenteritis in South Burgundy, France. J Clin Microbiol 44: 589591.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Cevallos AM, Zhang X, Waldor MK, Jaison S, Zhou X, Tzipori S, Neutra MR, Ward HD, 2000. Molecular cloning and expression of a gene encoding Cryptosporidium parvum glycoproteins gp40 and gp15. Infect Immun 68: 41084116.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Preidis GA, Wang HC, Lewis DE, Castellanos-Gonzalez A, Rogers KA, Graviss EA, Ward HD, White AC Jr, 2007. Seropositive human subjects produce interferon gamma after stimulation with recombinant Cryptosporidium hominis gp15. Am J Trop Med Hyg 77: 583585.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Priest JW, Kwon JP, Moss DM, Roberts JM, Arrowood MJ, Dworkin MS, Juranek DD, Lammie PJ, 1999. Detection by enzyme immunoassay of serum immunoglobulin G antibodies that recognize specific Cryptosporidium parvum antigens. J Clin Microbiol 37: 13851392.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Ajjampur SS, Sarkar R, Allison G, Banda K, Kane A, Muliyil J, Naumova E, Ward H, Kang G, 2011. Serum IgG response to Cryptosporidium immunodominant antigen gp15 and polymorphic antigen gp40 in children with cryptosporidiosis in South India. Clin Vaccine Immunol 18: 633639.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Allison GM, Rogers KA, Borad A, Ahmed S, Karim MM, Kane AV, Hibberd PL, Naumova EN, Calderwood SB, Ryan ET, Khan WA, Ward HD, 2011. Antibody responses to the immunodominant Cryptosporidium gp15 antigen and gp15 polymorphisms in a case-control study of cryptosporidiosis in children in Bangladesh. Am J Trop Med Hyg 85: 97104.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Borad AJ, Allison GM, Wang D, Ahmed S, Karim MM, Kane AV, Moy J, Hibberd PL, Ajjampur SS, Kang G, Calderwood SB, Ryan ET, Naumova E, Khan WA, Ward HD, 2012. Systemic antibody responses to the immunodominant p23 antigen and p23 polymorphisms in children with cryptosporidiosis in Bangladesh. Am J Trop Med Hyg 86: 214222.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Qadri F, Jonson G, Begum YA, Wenneras C, Albert MJ, Salam MA, Svennerholm AM, 1997. Immune response to the mannose-sensitive hemagglutinin in patients with cholera due to Vibrio cholerae O1 and O0139. Clin Diagn Lab Immunol 4: 429434.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Ajjampur SS, Sankaran P, Kang G, 2008. Cryptosporidium species in HIV-infected individuals in India: an overview. Natl Med J India 21: 178184.

  • 39.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Gassama A, Sow PS, Fall F, Camara P, Gueye-N'diaye A, Seng R, Samb B, M'Boup S, Aidara-Kane A, 2001. Ordinary and opportunistic enteropathogens associated with diarrhea in Senegalese adults in relation to human immunodeficiency virus serostatus. Int J Infect Dis 5: 192198.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Houpt ER, Bushen OY, Sam NE, Kohli A, Asgharpour A, Ng CT, Calfee DP, Guerrant RL, Maro V, Ole-Nguyaine S, Shao JF, 2005. Short report: asymptomatic Cryptosporidium hominis infection among human immunodeficiency virus-infected patients in Tanzania. Am J Trop Med Hyg 73: 520522.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Samie A, Bessong PO, Obi CL, Sevilleja JE, Stroup S, Houpt E, Guerrant RL, 2006. Cryptosporidium species: preliminary descriptions of the prevalence and genotype distribution among school children and hospital patients in the Venda region, Limpopo Province, South Africa. Exp Parasitol 114: 314322.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Sarfati C, Bourgeois A, Menotti J, Liegeois F, Moyou-Somo R, Delaporte E, Derouin F, Ngole EM, Molina JM, 2006. Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus-infected adults in Cameroon: a cross-sectional study. Am J Trop Med Hyg 74: 162164.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Anand L, Dhanachand C, Brajachand N, 1998. Prevalence and epidemiologic characteristics of opportunistic and non-opportunistic intestinal parasitic infections in HIV positive patients in Manipur. J Commun Dis 30: 1922.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Chhin S, Harwell JI, Bell JD, Rozycki G, Ellman T, Barnett JM, Ward H, Reinert SE, Pugatch D, 2006. Etiology of chronic diarrhea in antiretroviral-naive patients with HIV infection admitted to Norodom Sihanouk Hospital, Phnom Penh, Cambodia. Clin Infect Dis 43: 925932.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Wanke CA, Cohan D, Thummakul T, Jongwuitiwes S, Grayson ML, Hammer SM, Hanvanich M, 1999. Diarrheal disease in patients infected with human immunodeficiency virus in Bangkok, Thailand. Am J Trop Med Hyg 60: 871874.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Haque R, Mondal D, Karim A, Molla IH, Rahim A, Faruque AS, Ahmad N, Kirkpatrick BD, Houpt E, Snider C, Petri WA Jr, 2009. Prospective case-control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Clin Infect Dis 48: 11911197.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    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, Emerging Infections Program FoodNet Working Group, 2004. Risk factors for sporadic cryptosporidiosis among immunocompetent persons in the United States from 1999 to 2001. J Clin Microbiol 42: 29442951.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Cox MJ, Elwin K, Massad E, Azevedo RS, 2005. Age-specific seroprevalence to an immunodominant Cryptosporidium sporozoite antigen in a Brazilian population. Epidemiol Infect 133: 951956.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Putignani L, Menichella D, 2010. Global distribution, public health and clinical impact of the protozoan pathogen Cryptosporidium. Interdiscip Perspect Infect Dis 2010: 170.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Cama VA, Ross JM, Crawford S, Kawai V, Chavez-Valdez R, Vargas D, Vivar A, Ticona E, Navincopa M, Williamson J, Ortega Y, Gilman RH, Bern C, Xiao L, 2007. Differences in clinical manifestations among Cryptosporidium species and subtypes in HIV-infected persons. J Infect Dis 196: 684691.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Gatei W, Greensill J, Ashford RW, Cuevas LE, Parry CM, Cunliffe NA, Beeching NJ, Hart CA, 2003. Molecular analysis of the 18S rRNA gene of Cryptosporidium parasites from patients with or without human immunodeficiency virus infections living in Kenya, Malawi, Brazil, the United Kingdom, and Vietnam. J Clin Microbiol 41: 14581462.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Muthusamy D, Rao SS, Ramani S, Monica B, Banerjee I, Abraham OC, Mathai DC, Primrose B, Muliyil J, Wanke CA, Ward HD, Kang G, 2006. Multilocus genotyping of Cryptosporidium sp. isolates from human immunodeficiency virus-infected individuals in South India. J Clin Microbiol 44: 632634.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Raccurt CP, Brasseur P, Verdier RI, Li X, Eyma E, Stockman CP, Agnamey P, Guyot K, Totet A, Liautaud B, Nevez G, Dei-Cas E, Pape JW, 2006. Human cryptosporidiosis and Cryptosporidium spp. in Haiti. Trop Med Int Health 11: 929934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Gatei W, Ashford RW, Beeching NJ, Kamwati SK, Greensill J, Hart CA, 2002. Cryptosporidium muris infection in an HIV-infected adult, Kenya. Emerg Infect Dis 8: 204206.

  • 56.

    Morgan U, Weber R, Xiao L, Sulaiman I, Thompson RC, Ndiritu W, Lal A, Moore A, Deplazes P, 2000. Molecular characterization of Cryptosporidium isolates obtained from human immunodeficiency virus-infected individuals living in Switzerland, Kenya, and the United States. J Clin Microbiol 38: 11801183.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57.

    Jex AR, Gasser RB, 2010. Genetic richness and diversity in Cryptosporidium hominis and C. parvum reveals major knowledge gaps and a need for the application of “next generation” technologies–research review. Biotechnol Adv 28: 1726.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 58.

    Peng MM, Matos O, Gatei W, Das P, Stantic-Pavlinic M, Bern C, Sulaiman IM, Glaberman S, Lal AA, Xiao L, 2001. A comparison of Cryptosporidium subgenotypes from several geographic regions. J Eukaryot Microbiol (Suppl) 48: 28S31S.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 59.

    Akiyoshi DE, Tumwine JK, Bakeera-Kitaka S, Tzipori S, 2006. Subtype analysis of Cryptosporidium isolates from children in Uganda. J Parasitol 92: 10971100.

  • 60.

    Wanyiri JW, O'Connor R, Allison G, Kim K, Kane A, Qiu J, Plaut AG, Ward HD, 2007. Proteolytic processing of the Cryptosporidium glycoprotein gp40/15 by human furin and by a parasite-derived furin-like protease activity. Infect Immun 75: 184192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 61.

    Arrowood MJ, Sterling CR, Healey MC, 1991. Immunofluorescent microscopical visualization of trails left by gliding Cryptosporidium parvum sporozoites. J Parasitol 77: 315317.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 62.

    Enriquez FJ, Riggs MW, 1998. Role of immunoglobulin A monoclonal antibodies against P23 in controlling murine Cryptosporidium parvum infection. Infect Immun 66: 44694473.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 63.

    Perryman LE, Jasmer DP, Riggs MW, Bohnet SG, McGuire TC, Arrowood MJ, 1996. A cloned gene of Cryptosporidium parvum encodes neutralization-sensitive epitopes. Mol Biochem Parasitol 80: 137147.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 64.

    O'Connor RM, Thorpe CM, Cevallos AM, Ward HD, 2002. Expression of the highly polymorphic Cryptosporidium parvum Cpgp40/15 gene in genotype I and II isolates. Mol Biochem Parasitol 119: 203215.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 65.

    Strong WB, Gut J, Nelson RG, 2000. Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of its 15- and 45-kilodalton zoite surface antigen products. Infect Immun 68: 41174134.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 66.

    Sturbaum GD, Jost BH, Sterling CR, 2003. Nucleotide changes within three Cryptosporidium parvum surface protein encoding genes differentiate genotype I from genotype II isolates. Mol Biochem Parasitol 128: 8790.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 67.

    Ungar BL, Nash TE, 1986. Quantification of specific antibody response to Cryptosporidium antigens by laser densitometry. Infect Immun 53: 124128.

  • 68.

    Sandhu SK, Priest JW, Lammie PJ, Hubbard A, Colford JM Jr, Eisenberg JN, 2006. The natural history of antibody responses to Cryptosporidium parasites in men at high risk of HIV infection. J Infect Dis 194: 14281437.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 69.

    Kaushik K, Khurana S, Wanchu A, Malla N, 2009. Serum immunoglobulin G, M and A response to Cryptosporidium parvum in Cryptosporidium-HIV co-infected patients. BMC Infect Dis 9: 179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 70.

    Benhamou Y, Kapel N, Hoang C, Matta H, Meillet D, Magne D, Raphael M, Gentilini M, Opolon P, Gobert JG, 1995. Inefficacy of intestinal secretory immune response to Cryptosporidium in acquired immunodeficiency syndrome. Gastroenterology 108: 627635.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 71.

    Hunter PR, Nichols G, 2002. Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clin Microbiol Rev 15: 145154.

  • 72.

    Pantenburg B, Dann SM, Wang HC, Robinson P, Castellanos-Gonzalez A, Lewis DE, White AC Jr, 2008. Intestinal immune response to human Cryptosporidium sp. infection. Infect Immun 76: 2329.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 73.

    Ahs JW, Tao W, Löfgren J, Forsberg BC, 2010. Diarrheal diseases in low- and middle-income countries: incidence, prevention and management. The Open Infectious Diseases Journal 4: 113124.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 74.

    Dann SM, Okhuysen PC, Salameh BM, DuPont HL, Chappell CL, 2000. Fecal antibodies to Cryptosporidium parvum in healthy volunteers. Infect Immun 68: 50685074.

  • 75.

    Mejia R, Vicuna Y, Broncano N, Sandoval C, Vaca M, Chico M, Cooper PJ, Nutman TB, 2013. A novel, multi-parallel, real-time polymerase chain reaction approach for eight gastrointestinal parasites provides improved diagnostic capabilities to resource-limited at-risk populations. Am J Trop Med Hyg 88: 10411047.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 76.

    Thomas TA, Mondal D, Noor Z, Liu L, Alam M, Haque R, Banu S, Sun H, Peterson KM, 2010. Malnutrition and helminth infection affect performance of an interferon gamma-release assay. Pediatrics 126: e1522e1529.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 77.

    Hagel I, Cabrera M, Puccio F, Santaella C, Buvat E, Infante B, Zabala M, Cordero R, Di Prisco MC, 2011. Co-infection with Ascaris lumbricoides modulates protective immune responses against Giardia duodenalis in school Venezuelan rural children. Acta Trop 117: 189195.

    • PubMed
    • Search Google Scholar
    • Export Citation
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