Cryptosporidium meleagridis: Infectivity in Healthy Adult Volunteers

Cynthia L. Chappell Center for Infectious Diseases, The University of Texas Health Science Center at Houston, School of Public Health, Houston, Texas; Department of Internal Medicine, The University of Texas Health Science Center at Houston, Medical School, Houston, Texas; Department of Biomedical Sciences, Tufts University Cummings School of Veterinary Medicine, North Grafton, Massachusetts

Search for other papers by Cynthia L. Chappell in
Current site
Google Scholar
PubMed
Close
,
Pablo C. Okhuysen Center for Infectious Diseases, The University of Texas Health Science Center at Houston, School of Public Health, Houston, Texas; Department of Internal Medicine, The University of Texas Health Science Center at Houston, Medical School, Houston, Texas; Department of Biomedical Sciences, Tufts University Cummings School of Veterinary Medicine, North Grafton, Massachusetts

Search for other papers by Pablo C. Okhuysen in
Current site
Google Scholar
PubMed
Close
,
Rebecca C. Langer-Curry Center for Infectious Diseases, The University of Texas Health Science Center at Houston, School of Public Health, Houston, Texas; Department of Internal Medicine, The University of Texas Health Science Center at Houston, Medical School, Houston, Texas; Department of Biomedical Sciences, Tufts University Cummings School of Veterinary Medicine, North Grafton, Massachusetts

Search for other papers by Rebecca C. Langer-Curry in
Current site
Google Scholar
PubMed
Close
,
Donna E. Akiyoshi Center for Infectious Diseases, The University of Texas Health Science Center at Houston, School of Public Health, Houston, Texas; Department of Internal Medicine, The University of Texas Health Science Center at Houston, Medical School, Houston, Texas; Department of Biomedical Sciences, Tufts University Cummings School of Veterinary Medicine, North Grafton, Massachusetts

Search for other papers by Donna E. Akiyoshi in
Current site
Google Scholar
PubMed
Close
,
Giovanni Widmer Center for Infectious Diseases, The University of Texas Health Science Center at Houston, School of Public Health, Houston, Texas; Department of Internal Medicine, The University of Texas Health Science Center at Houston, Medical School, Houston, Texas; Department of Biomedical Sciences, Tufts University Cummings School of Veterinary Medicine, North Grafton, Massachusetts

Search for other papers by Giovanni Widmer in
Current site
Google Scholar
PubMed
Close
, and
Saul Tzipori Center for Infectious Diseases, The University of Texas Health Science Center at Houston, School of Public Health, Houston, Texas; Department of Internal Medicine, The University of Texas Health Science Center at Houston, Medical School, Houston, Texas; Department of Biomedical Sciences, Tufts University Cummings School of Veterinary Medicine, North Grafton, Massachusetts

Search for other papers by Saul Tzipori in
Current site
Google Scholar
PubMed
Close
Restricted access

Most Cryptosporidium infections in humans are caused by C. parvum or C. hominis. However, genotyping techniques have identified infections caused by unusual Cryptosporidium species. Cryptosporidium meleagridis has been identified in ≤ 1% of persons with diarrhea, although prevalence is higher in developing nations. We examined the infectivity of C. meleagridis in healthy adults. Five volunteers were challenged with 105 C. meleagridis oocysts and monitored six weeks for fecal oocysts and clinical manifestations. Four volunteers had diarrhea; three had detectable fecal oocysts; and one infected volunteer remained asymptomatic. Fecal DNA from two volunteers was amplified by using a polymerase chain reaction specific for the Cryptosporidium small subunit ribosomal RNA gene. Nucleotide sequence of these amplicons was diagnostic for C. meleagridis. All infections were self-limited; oocysts were cleared within ≤ 12 days of challenge. These studies establish that healthy adults can be infected and become ill from ingestion of C. meleagridis oocysts.

Author Notes

*Address correspondence to Cynthia L. Chappell, Center for Infectious Diseases, University of Texas School of Public Health, 1200 Herman Pressler, Suite 644, Houston, TX 77030. E-mail: cynthia.l.chappell@uth.tmc.edu

Financial support: This study was supported, in part, by the National Center for Environmental Research STAR Program of the Environmental Protection Agency (grant GR828035-01-0 to Cynthia L. Chappell), the National Institutes of Health General Clinical Research Centers (grant RR-02558), and the National Institute of Allergy and Infectious Diseases (grant AI52781 to Giovanni Widmer and grant NO1-AI-25466 to Saul Tzipori).

Authors' addresses: Cynthia L. Chappell, Center for Infectious Diseases, University of Texas School of Public Health, Houston, TX, E-mail: cynthia.l.chappell@uth.tmc.edu. Pablo C. Okhuysen, Division of Infectious Diseases University of Texas Health Medical School, Houston, TX, E-mail: pablo.c.okhuysen@uth.tmc.edu. Rebecca C. Langer-Curry, Bayer CropScience Bioscience, Morrisville, NC, E-mail: becky.langer@bayer.com. Donna E. Akiyoshi, Giovanni Widmer, and Saul Tzipori, Department of Biomedical Sciences, Tufts University, North Grafton, MA, Emails: donna.akiyoshi@tufts.edu, giovanni.widmer@tufts.edu, and saul.tzipori@tufts.edu.

  • 1.

    McLauchlin J, Amar C, Pedraza-Diaz S, Nichols GL, 2000. Molecular epidemiological analysis of Cryptosporidium spp. in the United Kingdom: results of genotyping Cryptosporidium spp. in 1,705 fecal samples from humans and 105 fecal samples from livestock animals. J Clin Microbiol 38: 39843990.

    • Search Google Scholar
    • Export Citation
  • 2.

    Chalmers RM, Elwin K, Thomas AL, Guy EC, Mason B, 2009. Long-term Cryptosporidium typing reveals the aetiology and species-specific epidemiology of human cryptosporidiosis in England and Wales, 2000 to 2003. Euro Surveill 14: pii: 19086.

    • Search Google Scholar
    • Export Citation
  • 3.

    Gatei W, Suputtamongkol Y, Waywa D, Ashford RW, Bailey JW, Greensill J, Beeching NJ, Hart CA, 2002. Zoonotic species of Cryptosporidium are as prevalent as the anthroponotic in HIV-infected patients in Thailand. Ann Trop Med Parasitol 96: 797802.

    • Search Google Scholar
    • Export Citation
  • 4.

    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.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cama VA, Bern C, Roberts J, Cabrera L, Sterling CR, Ortega Y, Gilman RH, Xiao L, 2008. Cryptosporidium species and subtypes and clinical manifestations in children, Peru. Emerg Infect Dis 14: 15671574.

    • Search Google Scholar
    • Export Citation
  • 6.

    Slavin D, 1955. Cryptosporidium meleagridis (sp. nov.). J Comp Pathol 65: 262266.

  • 7.

    Morgan UM, Xiao L, Limor J, Gelis S, Raidal SR, Fayer R, Lal A, Elliot A, Thompson RC, 2000. Cryptosporidium meleagridis in an Indian ring-necked parrot (Psittacula krameri). Aust Vet J 78: 182183.

    • Search Google Scholar
    • Export Citation
  • 8.

    Pages-Mante A, Pages-Bosch M, Majo-Masferrer N, Gomez-Couso H, Ares-Mazas E, 2007. An outbreak of disease associated with cryptosporidia on a red-legged partridge (Alectoris rufa) game farm. Avian Pathol 36: 275278.

    • Search Google Scholar
    • Export Citation
  • 9.

    Sreter T, Kovacs G, da Silva AJ, Pieniazek NJ, Szell Z, Dobos-Kovacs M, Marialigeti K, Varga I, 2000. Morphologic, host specificity, and molecular characterization of a Hungarian Cryptosporidium meleagridis isolate. Appl Environ Microbiol 66: 735738.

    • Search Google Scholar
    • Export Citation
  • 10.

    Huang K, Akiyoshi DE, Feng X, Tzipori S, 2003. Development of patent infection in immunosuppressed C57Bl/6 mice with a single Cryptosporidium meleagridis oocyst. J Parasitol 89: 620622.

    • Search Google Scholar
    • Export Citation
  • 11.

    Akiyoshi DE, Dilo J, Pearson C, Chapman S, Tumwine J, Tzipori S, 2003. Characterization of Cryptosporidium meleagridis of human origin passaged through different host species. Infect Immun 71: 18281832.

    • Search Google Scholar
    • Export Citation
  • 12.

    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.

    • Search Google Scholar
    • Export Citation
  • 13.

    Essid R, Mousli M, Aoun K, Abdelmalek R, Mellouli F, Kanoun F, Derouin F, Bouratbine A, 2008. Identification of Cryptosporidium species infecting humans in Tunisia. Am J Trop Med Hyg 79: 702705.

    • Search Google Scholar
    • Export Citation
  • 14.

    Pedraza-Díaz S, Amar CF, McLauchlin J, Nichols GL, Cotton KM, Godwin P, Iversen AM, Milne L, Mulla JR, Nye K, Panigrahl H, Venn SR, Wiggins R, Williams M, Youngs ER, 2001. Cryptosporidium meleagridis from humans: molecular analysis and description of affected patients. J Infect 42: 243250.

    • Search Google Scholar
    • Export Citation
  • 15.

    Cama VA, Bern C, Sulaiman IM, Gilman RH, Ticona E, Vivar A, Kawai V, Vargas D, Zhou L, Xiao L, 2003. Cryptosporidium species and genotypes in HIV-positive patients in Lima, Peru. J Eukaryot Microbiol 50: 531533.

    • Search Google Scholar
    • Export Citation
  • 16.

    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.

    • Search Google Scholar
    • Export Citation
  • 17.

    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.

    • Search Google Scholar
    • Export Citation
  • 18.

    Gatei W, Das P, Dutta P, Sen A, Cama V, Lal AA, Xiao L, 2007. Multilocus sequence typing and genetic structure of Cryptosporidium hominis from children in Kolkata, India. Infect Genet Evol 7: 197205.

    • Search Google Scholar
    • Export Citation
  • 19.

    Matos O, Alves M, Xiao L, Cama V, Antunes F, 2004. Cryptosporidium felis and C. meleagridis in persons with HIV, Portugal. Emerg Infect Dis 10: 22562257.

    • Search Google Scholar
    • Export Citation
  • 20.

    Hung CC, Tsaihong JC, Lee YT, Deng HY, Hsiao WH, Chang SY, Chang SC, Su KE, 2007. Prevalence of intestinal infection due to Cryptosporidium species among Taiwanese patients with human immunodeficiency virus infection. J Formos Med Assoc 106: 3135.

    • Search Google Scholar
    • Export Citation
  • 21.

    Tumwine JK, Kekitiinwa A, Nabukeera N, Akiyoshi DE, Rich SM, Widmer G, Feng X, Tzipori S, 2003. Cryptosporidium parvum in children with diarrhea in Mulago Hospital, Kampala, Uganda. Am J Trop Med Hyg 68: 710715.

    • Search Google Scholar
    • Export Citation
  • 22.

    Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, Akiyoshi DE, Tzipori S, 2005. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg 73: 921925.

    • Search Google Scholar
    • Export Citation
  • 23.

    Yagita K, Izumiyama S, Tachibana H, Masuda G, Iseki M, Furuya K, Kameoka Y, Kuroki T, Itagaki T, Endo T, 2001. Molecular characterization of Cryptosporidium isolates obtained from human and bovine infections in Japan. Parasitol Res 87: 950955.

    • Search Google Scholar
    • Export Citation
  • 24.

    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.

    • Search Google Scholar
    • Export Citation
  • 25.

    Llorente MT, Clavel A, Goñi MP, Varea M, Seral C, Becerril R, Suarez L, Gómez-Lus R, 2007. Genetic characterization of Cryptosporidium species from humans in Spain. Parasitol Int 56: 201205.

    • Search Google Scholar
    • Export Citation
  • 26.

    Guyot K, Follet-Dumoulin A, Lelièvre E, Sarfati C, Rabodonirina M, Nevez G, Cailliez JC, Camus D, Dei-Cas E, 2001. Molecular characterization of Cryptosporidium isolates obtained from humans in France. J Clin Microbiol 39: 34723480.

    • Search Google Scholar
    • Export Citation
  • 27.

    Tiangtip R, Jongwutiwes S, 2002. Molecular analysis of Cryptosporidium species isolated from HIV-infected patients in Thailand. Trop Med Int Health 7: 357364.

    • Search Google Scholar
    • Export Citation
  • 28.

    Blanco MA, Iborra A, Vargas A, Nsie E, Mbá L, Fuentes I, 2009. Molecular characterization of Cryptosporidium isolates from humans in Equatorial Guinea. Trans R Soc Trop Med Hyg 103: 12821284.

    • Search Google Scholar
    • Export Citation
  • 29.

    Al-Brikan FA, Salem HS, Beeching N, Hilal N, 2008. Multilocus genetic analysis of Cryptosporidium isolates from Saudi Arabia. J Egypt Soc Parasitol 38: 645658.

    • Search Google Scholar
    • Export Citation
  • 30.

    Araújo AJ, Kanamura HY, Almeida ME, Gomes AH, Pinto TH, Da Silva AJ, 2008. Genotypic identification of Cryptosporidium spp. isolated from HIV-infected patients and immunocompetent children of São Paulo, Brazil. Rev Inst Med Trop Sao Paulo 50: 139143.

    • Search Google Scholar
    • Export Citation
  • 31.

    Bajer A, Bednarska M, Cacciò SM, Wolska-Kusśnierz B, Heropolitanska-Pliszka E, Bernatowska E, Wielopolska M, Paziewska A, Welc-Faleciak R, Sinński E, 2008. Genotyping of Cryptosporidium isolates from human clinical cases in Poland. Parasitol Res 103: 3742.

    • Search Google Scholar
    • Export Citation
  • 32.

    Leoni F, Amar C, Nichols G, Pedraza-Díaz S, McLauchlin J, 2006. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J Med Microbiol 55: 703707.

    • Search Google Scholar
    • Export Citation
  • 33.

    Enemark HL, Ahrens P, Juel CD, Petersen E, Petersen RF, Andersen JS, Lind P, Thamsborg SM, 2002. Molecular characterization of Danish Cryptosporidium parvum isolates. Parasitology 125: 331341.

    • Search Google Scholar
    • Export Citation
  • 34.

    Xiao L, Bern C, Limor J, Sulaiman I, Roberts J, Checkley W, Cabre L, Gilman RH, Lal AA, 2001. Identification of 5 types of Cryptosporidium parasites in children in Lima, Peru. J Infect Dis 183: 492497.

    • Search Google Scholar
    • Export Citation
  • 35.

    Champliaud D, Gobet P, Naciri M, Vagner O, Lopez J, Buisson JC, Varga I, Harly G, Mancassola R, Bonnin A, 1998. Failure to differentiate Cryptosporidium parvum from C. meleagridis based on PCR amplification of eight DNA sequences. Appl Environ Microbiol 64: 14541458.

    • Search Google Scholar
    • Export Citation
  • 36.

    DuPont HL, Chappell CL, Sterling CR, Okhuysen PC, Rose JB, Jakubowski W, 1995. The infectivity of Cryptosporidium parvum in healthy volunteers. N Engl J Med 332: 855859.

    • Search Google Scholar
    • Export Citation
  • 37.

    Okhuysen PC, Chappell CL, Crabb JH, Sterling CR, DuPont HL, 1999. Virulence of three distinct Cryptosporidium parvum isolates for healthy adults. J Infect Dis 180: 12751281.

    • Search Google Scholar
    • Export Citation
  • 38.

    Okhuysen PC, Rich SM, Chappell CL, Grimes KA, Widmer G, Feng X, Tzipori S, 2002. Infectivity of a Cryptosporidium parvum isolate of cervine origin for healthy adults and interferon-γ knockout mice. J Infect Dis 185: 13201325.

    • Search Google Scholar
    • Export Citation
  • 39.

    Chappell CL, Okhuysen PC, Langer-Curry R, Widmer G, Akiyoshi DE, Tanriverdi S, Tzipori S, 2006. Cryptosporidium hominis: experimental challenge of healthy adults. Am J Trop Med Hyg 75: 851857.

    • Search Google Scholar
    • Export Citation
  • 40.

    Chappell CL, Okhuysen PC, White AC Jr, 2004. Cryptosporidium parvum: infectivity, pathogenesis and the host-parasite relationship. Thompson R, Armson A, Ryan U, eds. Cryptosporidium: From Molecules to Disease. Bridgewater, NJ: Elsevier Science, 1950.

    • Search Google Scholar
    • Export Citation
  • 41.

    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.

    • Search Google Scholar
    • Export Citation
  • 42.

    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: 33863391.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 44 44 10
Full Text Views 404 132 1
PDF Downloads 132 31 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save