Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-22T16:40:45.749Z Has data issue: false hasContentIssue false

Cryptosporidium and host resistance: historical perspective and some novel approaches

Published online by Cambridge University Press:  28 February 2007

James A. Harp*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, National Animal Disease Center, 2300 Dayton Avenue, Ames, IA 50010, USA
*

Abstract

Cryptosporidium parvum is recognized as a major cause of diarrheal disease in neonatal bovine calves. In addition, this protozoan parasite has emerged as an important cause of disease in both immunocompromised and immunocompetent humans. Despite years of research, no consistently effective means of prevention or treatment are readily available for cryptosporidiosis in any species. Infection through ingestion of contaminated water has been widely documented; C. parvum was reported to be responsible for the largest waterborne outbreak of infectious disease in US history. In addition to its role as a primary disease agent, C. parvum has potential to initiate or exacerbate other gastrointestinal disorders, such as inflammatory bowel disease. Thus, control of C. parvum infection in both animals and humans remains an important objective. Research in our laboratory has focused on understanding mechanisms of resistance to C. parvum. We have demonstrated that acquisition of intestinal flora increases resistance to C. parvum. Substances present in the intestinal mucosa of adult animals can transfer resistance when fed to susceptible infants. Both expression of intestinal enzymes and rate of proliferation of epithelial cells may be altered following C. parvum infection. These and other changes may have profound effects on host resistance to C. parvum.

Type
Research Article
Copyright
Copyright © USDA 2003

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abrahamsen, MS, Lancto, CA, Walcheck, B, Layton, W and Jutila, MA (1997) Localization of alpha/beta and gamma/delta T lymphocytes in Cryptosporidium parvum-infected tissues in naive and immune calves. Infection and Immunity 65: 24282433.Google Scholar
Akili, D and Harp, JA (2000) A factor derived from adult rat and cow small intestine reduces Cryptosporidium parvum infection in infant rats. Journal of Parasitology 86: 979982.CrossRefGoogle ScholarPubMed
Alak, JIB, Wolf, BW, Mdurvwa, EG, Pimentel-Smith, GE and Adeyemo, O (1997) Effect of Lactobacillus reuteri on intestinal resistance to Cryptosporidium parvum infection in a murine model of acquired immunodeficiency syndrome. Journal of Infectious Diseases 175: 218221.Google Scholar
Angus, KW (1990) Cryptosporidiosis in ruminants. In: Dubey, JP, Speer, CA and Fayer, R (eds), Cryptosporidiosis of Man and Animals. Boca Raton: CRC Press, pp 83103.Google Scholar
Bancroft, GJ, Schreiber, RD and Unanue, ER (1991) Natural immunity–a T-cell-independent pathway of macrophage activation, defined in the SCID mouse. Immunological Reviews 124: 524.CrossRefGoogle ScholarPubMed
Blagburn, BL and Soave, R (1997) Prophylaxis and chemotherapy: human and animal. In: Fayer, R (ed.), Cryptosporidium and Cryptosporidiosis. Boca Raton: CRC Press pp. 111128.Google Scholar
Bosma, GC, Custer, RP and Bosma, MJ (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301: 527530.CrossRefGoogle ScholarPubMed
Butler, JE (1999) Immunoglobulins and immunocytes in animal milks. In: Ogra, PL, Mestecky, J, Lamm, MEet al. (eds), Mucosal Immunology. New York: Academic Press, pp 15311554.Google Scholar
Caccio, S, Pinter, E, Fantini, R, Mezzaroma, I and Pozio, E (2002) Human infection with Cryptosporidium felis: case report and literature review. Emerging Infectious Diseases 8: 8586.CrossRefGoogle ScholarPubMed
Casas, I&Dobrogosz, WJ (1997) Lactobacillus reuteri: overview of a new probiotic for humans and animals. Microecology and Therapy 26: 221231.Google Scholar
Casemore, DP, Wright, SE and Coop, RL (1997) Cryptosporidiosis–human and animal epidemiology. In: Fayer, R (ed.), Cryptosporidium and Cryptosporidiosis. Boca Raton: CRC Press, pp 6592.Google Scholar
Casey, MJ (1991) Cryptosporidium and bovine cryptosporidiosis: a review. Irish Veterinary Journal 44: 27.Google Scholar
Chalmers, RM, Elwin, K, Thomas, AL and Joynson, DHM (2002) Infection with unusual types of Cryptosporidium is not restricted to immunocompromised patients. Journal of Infectious Diseases 185: 270271.Google Scholar
Chen, W, Harp, JA and Harmsen, AG (1993) Requirements for CD4+ cells and gamma interferon in resolution of established Cryptosporidium parvum infection in mice. Infection and Immunity 61: 39283932.Google Scholar
Chen, W, Harp, JA, Harmsen, AG and Havell, EA (1993) Gamma interferon functions in resistance to Cryptosporidium parvum infection in severe combined immunodeficient mice. Infection and Immunity 61: 35483551.Google Scholar
Chen, W, Chadwick, V, Tie, A and Harp, J (2001) Cryptosporidium parvum in intestinal mucosal biopsies from patients with inflammatory bowel disease. American Journal of Gastroenterology 96: 34633464.CrossRefGoogle ScholarPubMed
Chen, X-M, Keithly, JS, Paya, CV and LaRusso, NF (2002) Cryptosporidiosis. New England Journal of Medicine 346: 17231731.Google Scholar
Chomczynski, P and Sacchi, N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol– chloroform extraction. Analytical Biochemistry 162: 156159.Google Scholar
Davis, CP, McAllister, JS and Savage, DC (1973) Microbial colonization of the intestinal epithelium in suckling mice. Infection and Immunity 7: 666672.Google Scholar
de Graaf, DC, Walravens, K, Godfroid, J and Peeters, JE (1998) A Cryptosporidium parvum oocyst low molecular mass fraction evokes a CD4+ T-cell-dependent IFN-gamma response in bovine peripheral blood mononuclear cell cultures. International Journal for Parasitology 28(12): 18751880.Google Scholar
De Simone, C, Vesely, R, Salvadori, BB and Jirillo, E (1993) The role of probiotics in the modulation of the immune system in man and in animals. International Journal of Immunotherapy 1: 2329.Google Scholar
De Simone, C, Famularo, G, Harp, JA, Tzantzoglou, S and Chen, W (1995) Effect of lactobacilli on Cryptosporidium parvum infection in man and animals. Microecology and Therapy 25: 3236.Google Scholar
Edwards, DD (1993) Troubled waters in Milwaukee. ASM News 59: 342345.Google Scholar
Ekenna, O and Scheretz, RJ (1987) Factors affecting colonization and dissemination of Candida albicans from the gastrointestinal tract of mice. Infection and Immunity 55: 15581563.Google Scholar
Fayer, R and Ellis, W (1993) Paromomycin is effective as prophylaxis for cryptosporidiosis in dairy calves. Journal of Parasitology 79: 771774.Google Scholar
Fayer, R, Andrews, C, Ungar, BLP and Blagburn, B (1989) Efficacy of hyperimmune bovine colostrum for prophylaxis of cryptosporidiosis in neonatal calves. Journal of Parasitology 75: 393397.CrossRefGoogle ScholarPubMed
Fayer, R, Speer, CA and Dubey, JP (1997) The general biology of Cryptosporidium. In: Fayer, R (ed.), Cryptosporidium and Cryptosporidiosis. Boca Raton: CRC Press, pp 142.Google Scholar
Fayer, R, Gasbarre, L, Pasquali, P, Canals, A, Almeria, S and Zarlenga, D (1998) Cryptosporidium parvum infection in bovine neonates: dynamic clinical, parasitic and immunologic patterns. International Journal for Parasitology 28: 4956.Google Scholar
Fayer, R, Morgan, U and Upton, SJ (2000) Epidemiology of Cryptosporidium: transmission, detection and identification. International Journal for Parasitology 30: 13051322.Google Scholar
Feng, X, Rich, SM, Tzipori, S and Widmer, G (2002) Experimental evidence for genetic recombination in the opportunistic pathogen Cryptosporidium parvum. Molecular and Biochemical Parasitology 119: 5562.Google Scholar
Garber, LP, Salman, MD, Hurd, HS, Keefe, T and Schlater, JL (1994) Potential risk factors for Cryptosporidium infection in dairy calves. Journal of the American Veterinary Medical Association 205: 8691.CrossRefGoogle ScholarPubMed
Gilles, HM and Hoffman, PS (2002) Treatment of intestinal parasitic infections: a review of nitazoxanide. Trends in Parasitology 18: 9597.Google Scholar
Gordon, HA and Pesti, L (1971) The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriological Reviews 35: 390429.Google Scholar
Guerrant, RL, Steiner, TS, Lima, AAM and Bobak, DA (1999) How intestinal bacteria cause disease. Journal of Infectious Diseases 179 (Suppl. 2): S331337.Google Scholar
Harp, JA (1996) The importance of intestinal microflora in Cryptosporidium parvum infection. Journal of Immunology and Immunopharmacology 16: 1116.Google Scholar
Harp, JA (1999) Oral dosing of neonatal mice with sucrose reduces infection with Cryptosporidium parvum. Journal of Parasitology 85: 952955.Google Scholar
Harp, JA and Goff, JP (1995) Protection of calves with a vaccine against Cryptosporidium parvum. Journal of Parasitology 81: 5457.Google Scholar
Harp, JA and Goff, JP (1998) Strategies for the control of Cryptosporidium parvum infection in calves. Journal of Dairy Science 81: 289294.CrossRefGoogle ScholarPubMed
Harp, JA, Wannemuehler, MW, Woodmansee, DB and Moon, HW (1988) Susceptibility of germfree or antibiotic-treated adult mice to Cryptosporidium parvum. Infection and Immunity 56: 20062010.CrossRefGoogle ScholarPubMed
Harp, JA, Woodmansee, DB and Moon, HW (1989) Effects of colostral antibody on susceptibility of calves to Cryptosporidium parvum infection. American Journal of Veterinary Research 50: 21172119.Google Scholar
Harp, JA, Woodmansee, DB and Moon, HW (1990) Resistance of calves to Cryptosporidium parvum: Effects of age and previous exposure. Infection and Immunity 58: 22372240.Google Scholar
Harp, JA, Chen, W&Harmsen, AG (1992) Resistance of severe combined immunodeficient mice to infection with Cryptosporidium parvum: The importance of intestinal microflora. Infection and Immunity 60: 35093512.Google Scholar
Harp, JA, Jardon, P, Atwill, ER, Zylstra, M, Checel, S, Goff, JP and Simone, CD (1996) Field testing of prophylactic measures against Cryptosporidium parvum infection in calves in a California dairy herd. American Journal of Veterinary Research 57: 15861588.Google Scholar
Harp, JA, Akili, D and Pesch, BA (1999) Changes in murine intestinal epithelium following Cryptosporidium parvum infection. Journal of Eukaryotic Microbiology 46: 6465S.Google ScholarPubMed
Havell, EA and Rogerson, BJ (1993) Endotoxin-induced tumor necrosis factor alpha synthesis in murine embryo fibroblasts. Infection and Immunity 61: 16301635.Google Scholar
Heine, J, Moon, HW and Woodmansee, DB (1984) Persistent Cryptosporidium infection in congenitally athymic (nude) mice. Infection and Immunity 43: 856859.CrossRefGoogle ScholarPubMed
Heine, J, Pohlenz, JFL, Moon, HW and Woode, GN (1984) Enteric lesions and diarrhea in gnotobiotic calves monoinfected with Cryptosporidium species. Journal of Infectious Diseases 150: 768775.CrossRefGoogle ScholarPubMed
Henning, SJ (1987) Functional development of the gastrointestinal tract. In: Johnson, LR (eds), Physiology of the Gastrointestinal Tract, Vol. 1.. New York: Raven Press, pp. 285300.Google Scholar
Hewitt, RG, Yiannoutsos, CT, Higgs, ES, Carey, JT, Geisler, PJ, Soave, R, Rosenberg, R, Vazquez, GJ, Wheat, LJ, Fass, RJ, Antoninievic, Z, Walawander, AL, Flanigan, TP and Bender, JF (2000) Paromomycin: no more effective than placebo for treatment of cryptosporidiosis in patients with advanced human immunodeficiency virus infection. Clinical Infectious Diseases 31: 10841092.Google Scholar
Hunter, PR and Nichols, G (2002) Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clinical Microbiology Reviews 15: 145154.CrossRefGoogle ScholarPubMed
Kennedy, MJ and Volz, PA (1983) Dissemination of yeasts after gastrointestinal inoculation in antibiotic-treated mice. Sabouradia 21: 2733.Google Scholar
Kennedy, MJ and Volz, PA (1985) Effect of various antibiotics on gastrointestinal colonization and dissemination by Candida albicans. Sabouradia 23: 265273.CrossRefGoogle ScholarPubMed
Klein, RM (1989) Small intestinal cell proliferation during development. In: Lebenthal, E (ed.), Human Gastrointestinal Development. New York: Raven Press pp. 367392.Google Scholar
Kosek, M, Alcantara, C, Lima, AA and Guerrant, RL (2001) Cryptosporidiosis: an update. Lancet Infectious Diseases 1: 262269.Google Scholar
Kuhls, TL, Mosier, DA and Crawford, DL (1991) Effects of carbohydrates and lectins on cryptosporidial sporozoite penetration of cultured cell monolayers. Journal of Protozoology 38: S74S76.Google Scholar
Lindsay, DS, Woods, KM, Upton, SJ and Blagburn, BL (2000) Activity of decoquinate against Cryptosporidium parvum in cell cultures and neonatal mice. Veterinary Parasitology 89: 307311.Google Scholar
Llovo, J, Lopez, A, Fabregas, J and Munoz, A (1993) Interaction of lectins with Cryptosporidium parvum. Journal of Infectious Diseases 167: 14771480.CrossRefGoogle ScholarPubMed
MacKenzie, WR, Hoxie, NJ, Proctor, ME, Gradus, MS, Blair, KA, Peterson, DE, Kazmierczak, JJ, Addiss, DG, Fox, KR, Rose, JB and Davis, JP (1994) A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. New England Journal of Medicine 331: 161167.CrossRefGoogle Scholar
MacKenzie, WR, Schell, WL, Blair, KA, Addiss, DG, Peterson, DE, Hoxie, NJ, Kazmierczak, JJ and Davis, JP (1995) Massive outbreak of waterborne Cryptosporidium infection in Milwaukee, Wisconsin: recurrence of illness and risk of secondary transmission. Clinical Infectious Diseases 21: 5762.Google Scholar
Manthey, MW, Ross, AR and Soergel, KH (1997) Cryptosporidiosis and inflammatory bowel disease. Experience from the Milwaukee outbreak. Digestive Diseases and Sciences 42: 15801586.Google Scholar
McDonald, V and Bancroft, GJ (1998) Immunological control of Cryptosporidium infection. In: Liew, FY and Cox, FEG (eds), Immunology of Intracellular Parasitism, Vol. 70. Basel: Karger, pp. 103123.Google Scholar
Mead, JR, Arrowood, MJ, Sidwell, RW and Healey, MC (1991) Chronic Cryptosporidium parvum infections in congenitally immunodeficient SCID and nude mice. Journal of Infectious Diseases 163: 12971304.CrossRefGoogle ScholarPubMed
Moon, HW, McClurkin, AW, Isaacson, RE, Pohlenz, J, Skartvedt, SM, Gillette, KG and Baetz, AL (1978) Pathogenic relationships of rotavirus, Escherichia coli, and other agents in mixed infections in calves. Journal of the American Veterinary Medical Association 173: 577583.Google Scholar
Moore, D, Waters, WR, Wannemuehler, MJ and Harp, JA (2001) Treatment with agmatine inhibits Cryptosporidium parvum infection in infant mice. Journal of Parasitology 87: 211213.Google Scholar
Morgan-Ryan, UM, Fall, A, Ward, LA, Hijjawi, N, Sulaiman, I, Fayer, R, Thompson, RCA, Olson, M, Lal, A and Xiao, L (2002) Cryptosporidium hominis n. sp. (Apicomplexa: Cryptosporidiidae) from Homo sapiens. Journal of Eukaryotic Microbiology 49: 433440.Google Scholar
Nelson, RG and Rosowsky, A (2001) Dicyclic and tricyclic diaminopyrimidine derivatives as potent inhibitors of Cryptosporidium parvum dihydrofolate reductase: structure–activity and structure–selectivity correlations. Antimicrobial Agents and Chemotherapy 45: 32933303.Google Scholar
O'Donoghue, PJ (1995) Cryptosporidium and Cryptosporidiosis in man and animals. International Journal for Parasitology 25: 139195.Google Scholar
Okhuysen, PC and Chappell, CL (2002) Cryptosporidium virulence determinants: are we there yet. International Journal for Parasitology 32: 517525.Google Scholar
Olson, GB and Wostmann, BS (1966) Lymphocytopoiesis, plasmacytopoiesis and cellular proliferation in nonantigenically stimulated germfree mice. Journal of Immunology 97: 267274.Google Scholar
Ong, CSL, Eisler, DL, Alikhani, A, Fung, VKW, Tomblin, J, Bowie, WR and Isaac-Renton, JL (2002) Novel Cryptosporidium genotypes in sporadic cryptosporidiosis cases: first report of human infections with a cervine genotype. Emerging Infectious Diseases 8: 263268.Google Scholar
Pasquali, P, Fayer, R, Almeria, S, Trout, J, Polidori, GA and Gasbarre, LC (1997) Lymphocyte dynamic patterns in cattle during a primary infection with Cryptosporidium parvum. Journal of Parasitology 83: 247250.Google Scholar
Peeters, JE, Villacorta, I, Vanopdenbosch, E, Vandergheynst, D, Naciri, M, Ares-Mazas, E and Yvore, P (1992) Cryptosporidium parvum in calves: Kinetics and immunoblot analysis of specific serum and local antibody responses (Immunoglobulin A [IgA], IgG, and IgM) after natural and experimental infections. Infection and Immunity 60: 23092316.Google Scholar
Peng, MM, Xiao, L, Freeman, AR, Arrowood, MJ, Escalante, AA, Weltman, AC, Ong, CSL, MacKenzie, WR, Lal, AA and Beard, C (1997) Genetic polymorphism among Cryptosporidium parvum isolates: evidence of two distinct human transmission cycles. Emerging Infectious Diseases 3: 567573.Google Scholar
Perryman, LE, Kapil, SJ, Jones, ML and Hunt, EL (1999) Protection of calves against cryptosporidiosis with immune bovine colostrum induced by a Cryptosporidium parvum recombinant protein. Vaccine 17: 21422149.Google Scholar
Quaroni, A (1985) Pre- and postnatal development of differentiated functions in rat intestinal epithelial cells. Developmental Biology 111: 280292.Google Scholar
Que, JU and Hentges, DJ (1985) Effect of Streptomycin administration on colonization resistance to Salmonella typhimurium in mice. Infection and Immunity 48: 169174.CrossRefGoogle ScholarPubMed
Riggs, MW (1997) Immunology: host response and development of passive immunotherapy and vaccines. In: Fayer, R (ed.), Crytosporidium and cryptosporidiosis. Boca Raton: CRC Press, pp. 129162.Google Scholar
Riggs, MW (2002) Recent advances in cryptosporidiosis: the immune response. Microbes and Infection 4: 10671080.Google Scholar
Sacco, RE, Haynes, JS, Harp, JA, Waters, WR and Wannemuehler, MJ (1998) Cryptosporidium parvum initiates inflammatory bowel disease in germfree T cell receptor-alpha-deficient mice. American Journal of Pathology 153: 17171722.Google Scholar
Sagodira, S, Buzoni-Gatel, D, Iochmann, S, Naciri, M and Bout, D (1999) Protection of kids against Cryptosporidium parvum infection after immunization of dams with CP15-DNA. Vaccine 17: 23462355.Google Scholar
Savage, DC, Dubos, R and Schaedler, RW (1968) The gastrointestinal epithelium and its autochthonous bacterial flora. Journal of Experimental Medicine 127: 6775.CrossRefGoogle ScholarPubMed
Sherwood, D, Angus, KW, Snodgrass, DR and Tzipori, S (1982) Experimental cryptosporidiosis in laboratory mice. Infection and Immunity 38: 471475.Google Scholar
Sonea, IM, Palmer, MV, Akili, D and Harp, JA (2002) Treatment with neurokinin-1 receptor antagonist reduces severity of inflammatory bowel disease induced by Cryptosporidium parvum. Clinical and Diagnostic Laboratory Immunology 9: 333340.Google ScholarPubMed
Teunis, PFM, Chappell, CL and Okhuysen, PC (2002) Cryptosporidium dose response studies: variation between isolates. Risk Analysis 22: 175183.Google Scholar
Thea, DM, Pereira, MEA, Kotler, D, Sterling, CR and Keusch, GT (1992) Identification and partial purification of a lectin on the surface of the sporozoite of Cryptosporidium parvum. Journal of Parasitology 78: 886893.Google Scholar
Theodos, CM (1998) Innate and cell-mediated immune responses to Cryptosporidium parvum. In: Tzipori, S (ed.), Opportunistic Protozoa in Humans, Vol. 40. New York: Academic Press, pp. 87119.Google Scholar
Ungar, BLP, Burris, JA, Quinn, CA and Finkelman, FD (1990) New mouse models for chronic Cryptosporidium infection in immunodeficient hosts. Infection and Immunity 58: 961969.Google Scholar
Ungar, BLP, Kao, T-C, Burris, JA and Finkelman, FD (1991) Cryptosporidium infection in an adult mouse model. Independent roles for IFN-gamma and CD4+ T lymphocytes in protective immunity. Journal of Immunology 147: 10141022.Google Scholar
Urban, JF, Fayer, R, Chen, S-J, Gause, WC, Gately, MK and Finkelman, FD (1996) Il-12 protects immunocompetent and immunodeficient neonatal mice against infection with Cryptosporidium parvum. Journal of Immunology 156: 263268.Google Scholar
Waters, WR and Harp, JA (1996) Cryptosporidium parvum infection in T-cell receptor (TCR)-alpha- and TCR-delta-deficient mice. Infection and Immunity 64: 18541857.Google Scholar
Waters, WR, Harp, JA, Wannemuehler, MJ, Carbajal, NY and Casas, IA (1999) Effects of Lactobacillus reuteri on Cryptosporidium parvum infection of gnotobiotic TCR-alpha-deficient mice. Journal of Eukaryotic Microbiology 46: 6061S.Google Scholar
Wherry, JC, Schreiber, RD and Unanue, ER (1991) Regulation of gamma interferon production by natural killer cells in SCID mice: Roles of tumor necrosis factor and bacterial stimuli. Infection and Immunity 59: 17091715.Google Scholar
Whitmire, WM and Harp, JA (1991) Characterization of bovine cellular and serum antibody responses during infection by Cryptosporidium parvum. Infection and Immunity 59: 990995.Google Scholar
Wyatt, CR, Brackett, EJ, Perryman, LE, Rice-Ficht, AC, Brown, WC and O'Rourke, KI (1997) Activation of intestinal intraepithelial T lymphocytes in calves infected with Cryptosporidium parvum. Infection and Immunity 65: 185190.Google Scholar
Wyatt, CR, Brackett, EJ and Barrett, WJ (1999) Accumulation of mucosal T lymphocytes around epithelial cells after in vitro infection with Cryptosporidium parvum. Journal of Parasitology 85: 765768.Google Scholar
Wyatt, CR, Brackett, EJ and Savidge, J (2001) Evidence for the emergence of a type-1-like immune response in intestinal mucosa of calves recovering from cryptosporidiosis. Journal of Parasitology 87: 9095.Google Scholar
Xiao, L, Bern, C, Limor, J, Sulaiman, I, Roberts, J, Checkley, W, Cabrera, L, Gilman, RH and Lal, AA (2001) Identification of 5 types of Cryptosporidium parasites in children in Lima, Peru. Journal of Infectious Diseases 183: 492497.Google Scholar