Cryptosporidiosis as a zoonotic disease, a review

Authors

DOI:

https://doi.org/10.15517/am.2023.51759

Keywords:

coccidian, diarrhea, gatroenteritis, protozoan, virulence factors

Abstract

Introduction. Cryptosporidium spp. is a protozoan parasite belonging to the group of coccidia, causing diarrhea, gastroenteric, and respiratory disorders (less frequently) in different vertebrate species worldwide, primarily in young individuals. Objective. To document the most important virulence and pathogenic characteristics of Cryptosporidium spp., as well as the description of its genetic variants and its zoonotic potential. Development. There are more of 19 species of Cryptosporidium spp., with C. parvum (humans), C. bovis (cattle), C. suis (swine), and C. ubiquitum (birds) being noteworthy due to their high infectivity capacity, given by the diversity of their virulence factors. The parasite has an affinity for enterocytes and causes abnormalities in the intestinal absorption and secretory functions. Cryptosporidiosis varies depending on the host’s status (age, nutrition, and immunity), the source of contamination (water or ingestion), transmission, and hygiene. Diagnostic techniques range from conventional coproscopic tests to molecular biology tests. Conclusion. Factors such as the variability and virulence factors of Cryptosporidium spp. are considered mechanisms that favor the infection and spread of the parasite at an individual and group level in humans and domestic animals, as well as the complexity of its life cycle, resistance to environmental conditions, the infective capacity, and host interaction consolidate Cryptosporidium spp. as a zoonotic agent with significant economic effects.

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References

Agnamey, P., Sarfati, C., Pinel, C., Rabodoniriina, M., Kapel, N., Dutoit, E., Garnaud, C., Diouf, M., Garin, J., Totet, A., Derouin, F., & ANOFEL Cryptosporidium National Network. (2011). Evaluation of four commercial rapid immunochromatographic assays for detection of Cryptosporidium antigens in stool samples: A blind multicenter trial. Journal of Clinical Microbiology, 49(4), 1605–1607. https://doi.org/10.1128/JCM.02074-10

Alagappan, A., Bergquist, P. L., & Ferrari, B. C. (2009). Development of a two-color fluorescence in situ hybridization technique for species-level identification of human-infectious Cryptosporidium spp. Applied and Environmental Microbiology, 75(18), 5996–5998. https://doi.org/10.1128/AEM.00643-09

Alpert, G., Bell, L. M., Kirkpatrick, C. E., Budnick, L. D., Campos, J. M., Friedman, H. M., & Plotkin, S. A. (1986). Outbreak of cryptosporidiosis in a day-care center. Pediatrics, 77(2), 152–157. https://doi.org/10.1542/peds.77.2.152

Barker, I. K., & Carbonell, P. L. (1974). Cryptosporidium agni sp.n. From lambs, and Cryptosporidium bovis sp.n. from a calf, with observations on the oocyst. Zeitschrift Für Parasitenkunde, 44(4), 289–298. https://doi.org/10.1007/BF00366112

Baroudi, D., Khelef, D., Goucem, R., Adjou, K. T., Adamu, H., Zhang, H., & Xiao, L. (2013). Common occurrence of zoonotic pathogen Cryptosporidium meleagridis in broiler chickens and turkeys in Algeria. Veterinary Parasitology, 196(3–4), 334–340. https://doi.org/10.1016/j.vetpar.2013.02.022

Barr, S. C., Jamrosz, G. F., Hornbuckle, W. E., Bowman, D. D., & Fayer, R. (1994). Use of paromomycin for treatment of cryptosporidiosis in a cat. Journal of the American Veterinary Medical Association, 205(12), 1742–1743.

Baxby, D., Blundell, N., & Hart, C. A. (1984). The development and performance of a simple, sensitive method for the detection of Cryptosporidium oocysts in faeces. Epidemiology & Infection, 93(2), 317–323. https://doi.org/10.1017/S0022172400064858

Borowski, H., Thompson, R. C. A., Armstrong, T., & Clode, P. L. (2010). Morphological characterization of Cryptosporidium parvum life-cycle stages in an in vitro model system. Parasitology, 137(1), 13–26. https://doi.org/10.1017/S0031182009990837

Boulter-Bitzer, J. I., Lee, H., & Trevors, J. T. (2007). Molecular targets for detection and immunotherapy in Cryptosporidium parvum. Biotechnology Advances, 25(1), 13–44. https://doi.org/10.1016/j.biotechadv.2006.08.003

Bouzid, M., Hunter, P. R., Chalmers, R. M., & Tyler, K. M. (2013). Cryptosporidium pathogenicity and virulence. Clinical Microbiology Reviews, 26(1), 115–134. https://doi.org/10.1128/CMR.00076-12

Bouzid, M., Kintz, E., & Hunter, P. R. (2018). Risk factors for Cryptosporidium infection in low and middle income countries: A systematic review and meta-analysis. PLoS Neglected Tropical Diseases, 12(6), Article e0006553. https://doi.org/10.1371/journal.pntd.0006553

Carey, C. M., Lee, H., & Trevors, J. T. (2004). Biology, persistence and detection of Cryptosporidium parvum and Cryptosporidium hominis oocyst. Water Research, 38(4), 818–862. https://doi.org/10.1016/j.watres.2003.10.012

Certad, G., Dupouy-Camet, J., Gantois, N., Hammouma-Ghelboun, O., Pottier, M., Guyot, K., Benamrouz, S., Osman, M., Delaire, B., Creusy, C., Viscogliosi, E., Dei-Cas, E., Aliouat-Denis, C. A., & Follet, J. (2015). Identification of Cryptosporidium species in fish from Lake Geneva (Lac Léman) in France. PLoS ONE, 10(7), Article e0133047. https://doi.org/10.1371/journal.pone.0133047

Certad, G., Viscogliosi, E., Chabé, M., & Cacciò, S. M. (2017). Pathogenic mechanisms of Cryptosporidium and Giardia. Trends in Parasitology, 33(7), 561–576. https://doi.org/10.1016/j.pt.2017.02.006

Cevallos, A. M., Bhat, N., Verdon, R., Hamer, D. H., Stein, B., Tzipori, S., Pereira, M. E. A., Keusch, G. T., & Ward, H. D. (2000). Mediation of Cryptosporidium parvum infection in vitro by mucin-like glycoproteins defined by a neutralizing monoclonal antibody. Infection and Immunity, 68(9), 5167–5175. https://doi.org/10.1128/IAI.68.9.5167-5175.2000

Chalmers, R. M., & Davies, A. P. (2010). Minireview: Clinical cryptosporidiosis. Experimental Parasitology, 124(1), 138–146. https://doi.org/10.1016/j.exppara.2009.02.003

Chalmers, R. M., & Giles, M. (2010). Zoonotic cryptosporidiosis in the UK – challenges for control. Journal of Applied Microbiology, 109(5), 1487–1497. https://doi.org/10.1111/j.1365-2672.2010.04764.x

Chatterjee, A., Banerjee, S., Steffen, M., O’Connor, R. M., Ward, H. D., Robbins, P. W., & Samuelson, J. (2010). Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall. Eukaryotic Cell, 9(1), 84–96. https://doi.org/10.1128/EC.00288-09

Chen, X. -M., Gores, G. J., Paya, C. V., & LaRusso, N. F. (1999). Cryptosporidium parvum induces apoptosis in biliary epithelia by a Fas/Fas ligand-dependent mechanism. The American Journal of Physiology, 277(3), 599–608. https://doi.org/10.1152/ajpgi.1999.277.3.G599

Chen, X. -M., O’Hara, S. P., Huang, B. Q., Nelson, J. B., Lin, J. J. -C., Zhu, G., Ward, H. D., & LaRusso, N. F. (2004). Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infection and Immunity, 72(12), 6806–6816. https://doi.org/10.1128/IAI.72.12.6806-6816.2004

Chvala, S., Fragner, K., Hackl, R., Hess, M., & Weissenböck, H. (2006). Cryptosporidium infection in domestic geese (Anser anser f. domestica) detected by in-situ hybridization. Journal of Comparative Pathology, 134(2–3), 211–218. https://doi.org/10.1016/j.jcpa.2005.11.002

Clavel, A., Arnal, A. C., Sánchez, E. C., Castillo, F. J., Varea, M., Gómez-Lus, R., Cuesta, J., Letona, S., & Amiguet, J. A. (1996). Respiratory cryptosporidiosis: Case series and review of the literature. Infection, 24(5), 341–346. https://doi.org/10.1007/BF01716076

Connor, E. E., Wall, E. H., Bravo, D. M., Evock-Clover, C. M., Elsasser, T. H., Baldwin, R. L., Santín, M., Vinyard, B. T., Kahl, S., & Walker, M. P. (2017). Reducing gut effects from Cryptosporidium parvum infection in dairy calves through prophylactic glucagon-like peptide 2 therapy or feeding of an artificial sweetener. Journal of Dairy Science, 100(4), 3004–3018. https://doi.org/10.3168/jds.2016-11861

Current, W. L., & Reese, N. C. (1986). A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. The Journal of Protozoology, 33(1), 98–108. https://doi.org/10.1111/j.1550-7408.1986.tb05567.x

De, A. (2013). Current laboratory diagnosis of opportunistic enteric parasites in human immunodeficiency virus-infected patients. Tropical Parasitology, 3(1), 7–16. https://journals.lww.com/tpar/Fulltext/2013/03010/Current_laboratory_diagnosis_of_opportunistic.3.aspx

Del Coco, V. F., Córdoba, M. A., & Basualdo, J. A. (2008). Cryptosporidium infection in calves from a rural area of Buenos Aires, Argentina. Veterinary Parasitology, 158(1–2), 31–35. https://doi.org/10.1016/j.vetpar.2008.08.018

Díaz-Lee, A., Mercado, R., Onuoha, E. O., Ozaki, L. S., Muñoz, P., Muñoz, V., Martínez, F. G., & Fredes, F. (2011). Cryptosporidium parvum in diarrheic calves detected by microscopy and identified by immunochromatographic and molecular methods. Veterinary Parasitology, 176(2–3), 139–144. https://doi.org/10.1016/j.vetpar.2010.11.001

Dillingham, R. A., Lima, A. A., & Guerrant, R. L. (2002). Cryptosporidiosis: Epidemiology and impact. Microbes and Infection, 4(10), 1059–1066. https://doi.org/10.1016/S1286-4579(02)01630-1

Dowle, M., Hill, N. J., & Power, M. L. (2013). Cryptosporidium from a free-ranging marsupial host: Bandicoots in urban Australia. Veterinary Parasitology, 198(1–2), 197–200. https://doi.org/10.1016/j.vetpar.2013.08.017

Drinkard, L. N., Halbritter, A., Nguyen, G. T., Sertich, P. L., King, M., Bowman, S., Huxta, R., & Guagenti, M. (2015). Outbreak of Cryptosporidiosis among veterinary medicine students—Philadelphia, Pennsylvania, February 2015. MMWR. Morbidity and Mortality Weekly Report, 64(28), Article 773. https://doi.org/10.15585/mmwr.mm6428a7

Fayer, R., Trout, J. M., Xiao, L., Morgan, U. M., Lal, A. A., & Dubey, J. P. (2001). Cryptosporidium canis n. sp. from domestic dogs. The Journal of Parasitology, 87(6), 1415–1422. https://doi.org/10.1645/0022-3395(2001)087[1415:CCNSFD]2.0.CO;2

Fayer, R. (2004). Cryptosporidium: A water-borne zoonotic parasite. Veterinary Parasitology, 126(1–2), 37–56. https://doi.org/10.1016/j.vetpar.2004.09.004

Feng, Y., Dearen, T., Cama, V., & Xiao, L. (2009). 90-Kilodalton heat shock protein, Hsp90, as a target for genotyping Cryptosporidium spp. known to infect humans. Eukaryotic Cell, 8(4), 478–482. https://doi.org/10.1128/EC.00294-08

Feng, Y., Ryan, U. M., & Xiao, L. (2018). Genetic Diversity and Population Structure of Cryptosporidium. Trends in Parasitology, 34(11), 997–1011. https://doi.org/10.1016/j.pt.2018.07.009

Foreyt, W. J. (1990). Coccidiosis and Cryptosporidiosis in sheep and goats. Veterinary Clinics of North America: Food Animal Practice, 6(3), 655–670. https://doi.org/10.1016/S0749-0720(15)30838-0

Garcia, L. S. (2016). Diagnostic medical parasitology (6th ed.). American Society of Microbiology. https://doi.org/10.1128/9781555819002

Garber, L. P., Salman, M. D., Hurd, H.S., Keefe, T., & Schlater, J. L. (1994). Potential risk factors for Cryptosporidium infection in dairy calves. Journal of the American Veterinary Medical Association, 205(1), 86–91.

Garro, C. J., Morici, G. E., Utgés, M. E., Tomazic, M. L., & Schnittger, L. (2016). Prevalence and risk factors for shedding of Cryptosporidium spp. Oocysts in dairy calves of Buenos Aires Province, Argentina. Parasite Epidemiology and Control, 1(2), 36–41. https://doi.org/10.1016/j.parepi.2016.03.008

Gerace, E., Lo Presti, V. D. M., & Biondo, C. (2019). Cryptosporidium infection: epidemiology, pathogenesis, and differential diagnosis. European Journal of Microbiology & Immunology, 9(4), 119–123. https://doi.org/10.1556/1886.2019.00019

Gharpure, R., Perez, A., Miller, A. D., Wikswo, M. E., Silver, R., & Hlavsa, M. C. (2019). Cryptosporidiosis outbreaks—United States, 2009–2017. Morbidity and Mortality Weekly Report, 68(25), 568–572. https://doi.org/10.15585%2Fmmwr.mm6825a3

Gu, Y., Wang, X., Zhou, C., Li, P., Xu, Q., Zhao, C., Liu, W., & Xu, W. (2016). Investigation on Cryptosporidium infections in wild animals in a zoo in anhui province. Journal of Zoo and Wildlife Medicine, 47(3), 846–854. https://doi.org/10.1638/2015-0301.1

Guselle, N. J., Appelbee, A. J., & Olson, M. E. (2003). Biology of Cryptosporidium parvum in pigs: From weaning to market. Veterinary Parasitology, 113(1), 7–18. https://doi.org/10.1016/S0304-4017(03)00039-6

Hachich, E. M., Sato, M. I. Z., Galvani, A. T., Menegon, J. R. N., & Mucci, J. L. N. (2004). Giardia and Cryptosporidium in source waters of São Paulo State, Brazil. Water Science and Technology, 50(1), 239–245. https://doi.org/10.2166/wst.2004.0061

Hernández-Gallo, N., Hernández-Flórez, L. J., & Cortés-Vecino, J. A. (2018). Criptosporidiosis y «Una Salud». Revista de Salud Pública, 20(1), 138–143. https://doi.org/10.15446/rsap.V20n1.69959

Higgins, J. A., Fayer, R., Trout, J. M., Xiao, L., Lal, A. A., Kerby, S., & Jenkins, M. C. (2001). Real-time PCR for the detection of Cryptosporidium parvum. Journal of Microbiological Methods, 47(3), 323–337. https://doi.org/10.1016/S0167-7012(01)00339-6

Hunter, P. L., & Nichols, G. (2002). Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clinical Microbiology Reviews, 15(1), 145–154. https://doi.org/10.1128/cmr.15.1.145-154.2002

Hunter, P. R., Hadfield, S. J., Wilkinson, D., Lake, I. R., Harrison, F. C. D., & Chalmers, R. M. (2007). Correlation between Subtypes of Cryptosporidium parvum in Humans and Risk. Emerging Infectious Diseases, 13(1), 82–88. https://doi.org/10.3201%2Feid1301.060481

Jian, F., Qi, M., He, X., Wang, R., Zhang, S., Dong, H., & Zhang, L. (2014). Occurrence and molecular characterization of Cryptosporidium in dogs in Henan province, China. BMC Veterinary Research, 10, Article 26. https://doi.org/10.1186/1746-6148-10-26

Joe, A., Hamer, D. H., Kelley, M. A., Pereira, M. E., Keusch, G. T., Tzipori, S., & Ward, H. D. (1994). Role of a Gal/GalNAc-specific sporozoite surface lectin in Cryptosporidium parvum-host cell interaction. The Journal of Eukaryotic Microbiology, 41(5), 44S.

Klein, P., Kleinová, T., Volek, Z., & Šimůnek, J. (2008). Effect of Cryptosporidium parvum infection on the absorptive capacity and paracellular permeability of the small intestine in neonatal calves. Veterinary Parasitology, 152(1–2), 53–59. https://doi.org/10.1016/j.vetpar.2007.11.020

Laurent, F., McCole, D., Eckmann, L., & Kagnoff, M. F. (1999). Pathogenesis of Cryptosporidium parvum infection. Microbes and Infection, 1(2), 141–148. https://doi.org/10.1016/S1286-4579(99)80005-7

Leitch, G. J., & He, Q. (2011). Cryptosporidiosis-an overview. Journal of Biomedical Research, 25(1), 1–16. https://doi.org/10.1016/S1674-8301(11)60001-8

Lendner, M., & Daugschies, A. (2014). Cryptosporidium infections: Molecular advances. Parasitology, 141(11), 1511–1532. https://doi.org/10.1017/S0031182014000237

Limor, J. R., Lal, A. A., & Xiao, L. (2002). Detection and differentiation of cryptosporidium parasites that are pathogenic for humans by real-time PCR. Journal of Clinical Microbiology, 40(7), 2335–2338. https://doi.org/10.1128/JCM.40.7.2335-2338.2002

Liu, J., Enomoto, S., Lancto, C. A., Abrahamsen, M. S., & Rutherford, M. S. (2008). Inhibition of apoptosis in Cryptosporidium parvum-infected intestinal epithelial cells is dependent on survivin. Infection and Immunity, 76(8), 3784–3792. https://doi.org/10.1128/IAI.00308-08

Lougaris, V., Raffaele B., Ferrari S., & Plenaby A. (2005). Hyper immunoglobulin M syndrome due to CD40 deficiency: clinical, molecular, and immunological features. Immunological Reviews, 203(1), 48–66. https://doi.org/10.1111/j.0105-2896.2005.00229.x

Luo, X., Jedlicka, S., & Jellison, K. (2016). Pseudo-second-order calcium-mediated Cryptosporidium parvum oocyst attachment to environmental biofilms. Applied and Environmental Microbiology, 83(1), article e02339-16. https://doi.org/10.1128/AEM.02339-16

Majeed, Q. A. H., El-Azazy, O. M. E., Abdou, N.-E. M. I., Al-Aal, Z. A., El-Kabbany, A. I., Tahrani, L. M. A., AlAzemi, M. S., Wang, Y., Feng, Y., & Xiao, L. (2018). Epidemiological observations on cryptosporidiosis and molecular characterization of Cryptosporidium spp. In sheep and goats in Kuwait. Parasitology Research, 117(5), 1631–1636. https://doi.org/10.1007/s00436-018-5847-1

Mason, R. W., Hartley, W. J., & Tilt, L. (1981). Intestinal cryptosporidiosis in a kid goat. Australian Veterinary Journal, 57(8), 386–388. https://doi.org/10.1111/j.1751-0813.1981.tb00529.x

Maurya, P. S., Rakesh, R. L., Pradeep, B., Kumar, S., Kundu, K., Garg, R., Ram, H., Kumar, A., & Banerjee, P. S. (2013). Prevalence and risk factors associated with Cryptosporidium spp. infection in young domestic livestock in India. Tropical Animal Health and Production, 45(4), 941–946. https://doi.org/10.1007/s11250-012-0311-1

McNabb, S. J., Hensel, D. M., Welch, D. F., Heijbel, H., McKee, G. L., & Istre, G. R. (1985). Comparison of sedimentation and flotation techniques for identification of Cryptosporidium sp. oocysts in a large outbreak of human diarrhea. Journal of Clinical Microbiology, 22(4), 587–589. https://doi.org/10.1128/jcm.22.4.587-589.1985

Meinhardt, P. L., Casemore, D. P., & Miller, K. B. (1996). Epidemiologic aspects of human cryptosporidiosis and the role of waterborne transmission. Epidemiologic Reviews, 18(2), 118–136. https://doi.org/10.1093/oxfordjournals.epirev.a017920

Meireles, M. V. (2010). Cryptosporidium infection in Brazil: Implications for veterinary medicine and public health. Revista Brasileira De Parasitologia Veterinaria, 19(4), 197–204. https://doi.org/10.1590/s1984-29612010000400002

Mirhashemi, M. E., Zintl, A., Grant, T., Lucy, F. E., Mulcahy, G., & De Waal, T. (2015). Comparison of diagnostic techniques for the detection of Cryptosporidium oocysts in animal samples. Experimental Parasitology, 151-152, 14–20. https://doi.org/10.1016/j.exppara.2015.01.018

Mohteshamuddin, K., Hamdan, L., AlKaabi, A. B., & Barigye, R. (2020). Cryptosporidium parvum and other enteric pathogens in scouring neonatal dairy calves from the Al Ain region, United Arab Emirates. Veterinary Parasitology, Regional Studies and Reports, 21, Article 100435. https://doi.org/10.1016/j.vprsr.2020.100435

Morgan, U. M., Pallant, L., Dwyer, B. W., Forbes, D. A., Rich, G., & Thompson, R. C. A. (1998). Comparison of PCR and microscopy for detection of Cryptosporidium parvum in Human fecal specimens: Clinical trial. Journal of Clinical Microbiology, 36(4), 995–998. https://doi.org/10.1128/JCM.36.4.995-998.1998

Mtambo, M. M., Nash, A. S., Blewett, D. A., Smith, H. V., & Wright, S. (1991). Cryptosporidium infection in cats: Prevalence of infection in domestic and feral cats in the Glasgow area. The Veterinary Record, 129(23), 502–504.

Muadica, A. S., Balasegaram, S., Beebeejaun, K., Köster, P. C., Bailo, B., Hernández-de-Mingo, M., Dashti, A., Dacal, E., Saugar, J. M., Fuentes, I., & Carmena, D. (2021). Risk associations for intestinal parasites in symptomatic and asymptomatic schoolchildren in central Mozambique. Clinical Microbiology and Infection, 27(4), 624–629. https://doi.org/10.1016/j.cmi.2020.05.031

Murakoshi, F., Xiao, L., Matsubara, R., Sato, R., Kato, Y., Sasaki, T., Fukuda, Y., Tada, C., & Nakai, Y. (2012). Molecular characterization of Cryptosporidium spp. in grazing beef cattle in Japan. Veterinary Parasitology, 187(1–2), 123–128. https://doi.org/10.1016/j.vetpar.2011.12.011

Nava, S., White, A. C., & Castellanos-González, A. (2019). Cryptosporidium parvum subtilisin-like serine protease (SUB1) is crucial for parasite egress from host cells. Infection and Immunity, 87(5), e00784–18. https://doi.org/10.1128/IAI.00784-18

O’Connor, R. M., Wanyiri, J. W., Cevallos, A. M., Priest, J. W., & Ward, H. D. (2007). Cryptosporidium parvum glycoprotein gp40 localizes to the sporozoite surface by association with gp15. Molecular and Biochemical Parasitology, 156(1), 80–83. https://doi.org/10.1016/j.molbiopara.2007.07.010

Okhuysen, P. C., & Chappell, C. L. (2002). Cryptosporidium virulence determinants – are we there yet? International Journal for Parasitology, 32(5), 517–525. https://doi.org/10.1016/S0020-7519(01)00356-3

Pakdad, K., Nasab, S. D. M., Damraj, F. -A., & Ahmadi, N. A. (2018). Comparing the efficiency of four diagnostic concentration techniques performed on the same group of intestinal parasites. Alexandria Journal of Medicine, 54(4), 495–501. https://doi.org/10.1016/j.ajme.2017.11.005

Perez-Cordon, G., Nie, W., Schmidt, D., Tzipori, S., & Feng, H. (2011). Involvement of host calpain in the invasion of Cryptosporidium parvum. Microbes and Infection, 13(1), 103–107. https://doi.org/10.1016/j.micinf.2010.10.007

Pohjola, S., Jokipii, L., & Jokipii, A. M. (1985). Dimethylsulphoxide-Ziehl-Neelsen staining technique for detection of cryptosporidial oocysts. The Veterinary Record, 116(16), 442–443.

Quiroz, E. S., Bern, C., MacArthur, J. R., Xiao, L., Fletcher, M., Arrowood, M. J., Shay, D. K., Levy, E. E., Glass, R. I., & Lal, A. (2000). An outbreak of cryptosporidiosis linked to a foodhandler. The Journal of Infectious Diseases, 181(2), 695–700. https://doi.org/10.1086/315279

Reid, A., Lymbery, A., Ng, J., Tweedle, S., & Ryan, U. (2010). Identification of novel and zoonotic Cryptosporidium species in marine fish. Veterinary Parasitology, 168(3-4), 190–195. https://doi.org/10.1016/j.vetpar.2009.11.015

Reza Momeni, H. (2011). Role of calpain in apoptosis. Review article. Cell Journal (Yakhteh), 13(2), 65–72. https://www.celljournal.org/article_250071.html

Robertson, L. J., Björkman, C., Axén, C., & Fayer, R. (2014). Cryptosporidiosis in farmed animals. In S. M. Cacciò, & G. Widmer (Eds.), Cryptosporidium: Parasite and disease (pp. 149–235). Springer. https://doi.org/10.1007/978-3-7091-1562-6_4

Robinson, G., & Chalmers, R. M. (2010). The European rabbit (Oryctolagus cuniculus), a source of zoonotic cryptosporidiosis. Zoonoses and Public Health, 57(7–8), e1-e13. https://doi.org/10.1111/j.1863-2378.2009.01308.x

Rose, J. B. (1997). Environmental ecology of Cryptosporidium and public health implications. Annual Review of Public Health, 18, 135–161. https://doi.org/10.1146/annurev.publhealth.18.1.135

Rotz, L. D., Khan, A. S., Lillibridge, S. R., Ostroff, S. M., & Hughes, J. M. (2002). Public Health Assessment of Potential Biological Terrorism Agents. Emerging Infectious Diseases, 8(2), 225–230. https://doi.org/10.3201%2Feid0802.010164

Ryan, U., Fayer, R., & Xiao, L. (2014). Cryptosporidium species in humans and animals: Current understanding and research needs. Parasitology, 141(13), 1667–1685. https://doi.org/10.1017/S0031182014001085

Santin, M. (2020). Cryptosporidium and Giardia in ruminants. Veterinary Clinics of North America: Food Animal Practice, 36(1), 223–238. https://doi.org/10.1016/j.cvfa.2019.11.005

Sarkhosh, T., Zhang, X. F., Jellison, K. L., & Jedlicka, S. S. (2019). Calcium-mediated biophysical binding of Cryptosporidium parvum oocysts to surfaces is sensitive to oocyst age. Applied and Environmental Microbiology, 85(17), Article e00816-19. https://doi.org/10.1128/AEM.00816-19

Sasahara, T., Maruyama, H., Aoki, M., Kikuno, R., Sekiguchi, T., Takahashi, A., Maruyama, H., Aoki, M., & Inoue, M. (2003). Apoptosis of intestinal crypt epithelium after Cryptosporidium parvum infection. Journal of Infection and Chemotherapy, 9(3), 278–281. https://doi.org/10.1007/s10156-003-0259-1

Shahbazi, P., Aligolzadeh, A., Khordadmehr, M., Hashemzadeh Farhang, H., & Katiraee, F. (2020). Molecular study and genotyping of Cryptosporidium baileyi and Cryptosporidium parvum from free-range and commercial broiler chickens in Guilan province, Iran. Comparative Immunology, Microbiology and Infectious Diseases, 69, Article 101411. https://doi.org/10.1016/j.cimid.2019.101411

Snelling, W. J., Xiao, L., Ortega-Pierres, G., Lowery, C. J., Moore, J. E., Rao, J. R., Smyth, S., Millar, B. C., Rooney, P. J., Matsuda, M., Kenny, F., Xu, J., & Dooley, J. S. G. (2007). Cryptosporidiosis in developing countries. Journal of Infection in Developing Countries, 1(3), 242–256. https://doi.org/10.3855/jidc.360

Sparks, H., Nair, G., Castellanos-Gonzalez, A., & White, A. C. (2015). Treatment of Cryptosporidium: What we know, gaps, and the way forward. Current Tropical Medicine Reports, 2(3), 181–187. https://doi.org/10.1007/s40475-015-0056-9

Sréter, T., Kovács, G., da Silva, A. J., Pieniazek, N. J., Széll, Z., Dobos-Kovács, M., Márialigeti, K., & Varga, I. (2000). Morphologic, Host Specificity, and Molecular Characterization of a Hungarian Cryptosporidium meleagridis Isolate. Applied and Environmental Microbiology, 66(2), 735–738. https://doi.org/10.1128/AEM.66.2.735-738.2000

Tandel, J., English, E. D., Sateriale, A., Gullicksrud, J. A., Beiting, D. P., Sullivan, M. C., Pinkston, B., & Striepen, B. (2019). Life cycle progression and sexual development of the apicomplexan parasite Cryptosporidium parvum. Nature Microbiology, 4(12), 2226–2236. https://doi.org/10.1038/s41564-019-0539-x

Thompson, R. C. A., Koh, W. H., & Clode, P. L. (2016). Cryptosporidium—What is it? Food and Waterborne Parasitology, 4, 54–61. https://doi.org/10.1016/j.fawpar.2016.08.004

Tzipori, S., & Ward, H. (2002). Cryptosporidiosis: Biology, pathogenesis and disease. Microbes and Infection, 4(10), 1047–1058. https://doi.org/10.1016/S1286-4579(02)01629-5

Uga, S., Matsuo, J., Kono, E., Kimura, K., Inoue, M., Rai, S. K., & Ono, K. (2000). Prevalence of Cryptosporidium parvum infection and pattern of oocyst shedding in calves in Japan. Veterinary Parasitology, 94(1-2), 27–32. https://doi.org/10.1016/S0304-4017(00)00338-1

Ursini, T., Moro, L., Requena-Méndez, A., Bertoli, G., & Buonfrate, D. (2020). A review of outbreaks of cryptosporidiosis due to unpasteurized milk. Infection, 48(5), 659–663. https://doi.org/10.1007/s15010-020-01426-3

Vanathy, K., Parija, S. C., Mandal, J., Hamide, A., & Krishnamurthy, S. (2017). Detection of Cryptosporidium in stool samples of immunocompromised patients. Tropical Parasitology, 7(1), 41–46. https://journals.lww.com/tpar/Fulltext/2017/07010/Detection_of_Cryptosporidium_in_stool_samples_of.8.aspx

Verweij, J. J., Blangé, R. A., Templeton, K., Schinkel, J., Brienen, E. A. T., van Rooyen, M. A. A., van Lieshout, L., & Polderman, A. M. (2004). Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. Journal of Clinical Microbiology, 42(3), 1220–1223. https://doi.org/10.1128/JCM.42.3.1220-1223.2004

Vieira, L. S., Silva, M. B., Tolentino, A. C., Lima, J. D., & Silva, A. C. (1997). Outbreak of cryptosporidiosis in dairy goats in Brazil. The Veterinary Record, 140(16), 427–428. https://doi.org/10.1136/vr.140.16.427

Xiao, L., Bern, C., Arrowood, M., Sulaiman, I., Zhou, L., Kawai, V., Vivar, A., Lal, A. A., & Gilman, R. H. (2002). Identification of the cryptosporidium pig genotype in a human patient. The Journal of Infectious Diseases, 185(12), 1846–1848. https://doi.org/10.1086/340841

Xiao, L., & Fayer, R. (2008). Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. International Journal for Parasitology, 38(11), 1239–1255. https://doi.org/10.1016/j.ijpara.2008.03.006

Xiao, L., Sulaiman, I. M., Ryan, U. M., Zhou, L., Atwill, E. R., Tischler, M. L., Zhang, X., Fayer, R., & Lal, A. A. (2002). Host adaptation and host–parasite co-evolution in Cryptosporidium: Implications for taxonomy and public health. International Journal for Parasitology, 32(14), 1773–1785. https://doi.org/10.1016/S0020-7519(02)00197-2

Yalda Lucero, A. (2014). Etiología y manejo de la gastroenteritis aguda infecciosa en niños y adultos. Revista Médica Clínica Las Condes, 25(3), 463–472. https://doi.org/10.1016/S0716-8640(14)70063-X

Yimming, B., Pattanatanang, K., Sanyathitiseree, P., Inpankaew, T., Kamyingkird, K., Pinyopanuwat, N., Chimnoi, W., & Phasuk, J. (2016). Molecular identification of Cryptosporidium species from pet snakes in Thailand. The Korean Journal of Parasitology, 54(4), 423–429. https://doi.org/10.3347%2Fkjp.2016.54.4.423

Yoder, J. S., Beach, M. J. (2010). Cryptosporidium surveillance and risk factors in the United States. Experimental Parasitology, 124(1), 31–39. https://doi.org/10.1016/j.exppara.2009.09.020

Zahedi, A., Paparini, A., Jian, F., Robertson, I., & Ryan, U. (2016). Public health significance of zoonotic Cryptosporidium species in wildlife: Critical insights into better drinking water management. International Journal for Parasitology: Parasites and Wildlife, 5(1), 88–109. https://doi.org/10.1016/j.ijppaw.2015.12.001

Zhang, Q., Li, J., Li, Z., Xu, C., Hou, M., & Qi, M. (2020). Molecular identification of Cryptosporidium spp. in alpacas (Vicugna pacos) in China. International Journal for Parasitology: Parasites and Wildlife, 12, 181–184. https://doi.org/10.1016/j.ijppaw.2020.06.007

Published

2023-07-12

How to Cite

Ramírez-Navarro, V., Lopera-Vásquez, R., & Rodríguez-Gutiérrez, V. (2023). Cryptosporidiosis as a zoonotic disease, a review. Agronomía Mesoamericana, 34(3), 51759. https://doi.org/10.15517/am.2023.51759