Hostname: page-component-7857688df4-74lm6 Total loading time: 0 Render date: 2025-11-12T10:34:47.586Z Has data issue: false hasContentIssue false
  • English
  • Français

The global prevalence of Cryptosporidium in sheep: a systematic review and meta-analysis

Published online by Cambridge University Press:  24 August 2022

Yuancai Chen ,
Huikai Qin ,
Jianying Huang ,
Junqiang Li  and
Longxian Zhang Open the ORCID record for Longxian Zhang [Opens in a new window]
Yuancai Chen
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Huikai Qin
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Jianying Huang
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Junqiang Li
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Longxian Zhang*
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
*
Author for correspondence: Longxian Zhang, E-mail: zhanglx8999@henau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Cryptosporidium spp. are important pathogens with some species causing diarrhoea in humans and animals. Sheep are one of the most common potential hosts for various Cryptosporidium spp. The prevalence of Cryptosporidium in sheep globally was evaluated from published information including molecular data via meta-analysis. In total, 126 datasets from 41 countries were included for final quantitative analysis. Sheep aged <3 months had a significantly higher prevalence (27.8%; 3284/11 938) than those at the age of 3–12 and >12 months. The prevalence of Cryptosporidium in sheep with diarrhoea of 35.4% (844/1915) was higher than in sheep that did not show diarrhoea (11.3%; 176/1691). Fourteen Cryptosporidium species/genotypes were detected in sheep globally. The proportion of subgenotype family XIIa of Cryptosporidium ubiquitum was 90.0% (216/240); the proportions of subgenotypes IIdA20G1 and IIaA15G2R1 of Cryptosporidium parvum were 15.4% (62/402) and 19.7% (79/402). The results indicate that C. parvum is the dominant species in Europe while Cryptosporidium xiaoi is the dominant species in Oceania, Asia and Africa and C. ubiquitum is the dominant species in North America and South America. Subgenotype family IIa of C. parvum is particularly widespread among sheep worldwide. The results highlight the role of sheep as a reservoir host for zoonotic cryptosporidia and the need for further study of prevalence, transmission and control of this pathogen in sheep.

Keywords

Cryptosporidiummeta-analysisprevalencesheep

Information

Type
Research Article
Information
Parasitology , Volume 149 , Issue 12 , October 2022 , pp. 1652 - 1665
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

Adamu, H, Petros, B, Zhang, G, Kassa, H, Amer, S, Ye, J and Xiao, L (2014) Distribution and clinical manifestations of Cryptosporidium species and subtypes in HIV/AIDS patients in Ethiopia. PLoS Neglected Tropical Diseases 8, e2831.CrossRefGoogle ScholarPubMed
Adeyemo, FE, Singh, G, Reddy, P and Stenstrom, TA (2018) Methods for the detection of Cryptosporidium and Giardia: from microscopy to nucleic acid based tools in clinical and environmental regimes. Acta Tropica 184, 15–28.CrossRefGoogle ScholarPubMed
Baroudi, D, Hakem, A, Adamu, H, Amer, S, Khelef, D, Adjou, K and Xiao, L (2018) Zoonotic Cryptosporidium species and subtypes in lambs and goat kids in Algeria. Parasites and Vectors 11, 582.CrossRefGoogle ScholarPubMed
Bordes, L, Houert, P, Costa, D, Favennec, L, Vial-Novella, C, Fidelle, F and Razakandrainibe, R (2020) Asymptomatic Cryptosporidium infections in ewes and lambs are a source of environmental contamination with zoonotic genotypes of Cryptosporidium parvum. Parasite 27, 57.CrossRefGoogle ScholarPubMed
Bouwknegt, M, Devleesschauwer, B, Graham, H, Robertson, LJ, van der Giessen, JW and The Euro-FBP Workshop Participants (2018) Prioritisation of food-borne parasites in Europe, 2016. Eurosurveillance 23, 17-00161.CrossRefGoogle ScholarPubMed
Casemore, DP (1989) Sheep as a source of human cryptosporidiosis. The Journal of Infection 19, 101–104.CrossRefGoogle ScholarPubMed
Chalmers, RM and Katzer, F (2013) Looking for Cryptosporidium: the application of advances in detection and diagnosis. Trends in Parasitology 29, 237–251.CrossRefGoogle ScholarPubMed
Checkley, W, White, AC Jr., Jaganath, D, Arrowood, MJ, Chalmers, RM, Chen, XM and Houpt, ER (2015) A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. The Lancet Infectious Diseases 15, 85–94.CrossRefGoogle ScholarPubMed
Dahmani, H, Ouchene, N, Dahmani, A, Ouchene-Khelifi, NA and Oumouna, M (2020) First report on Cryptosporidium parvum, Escherichia coli K99, rotavirus and coronavirus in neonatal lambs from north-center region, Algeria. Comparative Immunology, Microbiology and Infectious Diseases 73, 101567.CrossRefGoogle ScholarPubMed
Dessi, G, Tamponi, C, Varcasia, A, Sanna, G, Pipia, AP, Carta, S and Scala, A (2020) Cryptosporidium infections in sheep farms from Italy. Parasitology Research 119, 4211–4218.CrossRefGoogle ScholarPubMed
Díaz, P, Quilez, J, Chalmers, RM, Panadero, R, Lopez, C, Sanchez-Acedo, C and Diez-Banos, P (2010) Genotype and subtype analysis of Cryptosporidium isolates from calves and lambs in Galicia (NW Spain). Parasitology 137, 1187–1193.CrossRefGoogle ScholarPubMed
Díaz, P, Quílez, J, Prieto, A, Navarro, E, Pérez-Creo, A, Fernández, G and Morrondo, P (2015) Cryptosporidium species and subtype analysis in diarrhoeic pre-weaned lambs and goat kids from north-western Spain. Parasitology Research 114, 4099–4105.CrossRefGoogle ScholarPubMed
Díaz, P, Navarro, E, Prieto, A, Perez-Creo, A, Vina, M, Diaz-Cao, JM and Morrondo, P (2018) Cryptosporidium species in post-weaned and adult sheep and goats from N.W. Spain: public and animal health significance. Veterinary Parasitology 254, 1–5.CrossRefGoogle ScholarPubMed
Egger, M, Davey Smith, G, Schneider, M and Minder, C (1997) Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 315, 629–634.CrossRefGoogle ScholarPubMed
Feng, Y, Ryan, UM and Xiao, L (2018) Genetic diversity and population structure of Cryptosporidium. Trends in Parasitology 34, 997–1011.CrossRefGoogle ScholarPubMed
Firoozi, Z, Sazmand, A, Zahedi, A, Astani, A, Fattahi-Bafghi, A, Kiani-Salmi, N and Akrami-Mohajeri, F (2019) Prevalence and genotyping identification of Cryptosporidium in adult ruminants in central Iran. Parasites & Vectors 12, 510.CrossRefGoogle ScholarPubMed
Geurden, T, Thomas, P, Casaert, S, Vercruysse, J and Claerebout, E (2008) Prevalence and molecular characterisation of Cryptosporidium and Giardia in lambs and goat kids in Belgium. Veterinary Parasitology 155, 142–145.CrossRefGoogle ScholarPubMed
Goma, FY, Geurden, T, Siwila, J, Phiri, IGK, Gabriel, S, Claerebout, E and Vercruysse, J (2007) The prevalence and molecular characterisation of Cryptosporidium spp. in small ruminants in Zambia. Small Ruminant Research 72, 77–80.CrossRefGoogle Scholar
Guo, Y, Li, N, Ryan, U, Feng, Y and Xiao, L (2021) Small ruminants and zoonotic cryptosporidiosis. Parasitology Research 120, 4189–4198.CrossRefGoogle ScholarPubMed
Guyatt, GH, Oxman, AD, Vist, GE, Kunz, R, Falck-Ytter, Y, Alonso-Coello, P and Group GW (2008) GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. British Medical Journal 336, 924–926.CrossRefGoogle ScholarPubMed
Higuera, A, Villamizar, X, Herrera, G, Giraldo, JC, Vasquez, LR, Urbano, P and Ramirez, JD (2020) Molecular detection and genotyping of intestinal protozoa from different biogeographical regions of Colombia. Peerj 8, e8554.CrossRefGoogle ScholarPubMed
Hijjawi, N, Mukbel, R, Yang, R and Ryan, U (2016) Genetic characterization of Cryptosporidium in animal and human isolates from Jordan. Veterinary Parasitology 228, 116–120.CrossRefGoogle ScholarPubMed
Imre, K, Luca, C, Costache, M, Sala, C, Morar, A, Morariu, S and Darabus, G (2013) Zoonotic Cryptosporidium parvum in Romanian newborn lambs (Ovis aries). Veterinary Parasitology 191, 119–122.CrossRefGoogle ScholarPubMed
Kabir, MHB, Ceylan, O, Ceylan, C, Shehata, AA, Bando, H, Essa, MI and Kato, K (2020) Molecular detection of genotypes and subtypes of Cryptosporidium infection in diarrheic calves, lambs, and goat kids from Turkey. Parasitology International 79, 102163.CrossRefGoogle ScholarPubMed
Kaupke, A, Michalski, MM and Rzeżutka, A (2017) Diversity of Cryptosporidium species occurring in sheep and goat breeds reared in Poland. Parasitology Research 116, 871–879.CrossRefGoogle ScholarPubMed
Khan, A, Shaik, JS and Grigg, ME (2018) Genomics and molecular epidemiology of Cryptosporidium species. Acta Tropica 184, 1–14.CrossRefGoogle ScholarPubMed
Koinari, M, Lymbery, AJ and Ryan, UM (2014) Cryptosporidium species in sheep and goats from Papua New Guinea. Experimental Parasitology 141, 134–137.CrossRefGoogle ScholarPubMed
Kotkova, M, Nemejc, K, Sak, B, Hanzal, V, Kvetonova, D, Hlaskova, L and Kvac, M (2016) Cryptosporidium ubiquitum, C. muris and Cryptosporidium deer genotype in wild cervids and caprines in the Czech Republic. Folia Parasitologica 63, 2016.003.CrossRefGoogle ScholarPubMed
Kotloff, KL (2017) The burden and etiology of diarrheal illness in developing countries. Pediatric Clinics of North America 64, 799–814.CrossRefGoogle ScholarPubMed
Kotloff, KL, Nataro, JP, Blackwelder, WC, Nasrin, D, Farag, TH, Panchalingam, S and Levine, MM (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382, 209–222.CrossRefGoogle ScholarPubMed
Li, N, Xiao, LH, Alderisio, K, Elwin, K, Cebelinski, E, Chalmers, R and Feng, YY (2014) Subtyping Cryptosporidium ubiquitum, a zoonotic pathogen emerging in humans. Emerging Infectious Diseases 20, 217–224.CrossRefGoogle ScholarPubMed
Li, P, Cai, JZ, Cai, M, Wu, WX, Li, CH, Lei, MT and Xiao, LH (2016) Distribution of Cryptosporidium species in Tibetan sheep and yaks in Qinghai, China. Veterinary Parasitology 215, 58–62.CrossRefGoogle ScholarPubMed
Li, W, Wang, K, Tang, L, Chen, M, Li, H, Kan, Z and Gu, Y (2019) Molecular characterization of Cryptosporidium species in sheep and goats in Anhui Province and neighboring provinces. Chinese Journal of Schistosomiasis Control 31, 474–478, 485.Google ScholarPubMed
Mahdi, NK and Ali, NH (2002) Cryptosporidiosis among animal handlers and their livestock in Basrah, Iraq. East African Medical Journal 79, 550–553.CrossRefGoogle ScholarPubMed
Majeed, QAH, El-Azazy, OME, Abdou, NMI, Al-Aal, ZA, El-Kabbany, AI, Tahrani, LMA and Xiao, L (2018) Epidemiological observations on cryptosporidiosis and molecular characterization of Cryptosporidium spp. in sheep and goats in Kuwait. Parasitology Research 117, 1631–1636.CrossRefGoogle ScholarPubMed
Mammeri, M, Cartou, L, Chevillot, A, Thomas, M, Julien, C, Vallée, I, Polack, B, Follet, J and Adjou, KT (2019) First identification of Cryptosporidium parvum zoonotic subtype IIaA15G2R1 in diarrheal lambs in France. Veterinary Parasitology, Regional Studies and Reports 18, 100355.CrossRefGoogle ScholarPubMed
Mi, RS, Wang, XJ, Huang, Y, Mu, GD, Zhang, YH, Jia, HY and Chen, ZG (2018) Sheep as a potential source of zoonotic cryptosporidiosis in China. Applied and Environmental Microbiology 84, e00868-18.CrossRefGoogle ScholarPubMed
Mirhashemi, ME, Zintl, A, Grant, T, Lucy, F, Mulcahy, G and De Waal, T (2016) Molecular epidemiology of Cryptosporidium species in livestock in Ireland. Veterinary Parasitology 216, 18–22.CrossRefGoogle ScholarPubMed
Papanikolopoulou, V, Baroudi, D, Guo, Y, Wang, Y, Papadopoulos, E, Lafi, SQ and Xiao, L (2018) Genotypes and subtypes of Cryptosporidium spp. in diarrheic lambs and goat kids in northern Greece. Parasitology International 67, 472–475.CrossRefGoogle ScholarPubMed
Paz e Silva, FM, Lopes, RS, Bresciani, KD, Amarante, AF and Araujo, JP Jr. (2014) High occurrence of Cryptosporidium ubiquitum and Giardia duodenalis genotype E in sheep from Brazil. Acta Parasitologica 59, 193–196.CrossRefGoogle ScholarPubMed
Pritchard, GC, Marshall, JA, Giles, M, Mueller-Doblies, D, Sayers, AR, Marshall, RN and Chalmers, RM (2008) Cryptosporidium species in lambs submitted for diagnostic postmortem examination in England and Wales. The Veterinary Record 163, 688–689.Google ScholarPubMed
Qi, M, Zhang, ZJ, Zhao, AY, Jing, B, Guan, GQ, Luo, JX and Zhang, LX (2019) Distribution and molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi amongst grazing adult sheep in Xinjiang, China. Parasitology International 71, 80–86.CrossRefGoogle ScholarPubMed
Robertson, LJ (2009) Giardia and Cryptosporidium infections in sheep and goats a review of the potential for transmission to humans via environmental contamination. Epidemiology and Infection 137, 913–921.CrossRefGoogle ScholarPubMed
Robinson, G and Chalmers, RM (2020) Cryptosporidium diagnostic assays: microscopy. Methods in Molecular Biology 2052, 1–10.CrossRefGoogle ScholarPubMed
Ryan, U, Fayer, R and Xiao, L (2014) Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology 141, 1667–1685.CrossRefGoogle ScholarPubMed
Ryan, U, Zahedi, A and Paparini, A (2016) Cryptosporidium in humans and animals – a one health approach to prophylaxis. Parasite Immunology 38, 535–547.CrossRefGoogle ScholarPubMed
Ryan, UM, Bath, C, Robertson, I, Read, C, Elliot, A, McInnes, L and Besier, B (2005) Sheep may not be an important zoonotic reservoir for Cryptosporidium and Giardia parasites. Applied and Environmental Microbiology 71, 4992–4997.CrossRefGoogle Scholar
Ryan, UM, Feng, Y, Fayer, R and Xiao, L (2021) Taxonomy and molecular epidemiology of Cryptosporidium and Giardia – a 50 year perspective (1971–2021). International Journal for Parasitology 51, 1099–1119.CrossRefGoogle ScholarPubMed
Sahraoui, L, Thomas, M, Chevillot, A, Mammeri, M, Polack, B, Vallee, I and Adjou, KT (2019) Molecular characterization of zoonotic Cryptosporidium spp. and Giardia duodenalis pathogens in Algerian sheep. Veterinary Parasitology – Regional Studies and Reports 16, 100280.CrossRefGoogle ScholarPubMed
Santin, M (2013) Clinical and subclinical infections with Cryptosporidium in animals. New Zealand Veterinary Journal 61, 1–10.CrossRefGoogle ScholarPubMed
Smith, RP, Chalmers, RM, Mueller-Doblies, D, Clifton-Hadley, FA, Elwin, K, Watkins, J and Giles, M (2010) Investigation of farms linked to human patients with cryptosporidiosis in England and Wales. Preventive Veterinary Medicine 94, 9–17.CrossRefGoogle ScholarPubMed
Sow, SO, Muhsen, K, Nasrin, D, Blackwelder, WC, Wu, YK, Farag, TH and Levine, MM (2016) The burden of Cryptosporidium diarrheal disease among children <24 months of age in moderate/high mortality regions of Sub-Saharan Africa and South Asia, utilizing data from the Global Enteric Multicenter Study (GEMS). PLoS Neglected Tropical Diseases 10, e0004729.CrossRefGoogle ScholarPubMed
Squire, SA, Yang, R, Robertson, I, Ayi, I and Ryan, U (2017) Molecular characterization of Cryptosporidium and Giardia in farmers and their ruminant livestock from the Coastal Savannah zone of Ghana. Infection Genetics and Evolution 55, 236–243.CrossRefGoogle ScholarPubMed
Sweeny, JP, Ryan, UM, Robertson, ID, Yang, R, Bell, K and Jacobson, C (2011) Longitudinal investigation of protozoan parasites in meat lamb farms in southern Western Australia. Preventive Veterinary Medicine 101, 192–203.CrossRefGoogle ScholarPubMed
Sweeny, JP, Robertson, ID, Ryan, UM, Jacobson, C and Woodgate, RG (2012) Impacts of naturally acquired protozoa and strongylid nematode infections on growth and faecal attributes in lambs. Veterinary Parasitology 184, 298–308.CrossRefGoogle ScholarPubMed
Tzanidakis, N, Sotiraki, S, Claerebout, E, Ehsan, A, Voutzourakis, N, Kostopoulou, D and Geurden, T (2014) Occurrence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in sheep and goats reared under dairy husbandry systems in Greece. Parasite 21, 45.CrossRefGoogle ScholarPubMed
Urrea-Quezada, A, Gonzalez-Diaz, M, Villegas-Gomez, I, Durazo, M, Hernandez, J, Xiao, LH and Valenzuela, O (2018) Clinical manifestations of cryptosporidiosis and identification of a new Cryptosporidium subtype in patients from Sonora, Mexico. Pediatric Infectious Disease Journal 37, E136–E138.CrossRefGoogle ScholarPubMed
Wang, Y, Feng, Y, Cui, B, Jian, F, Ning, C, Wang, R and Xiao, L (2010) Cervine genotype is the major Cryptosporidium genotype in sheep in China. Parasitology Research 106, 341–347.CrossRefGoogle ScholarPubMed
Wang, ZD, Liu, Q, Liu, HH, Li, S, Zhang, L, Zhao, YK and Zhu, XQ (2018) Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: a global systematic review and meta-analysis. Parasites &Vectors 11, 28.CrossRefGoogle ScholarPubMed
Wu, Y, Chang, Y, Chen, Y, Zhang, X, Li, D, Zheng, S and Zhang, L (2018) Occurrence and molecular characterization of Cryptosporidium spp. Giardia duodenalis, and Enterocytozoon bieneusi from Tibetan sheep in Gansu, China. Infection Genetics and Evolution 64, 46–51.CrossRefGoogle ScholarPubMed
Xiao, L and Feng, Y (2008) Zoonotic cryptosporidiosis. FEMS Immunology Medical Microbiology 52, 309–323.CrossRefGoogle ScholarPubMed
Xiao, L and Feng, Y (2017) Molecular epidemiologic tools for waterborne pathogens Cryptosporidium spp. and Giardia duodenalis. Food and Waterborne Parasitology 8–9, 14–32.CrossRefGoogle ScholarPubMed
Yang, R, Jacobson, C, Gordon, C and Ryan, U (2009) Prevalence and molecular characterisation of Cryptosporidium and Giardia species in pre-weaned sheep in Australia. Veterinary Parasitology 161, 19–24.CrossRefGoogle ScholarPubMed
Yang, R, Jacobson, C, Gardner, G, Carmichael, I, Campbell, AJ, Ng-Hublin, J and Ryan, U (2014) Longitudinal prevalence, oocyst shedding and molecular characterisation of Cryptosporidium species in sheep across four states in Australia. Veterinary Parasitology 200, 50–58.CrossRefGoogle ScholarPubMed
Yang, R, Gardner, GE, Ryan, U and Jacobson, C (2015) Prevalence and pathogen load of Cryptosporidium and Giardia in sheep faeces collected from saleyards and in abattoir effluent in Western Australia. Small Ruminant Research 130, 216–220.CrossRefGoogle Scholar
Yang, X, Guo, Y, Xiao, L and Feng, Y (2021) Molecular epidemiology of human cryptosporidiosis in low- and middle-income countries. Clinical Microbiology Reviews 34, e00087-19.CrossRefGoogle ScholarPubMed
Ye, J, Xiao, L, Wang, Y, Wang, L, Amer, S, Roellig, DM and Feng, Y (2013) Periparturient transmission of Cryptosporidium xiaoi from ewes to lambs. Veterinary Parasitology 197, 627–633.CrossRefGoogle ScholarPubMed
Zahedi, A and Ryan, U (2020) Cryptosporidium – an update with an emphasis on foodborne and waterborne transmission. Research in Veterinary Science 132, 500–512.CrossRefGoogle ScholarPubMed
Zahedi, A, Monis, P, Gofton, AW, Oskam, CL, Ball, A, Bath, A and Ryan, U (2018) Cryptosporidium species and subtypes in animals inhabiting drinking water catchments in three states across Australia. Water Research 134, 327–340.CrossRefGoogle ScholarPubMed
Zhang, X, Jian, Y, Li, X, Ma, L, Karanis, G, Qigang, C and Karanis, P (2018) Molecular detection and prevalence of Cryptosporidium spp. infections in two types of domestic farm animals in the Qinghai-Tibetan Plateau Area (QTPA) in China. Parasitology Research 117, 233–239.CrossRefGoogle ScholarPubMed
Zhang, ZW, Chen, D, Zou, Y, Hou, JL, Sun, LX, Li, Z and Zhu, XQ (2020) First report of Cryptosporidium spp. infection and risk factors in black-boned goats and black-boned sheep in China. Parasitology Research 119, 2813–2819.CrossRefGoogle ScholarPubMed
Zucatto, AS, Aquino, MCC, Inacio, SV, Figueiredo, RN, Pierucci, JC, Perri, SHV and Bresciani, KDS (2015) Molecular characterisation of Cryptosporidium spp. in lambs in the South Central region of the State of Sao Paulo. Arquivo Brasileiro De Medicina Veterinaria E Zootecnia 67, 441–446.CrossRefGoogle Scholar
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material

Download Chen et al. supplementary material(File)
File 799 KB