Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T16:01:54.128Z Has data issue: false hasContentIssue false
  • English
  • Français

Cryptosporidium ratti n. sp. (Apicomplexa: Cryptosporidiidae) and genetic diversity of Cryptosporidium spp. in brown rats (Rattus norvegicus) in the Czech Republic

Published online by Cambridge University Press:  28 September 2020

Jana Ježková ,
Jitka Prediger ,
Nikola Holubová ,
Bohumil Sak ,
Roman Konečný ,
Yaoyu Feng ,
Lihua Xiao ,
Michael Rost ,
John McEvoy Open the ORCID record for John McEvoy [Opens in a new window]  and
Martin Kváč Open the ORCID record for Martin Kváč [Opens in a new window]
Jana Ježková
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 37005České Budějovice, Czech Republic
Jitka Prediger
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 37005České Budějovice, Czech Republic
Nikola Holubová
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 37005České Budějovice, Czech Republic Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05České Budějovice, Czech Republic
Bohumil Sak
Affiliation:
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05České Budějovice, Czech Republic
Roman Konečný
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 37005České Budějovice, Czech Republic
Yaoyu Feng
Affiliation:
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, Guangzhou510642, Guangdong, China Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou510642, Guangdong, China
Lihua Xiao
Affiliation:
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, Guangzhou510642, Guangdong, China Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou510642, Guangdong, China
Michael Rost
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 37005České Budějovice, Czech Republic
John McEvoy
Affiliation:
Microbiological Sciences Department, North Dakota State University, 1523 Centennial Blvd, Van Es Hall, Fargo, ND58102, USA
Martin Kváč*
Affiliation:
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 1668, 37005České Budějovice, Czech Republic Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05České Budějovice, Czech Republic
*
Author for correspondence: Martin Kváč, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The diversity and biology of Cryptosporidium that is specific for rats (Rattus spp.) are not well studied. We examined the occurrence and genetic diversity of Cryptosporidium spp. in wild brown rats (Rattus norvegicus) by microscopy and polymerase chain reaction (PCR)/sequencing targeting the small subunit rDNA (SSU), actin and HSP70 genes. Out of 343 faecal samples tested, none were positive by microscopy and 55 were positive by PCR. Sequence analysis of SSU gene revealed the presence of Cryptosporidium muris (n = 4), C. andersoni (n = 3), C. ryanae (n = 1), C. occultus (n = 3), Cryptosporidium rat genotype I (n = 23), Cryptosporidium rat genotype IV (n = 16) and novel Cryptosporidium rat genotype V (n = 5). Spherical oocysts of Cryptosporidium rat genotype I obtained from naturally-infected rats, measuring 4.4–5.4 μm × 4.3–5.1 μm, were infectious to the laboratory rats, but not to the BALB/c mice (Mus musculus) nor Mongolian gerbils (Meriones unguiculatus). The prepatent period was 3 days post infection and the patent period was longer than 30 days. Naturally- and experimentally-infected rats showed no clinical signs of disease. Percentage of nucleotide similarities at the SSU, actin, HSP70 loci between C. ratti n. sp. and the rat derived C. occultus and Cryptosporidium rat genotype II, III, IV, and V ranged from 91.0 to 98.1%. These genetic variations were similar or greater than that observed between closely related species, i.e. C. parvum and C. erinacei (93.2–99.5%). Our morphological, genetic and biological data support the establishment of Cryptosporidium rat genotype I as a new species, Cryptosporidium ratti n. sp.

Keywords

Cryptosporidium rattiinfectivitymorphometric analysisphylogenyprevalence
Type
Research Article
Information
Parasitology , Volume 148 , Issue 1 , January 2021 , pp. 84 - 97
Check for updates
Copyright
Copyright © The Author(s), 2020. 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.)

References

Arrowood, MJ and Donaldson, K (1996) Improved purification methods for calf-derived Cryptosporidium parvum oocysts using discontinuous sucrose and cesium chloride gradients. Journal of Eukaryotic Microbiology 43, 89S.CrossRefGoogle ScholarPubMed
Bahrami, F, Sadraei, J and Frozandeh, M (2012) Molecular characterization of Cryptosporidium Spp. in wild rats of Tehran, Iran using 18s rRNA gene and PCR_RFLP method. Jundishapur Journal of Microbiology 5, 486–490.CrossRefGoogle Scholar
Chalmers, RM, Robinson, G, Elwin, K, Hadfield, SJ, Thomas, E, Watkins, J, Casemore, D and Kay, D (2010) Detection of Cryptosporidium species and sources of contamination with Cryptosporidium hominis during a waterborne outbreak in north west Wales. Journal of Water & Health 8, 311–325.CrossRefGoogle ScholarPubMed
Chappell, CL, Okhuysen, PC, Langer-Curry, RC, Lupo, PJ, Widmer, G and Tzipori, S (2015) Cryptosporidium muris: infectivity and illness in healthy adult volunteers. The American Journal of Tropical Medicine and Hygiene 92, 50–55.CrossRefGoogle ScholarPubMed
Čondlová, S, Horčičková, M, Sak, B, Květoňová, D, Hlásková, L, Konečný, R, Stanko, M, McEvoy, J and Kváč, M (2018) Cryptosporidium apodemi sp. n. and Cryptosporidium Ditrichi sp. n. (Apicomplexa: Cryptosporidiidae) in Apodemus Spp. European Journal of Protistology 63, 1–12.CrossRefGoogle Scholar
Čondlová, S, Horčičková, M, Havrdová, N, Sak, B, Hlásková, L, Perec-Matysiak, A, Kicia, M, McEvoy, J and Kváč, M (2019) Diversity of Cryptosporidium Spp. in Apodemus Spp. in Europe. European Journal of Protistology 69, 1–13.CrossRefGoogle ScholarPubMed
Crawshaw, GJ and Mehren, KG (1987) Cryptosporidiosis in zoo and wild animals. In Ippen, R and Schroder, HD (eds), Erkrankungen der Zootiere. Verhandlungsbericht des 29. Internationalen Symposiums Uber die Erkrankungen der Zootiere. Berlin, Cardiff: Akademie-Verlag, pp. 353–362.Google Scholar
Elwin, K, Hadfield, SJ, Robinson, G, Crouch, ND and Chalmers, RM (2012) Cryptosporidium viatorum n. sp. (Apicomplexa: Cryptosporidiidae) among travellers returning to Great Britain from the Indian subcontinent, 2007–2011. International Journal for Parasitology 42, 675–682.CrossRefGoogle ScholarPubMed
Fayer, R (2010) Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 90–97.CrossRefGoogle ScholarPubMed
Fayer, R and Santín, M (2009) Cryptosporidium Xiaoi N. sp. (Apicomplexa: Cryptosporidiidae) in sheep (Ovis Aries). Veterinary Parasitology 164, 192–200.CrossRefGoogle Scholar
Fayer, R, Santín, M and Macarisin, D (2010) Cryptosporidium Ubiquitum n. sp. in animals and humans. Veterinary Parasitology 172, 23–32.CrossRefGoogle ScholarPubMed
Feng, Y, Li, N, Duan, L and Xiao, L (2009) Cryptosporidium Genotype and subtype distribution in raw wastewater in Shanghai, China: evidence for possible unique Cryptosporidium hominis Transmission. Journal of Clinical Microbiology 47, 153–157.CrossRefGoogle ScholarPubMed
Feng, Y, Lal, AA, Li, N and Xiao, L (2011) Subtypes of Cryptosporidium Spp. in mice and other small mammals. Experimental Parasitology 127, 238–242.CrossRefGoogle ScholarPubMed
Gholipoury, M, Rezai, HR, Namroodi, S and Arab Khazaeli, F (2016) Zoonotic and non-zoonotic parasites of wild rodents in Turkman Sahara, Northeastern Iran. Iranian Journal of Parasitology 11, 350–357.Google Scholar
Graczyk, TK, Cranfield, MR, Fayer, R and Anderson, MS (1996) Viability and infectivity of Cryptosporidium parvum oocysts are retained upon intestinal passage through a refractory avian host. Applied and Environmental Microbiology 62, 3234–3237.CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Henriksen, SA and Pohlenz, JF (1981) Staining of cryptosporidia by a modified Ziehl-Neelsen technique. Acta Veterinaria Scandinavica 22, 594–596.Google ScholarPubMed
Holubová, N, Zikmundová, V, Limpouchová, Z, Sak, B, Konečný, R, Hlásková, L, Rajský, D, Kopacz, Z, McEvoy, J and Kváč, M (2019) Cryptosporidium Proventriculi sp. n. (Apicomplexa: Cryptosporidiidae) in Psittaciformes birds. European Journal of Protistology 69, 70–87.CrossRefGoogle Scholar
Holubová, N, Tůmová, L, Sak, B, Hejzlerová, A, Konečný, R, McEvoy, J and Kváč, M (2020) Description of Cryptosporidium Ornithophilus sp. n. (Apicomplexa: Cryptosporidiidae) as a new species and diversity in farmed ostriches. Parasites & Vectors 13, 340.CrossRefGoogle Scholar
Horčičková, M, Čondlová, S, Holubová, N, Sak, B, Květoňová, D, Hlásková, L, Konečný, R, Sedláček, F, Clark, M, Giddings, C, McEvoy, J and Kváč, M (2018) Diversity of Cryptosporidium in common voles and description of Cryptosporidium Alticolis sp. n. and Cryptosporidium microti sp. n. (Apicomplexa: Cryptosporidiidae). Parasitology 146, 220–233. doi: 10.1017/S0031182018001142CrossRefGoogle Scholar
ICZN, (2012) International Commission on Zoological Nomenclature: amendmentof articles 8, 9, 10, 21 and 78 of the international code of zoologicalnomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature 69, 161–169.Google Scholar
Iseki, M (1986) Two species of Cryptosporidium Naturally infecting house rats, Rattus norvegicus. Japanese Journal of Parasitology 35, 251–256.Google Scholar
Ježková, J, Horčičková, M, Hlásková, L, Sak, B, Květoňová, D, Novák, J, Hofmannová, L, McEvoy, J and Kváč, M (2016) Cryptosporidium testudinis sp. n., Cryptosporidium Ducismarci Traversa, 2010 and Cryptosporidium Tortoise genotype III (Apicomplexa: Cryptosporidiidae) in tortoises. Folia Parasitologica 63, 035.CrossRefGoogle Scholar
Jiang, J, Alderisio, KA and Xiao, L (2005) Distribution of Cryptosporidium Genotypes in storm event water samples from three watersheds in New York. Applied and Environmental Microbiology 71, 4446–4454.CrossRefGoogle ScholarPubMed
Kimura, A, Edagawa, A, Okada, K, Takimoto, A, Yonesho, S and Karanis, P (2007) Detection and genotyping of Cryptosporidium From brown rats (Rattus norvegicus) captured in an urban area of Japan. Parasitology Research 100, 1417–1420.CrossRefGoogle Scholar
Koehler, AV, Wang, T, Haydon, SR and Gasser, RB (2018) Cryptosporidium viatorum from the native Australian swamp rat Rattus Lutreolus – An emerging zoonotic pathogen? International Journal for Parasitology: Parasites and Wildlife 7, 18–26.Google ScholarPubMed
Kváč, M, Hanzlíková, D, Sak, B and Květoňová, D (2009) Prevalence and age-related infection of Cryptosporidium suis, C. muris And Cryptosporidium Pig genotype II in pigs on a farm complex in the Czech Republic. Veterinary Parasitology 160, 319–322.CrossRefGoogle Scholar
Kváč, M, Kestřánová, M, Květoňová, D, Kotková, M, Ortega, Y, McEvoy, J and Sak, B (2012) Cryptosporidium Tyzzeri and Cryptosporidium muris originated from wild West-European house mice (Mus Musculus domesticus) and East-European house mice (Mus Musculus Musculus) are non-infectious for pigs. Experimental Parasitology 131, 107–110.CrossRefGoogle ScholarPubMed
Kváč, M, Kestřánová, M, Pinková, M, Květoňová, D, Kalinová, J, Wagnerová, P, Kotková, M, Vítovec, J, Ditrich, O, McEvoy, J, Stenger, B and Sak, B (2013) Cryptosporidium Scrofarum n. sp. (Apicomplexa: Cryptosporidiidae) in domestic pigs (Sus scrofa). Veterinary Parasitology 191, 218–227.CrossRefGoogle Scholar
Kváč, M, Hofmannová, L, Hlásková, L, Květoňová, D, Vítovec, J, McEvoy, J and Sak, B (2014 a) Cryptosporidium Erinacei n. sp. (Apicomplexa: Cryptosporidiidae) in hedgehogs. Veterinary Parasitology 201, 9–17.CrossRefGoogle Scholar
Kváč, M, McEvoy, J, Stenger, B and Clark, M (2014 b) Cryptosporidiosis in other vertebrates. In Cacciò, SM and Widmer, G (eds), Cryptosporidium: Parasite and Disease. Wien: Springer, pp. 237–326.CrossRefGoogle Scholar
Kváč, M, Havrdová, N, Hlásková, L, Daňková, T, Kanděra, J, Ježková, J, Vítovec, J, Sak, B, Ortega, Y, Xiao, L, Modrý, D, Chelladurai, JR, Prantlová, V and McEvoy, J (2016) Cryptosporidium proliferans N. sp. (Apicomplexa: Cryptosporidiidae): molecular and biological evidence of cryptic species within gastric Cryptosporidium Of mammals. PLoS One 11, e0147090.CrossRefGoogle ScholarPubMed
Kváč, M, Vlnatá, G, Ježková, J, Horčičková, M, Konečný, R, Hlásková, L, McEvoy, J and Sak, B (2018) Cryptosporidium occultus sp. n. (Apicomplexa: Cryptosporidiidae) in rats. European Journal of Protistology 63, 96–104.CrossRefGoogle Scholar
Li, X, Pereira, M, Larsen, R, Xiao, C, Phillips, R, Striby, K, McCowan, B and Atwill, ER (2015) Cryptosporidium Rubeyi N. sp. (Apicomplexa: Cryptosporidiidae) in multiple Spermophilus ground squirrel species. International Journal for Parasitology: Parasites and Wildlife 4, 343–350.Google ScholarPubMed
Lindsay, DS, Blagburn, BL, Sundermann, CA and Hoerr, FJ (1989) Experimental infections in domestic ducks with Cryptosporidium baileyi isolated from chickens. Avian Diseases 33, 69–73.CrossRefGoogle ScholarPubMed
Lv, C, Zhang, L, Wang, R, Jian, F, Zhang, S, Ning, C, Wang, H, Feng, C, Wang, X, Ren, X, Qi, M and Xiao, L (2009) Cryptosporidium spp. in wild, laboratory, and pet rodents in China: prevalence and molecular characterization. Applied and Environmental Microbiology 75, 7692–7699.CrossRefGoogle ScholarPubMed
Miláček, P and Vítovec, J (1985) Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitologica 32, 50.Google ScholarPubMed
Mirzaghavami, M, Sadraei, J and Forouzandeh, M (2016) Detection of Cryptosporidium Spp. in free ranging animals of Tehran, Iran. Journal of Parasitic Diseases 40, 1528–1531.CrossRefGoogle ScholarPubMed
Morgan-Ryan, UM, Fall, A, Ward, LA, Hijjawi, N, Sulaiman, I, Fayer, R, Thompson, RC, Olson, M, Lal, A and Xiao, L (2002) Cryptosporidium hominis n. sp. (Apicomplexa: Cryptosporidiidae) from Homo sapiens. Journal of Eukaryotic Microbiology 49, 433–440.CrossRefGoogle ScholarPubMed
Naciri, M, Lefay, MP, Mancassola, R, Poirier, P and Chermette, R (1999) Role of Cryptosporidium parvum as a pathogen in neonatal diarrhoea complex in suckling and dairy calves in France. Veterinary Parasitology 85, 245–257.CrossRefGoogle ScholarPubMed
Ng-Hublin, JS, Singleton, GR and Ryan, U (2013) Molecular characterization of Cryptosporidium Spp. from wild rats and mice from rural communities in the Philippines. Infection Genetics and Evolution 16, 5–12.CrossRefGoogle ScholarPubMed
Nordhausen, K, Sirkia, S, Oja, H and Tyler, D (2018). CSNP: Tools for Multivariate Nonparametrics. R package version 1.1-1. Available at https://CRAN.R-project.org/package=ICSNP.Google Scholar
Nydam, DV, Wade, SE, Schaaf, SL and Mohammed, HO (2001) Number of Cryptosporidium parvum Oocysts or Giardia Spp. cysts shed by dairy calves after natural infection. American Journal of Veterinary Research 62, 1612–1615.CrossRefGoogle ScholarPubMed
Paparini, A, Jackson, B, Ward, S, Young, S and Ryan, UM (2012) Multiple Cryptosporidium genotypes detected in wild black rats (Rattus Rattus) from northern Australia. Experimental Parasitology 131, 404–412.CrossRefGoogle ScholarPubMed
Prasetyo, RH (2016) Survey of house rat intestinal parasites from Surabaya District, East Java, Indonesia that can cause opportunistic infections in humans. Southeast Asian Journal of Tropical Medicine and Public Health 47, 194–198.Google ScholarPubMed
Rašková, V, Květoňová, D, Sak, B, McEvoy, J, Edwinson, A, Stenger, B and Kváč, M (2013) Human cryptosporidiosis caused by Cryptosporidium Tyzzeri And C. parvum Isolates presumably transmitted from wild mice. Journal of Clinical Microbiology 51, 360–362.CrossRefGoogle Scholar
R Core Team (2019). R. A language and environment for statistical computing. In R Foundation for Statistical Computing Vienna, Austria.Google Scholar
Reid, FA (2007) A field guide to mammals of North America, 4th ed. Choice: Current Reviews for Academic Libraries 44, 1560–1560.Google Scholar
Ren, X, Zhao, J, Zhang, L, Ning, C, Jian, F, Wang, R, Lv, C, Wang, Q, Arrowood, MJ and Xiao, L (2012) Cryptosporidium Tyzzeri n. sp. (Apicomplexa: Cryptosporidiidae) in domestic mice (Mus Musculus). Experimental Parasitology 130, 274–281.CrossRefGoogle Scholar
Robertson, LJ, Björkman, C, Axén, C and Fayer, R (2014) Cryptosporidiosis in farmed animals. In Cacciò, SM and Widmer, G (eds), Cryptosporidium: Parasite and Disease. Wien: Springer, pp. 149–236.CrossRefGoogle Scholar
Saki, J, Foroutan-Rad, M and Asadpouri, R (2016) Molecular characterization of Cryptosporidium Spp. in wild rodents of Southwestern Iran using 18s rRNA gene nested-PCR-RFLP and sequencing techniques. Journal of Tropical Medicine 2016, 6834206.CrossRefGoogle ScholarPubMed
Sauch, JF, Flanigan, D, Galvin, ML, Berman, D and Jakubowski, W (1991) Propidium iodide as an indicator of Giardia cyst viability. Applied and Environmental Microbiology 57, 3243–3247.CrossRefGoogle ScholarPubMed
Seoki, S, Park, J, Cho, S, Baek, M, Lee, H, Kim, D, Yang, KW, Jang, D, Han, B, Nam, K and Park, J (2005) Health surveillance of specific pathogen-free and conventionally-housed mice and rats in Korea. Experimental Animals 54, 85–92.CrossRefGoogle Scholar
Silva, SO, Richtzenhain, LJ, Barros, IN, Gomes, AM, Silva, AV, Kozerski, ND, de Araujo Ceranto, JB, Keid, LB and Soares, RM (2013) A new set of primers directed to 18S rRNA gene for molecular identification of Cryptosporidium Spp. and their performance in the detection and differentiation of oocysts shed by synanthropic rodents. Experimental Parasitology 135, 551–557.CrossRefGoogle ScholarPubMed
Song, J, Kim, CY, Chang, SN, Abdelkader, TS, Han, J, Kim, TH, Oh, H, Lee, JM, Kim, DS, Kim, JT, Oh, HS, Hur, M, Suh, JH and Park, JH (2015) Detection and molecular characterization of Cryptosporidium Spp. from wild rodents and insectivores in South Korea. The Korean Journal of Parasitology 53, 737–743.CrossRefGoogle ScholarPubMed
Stenger, BLS, Horčičková, M, Clark, ME, Kváč, M, Čondlová, S, Khan, E, Widmer, G, Xiao, L, Giddings, CW, Pennil, C, Stanko, M, Sak, B and McEvoy, JM (2017) Cryptosporidium Infecting wild cricetid rodents from the subfamilies Arvicolinae and Neotominae. Parasitology 145, 326–334.CrossRefGoogle ScholarPubMed
Sulaiman, IM, Morgan, UM, Thompson, RC, Lal, AA and Xiao, L (2000) Phylogenetic relationships of Cryptosporidium Parasites based on the 70-kilodalton heat shock protein (HSP70) gene. Applied and Environmental Microbiology 66, 2385–2391.CrossRefGoogle ScholarPubMed
Sulaiman, IM, Lal, AA and Xiao, LH (2002) Molecular phylogeny and evolutionary relationships of Cryptosporidium Parasites at the actin locus. Journal of Parasitology 88, 388–394.CrossRefGoogle ScholarPubMed
Tan, TK, Low, VL, Ng, WH, Ibrahim, J, Wang, D, Tan, CH, Chellappan, S and Lim, YAL (2019) Occurrence of zoonotic Cryptosporidium And Giardia Duodenalis species/genotypes in urban rodents. Parasitology International 69, 110–113.CrossRefGoogle ScholarPubMed
Thomson, V, Wiewel, A, Chinen, A, Maryanto, I, Sinaga, MH, How, R, Aplin, K and Suzuki, H (2018) A perspective for resolving the systematics of Rattus, the vertebrates with the most influence on human welfare. Zootaxa 4459, 431–452.CrossRefGoogle ScholarPubMed
Tijjani, M, Abd Majid, R, Abdullahi, SA and Unyah, NZ (2020) Detection of rodent-borne parasitic pathogens of wild rats in Serdang, Selangor, Malaysia: a potential threat to human health. International Journal for Parasitology-Parasites and Wildlife 11, 174–182.CrossRefGoogle ScholarPubMed
Tyzzer, EE (1910) An extracellular coccidium, Cryptosporidium muris (gen. et sp. nov.) of the gastric glands of the common mouse. Journal of Medical Research 23, 487–509.Google ScholarPubMed
Tzipori, S, Smith, M, Halpin, C, Angus, KW, Sherwood, D and Campbell, I (1983) Experimental cryptosporidiosis in calves – clinical manifestations and pathological findings. Veterinary Record 112, 116–120.CrossRefGoogle ScholarPubMed
Vetterling, JM, Jervis, HR, Merrill, TG and Sprinz, H (1971) Cryptosporidium Wrairi sp. n. from the guinea pig Cavia Porcellus, with an emendation of the genus. The Journal of Protozoology 18, 243–247.CrossRefGoogle Scholar
Webster, JP and Macdonald, DW (1995) Cryptosporidiosis reservoir in wild brown rats (Rattus norvegicus) in the UK. Epidemiology and Infection 115, 207–209.CrossRefGoogle Scholar
Wei, Z, Liu, Q, Zhao, W, Jiang, X, Zhang, Y, Zhao, A, Jing, B, Lu, G and Qi, M (2019) Prevalence and diversity of Cryptosporidium Spp. in bamboo rats (Rhizomys sinensis) in South Central China. International Journal for Parasitology: Parasites and Wildlife 9, 312–316.Google Scholar
Xiao, L, Morgan, UM, Limor, J, Escalante, A, Arrowood, M, Shulaw, W, Thompson, RC, Fayer, R and Lal, AA (1999) Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Applied and Environmental Microbiology 65, 3386–3391.CrossRefGoogle ScholarPubMed
Xiao, L, Ryan, UM, Graczyk, TK, Limor, J, Li, L, Kombert, M, Junge, R, Sulaiman, IM, Zhou, L, Arrowood, MJ, Koudela, B, Modrý, D and Lal, AA (2004) Genetic diversity of Cryptosporidium Spp. in captive reptiles. Applied and Environmental Microbiology 70, 891–899.CrossRefGoogle ScholarPubMed
Yamaura, H, Shirasaka, R, Asahi, H, Koyama, T, Motoki, M and Ito, H (1990) Prevalence of Cryptosporidium Infection among house rats, Rattus Rattus And R. norvegicus, in Tokyo, Japan and experimental cryptosporidiosis in roof rats. Japanese Journal of Parasitology 39, 439–444.Google Scholar
Zahedi, A, Durmic, Z, Gofton, AW, Kueh, S, Austen, J, Lawson, M, Callahan, L, Jardine, J and Ryan, U (2017) Cryptosporidium Homai n. sp. (Apicomplexa: Cryptosporidiiae) from the guinea pig (Cavia Porcellus). Veterinary Parasitology 245, 92–101.CrossRefGoogle Scholar
Zhao, Z, Wang, R, Zhao, W, Qi, M, Zhao, J, Zhang, L, Li, J and Liu, A (2015) Genotyping and subtyping of Giardia And Cryptosporidium Isolates from commensal rodents in China. Parasitology 142, 800–806.CrossRefGoogle ScholarPubMed
Zhao, W, Wang, J, Ren, G, Yang, Z, Yang, F, Zhang, W, Xu, Y, Liu, A and Ling, H (2018) Molecular characterizations of Cryptosporidium Spp. and Enterocytozoon bieneusi in brown rats (Rattus norvegicus) from Heilongjiang Province, China. Parasites & Vectors 11, 313.CrossRefGoogle ScholarPubMed
Zhao, W, Zhou, H, Huang, Y, Xu, L, Rao, L, Wang, S, Wang, W, Yi, Y, Zhou, X, Wu, Y, Ma, T, Wang, G, Hu, X, Peng, R, Yin, F and Lu, G (2019) Cryptosporidium spp. in wild rats (Rattus Spp.) from the Hainan Province, China: molecular detection, species/genotype identification and implications for public health. International Journal for Parasitology: Parasites and Wildlife 9, 317–321.Google ScholarPubMed