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

. 2021 Jan ; 148 (1) : 84-97. [epub] 20200928

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32981543

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.

Zobrazit více v PubMed

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. PubMed

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.

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. PubMed

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. PubMed PMC

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. PubMed

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. PubMed PMC

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.

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. PubMed

Fayer R (2010) Taxonomy and species delimitation in Cryptosporidium. Experimental Parasitology 124, 90–97. PubMed

Fayer R and Santín M (2009) Cryptosporidium Xiaoi N. sp. (Apicomplexa: Cryptosporidiidae) in sheep (Ovis Aries). Veterinary Parasitology 164, 192–200. PubMed

Fayer R, Santín M and Macarisin D (2010) Cryptosporidium Ubiquitum n. sp. in animals and humans. Veterinary Parasitology 172, 23–32. PubMed

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. PubMed PMC

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. PubMed

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. PubMed PMC

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. PubMed PMC

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.

Henriksen SA and Pohlenz JF (1981) Staining of cryptosporidia by a modified Ziehl-Neelsen technique. Acta Veterinaria Scandinavica 22, 594–596. PubMed PMC

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. PubMed

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. PubMed PMC

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/S0031182018001142 PubMed DOI PMC

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.

Iseki M (1986) Two species of Cryptosporidium Naturally infecting house rats, Rattus norvegicus. Japanese Journal of Parasitology 35, 251–256.

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. PubMed

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. PubMed PMC

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. PubMed

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. PubMed PMC

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. PubMed

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. PubMed

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. PubMed PMC

Kváč M, Hofmannová L, Hlásková L, Květoňová D, Vítovec J, McEvoy J and Sak B (2014a) Cryptosporidium Erinacei n. sp. (Apicomplexa: Cryptosporidiidae) in hedgehogs. Veterinary Parasitology 201, 9–17. PubMed

Kváč M, McEvoy J, Stenger B and Clark M (2014b) Cryptosporidiosis in other vertebrates. In Cacciò SM and Widmer G (eds), Cryptosporidium: Parasite and Disease. Wien: Springer, pp. 237–326.

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. PubMed PMC

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. PubMed

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. PubMed PMC

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. PubMed

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. PubMed PMC

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. PubMed

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. PubMed PMC

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. PubMed

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. PubMed PMC

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. PubMed

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.

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. PubMed

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. PubMed

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. PubMed

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. PubMed PMC

R Core Team (2019). R. A language and environment for statistical computing. In R Foundation for Statistical Computing Vienna, Austria.

Reid FA (2007) A field guide to mammals of North America, 4th ed. Choice: Current Reviews for Academic Libraries 44, 1560–1560.

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. PubMed

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.

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. PubMed PMC

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. PubMed PMC

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. PubMed

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. PubMed

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. PubMed PMC

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. PubMed PMC

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. PubMed PMC

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. PubMed

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. PubMed

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. PubMed

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. PubMed PMC

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. PubMed PMC

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. PubMed

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. PubMed

Webster JP and Macdonald DW (1995) Cryptosporidiosis reservoir in wild brown rats (Rattus norvegicus) in the UK. Epidemiology and Infection 115, 207–209. PubMed PMC

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. PubMed PMC

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. PubMed PMC

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. PubMed PMC

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.

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. PubMed

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. PubMed

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. PubMed PMC

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. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace