Abstract
Cryptosporidium spp. are significant zoonotic parasites in humans and animals worldwide. This study aimed to investigate the prevalence of Cryptosporidium infection among raccoon (Procyon lotor) in north of Iran. The fecal samples (n = 30) were collected from raccoons. After DNA extraction, all samples were examined by nested PCR amplification of the 18S ribosomal RNA (rRNA) gene. From 30 raccoon samples, 4 (13.3%) were positive, and the isolates were identified as Cryptosporidium skunk genotype based on sequence analysis. The large distribution of raccoons in northern provinces of Iran and their potency for carrying some human-infecting parasites like Cryptosporidium spp. propose this mammalian as a source for zoonotic parasites.
References
Elwin K, Hadfield SJ, Robinson G, Chalmers RM (2012) The epidemiology of sporadic human infections with unusual cryptosporidia detected during routine typing in England and Wales, 2000–2008. Epidemiol Infect 140(4):673–683. https://doi.org/10.1017/s0950268811000860
Farashi A, Kaboli M, Karami M (2013) Predicting range expansion of invasive raccoons in northern Iran using ENFA model at two different scales. Ecol Inform 15:96–102. https://doi.org/10.1016/j.ecoinf.2013.01.001
Feng Y, Xiao L (2017) Molecular epidemiology of cryptosporidiosis in China. Front Microbiol 8:1701
Feng Y et al (2007) Cryptosporidium genotypes in wildlife from a New York watershed. Applied and Environ Microbiol 73(20):6475–6483
Guo Y, Cebelinski E, Matusevich C, Alderisio KA, Lebbad M et al (2015) Subtyping novel zoonotic pathogen Cryptosporidium chipmunk genotype I. J Clin Microbiol 53:1648–1654
Guyot K, Follet-Dumoulin A, Lelievre E, Sarfati C, Rabodonirina M et al (2001) Molecular characterization of Cryptosporidium isolates obtained from humans in France. J Clin Microbiol 39:3472–3480
Hattori K, Donomoto T, Manchanayake T, Shibahara T, Sasai K, Matsubayashi M (2018) First surveillance and molecular identification of the Cryptosporidium skunk genotype and Cryptosporidium parvum in wild raccoons (Procyon lotor) in Osaka. Japan Parasitol Res 117(11):3669–3674
Hunter PR, Thompson RA (2005) The zoonotic transmission of Giardia and Cryptosporidium. Int J Parasitol 35(11–12):1181–1190
Ikeda T, Asano M, Matoba Y, Abe G (2004) Present status of invasive alien raccoon and its impact in Japan. Glob Environ Res 8(2):125–131
Javanmard E et al (2020a) Prevalence of Cryptosporidium and Giardia in vegetables in Iran: a nineteen-years meta-analysis review. J Environ Health Sci Engin 18(2):1629–1641. https://doi.org/10.1007/s40201-020-00493-w
Javanmard E, Nemati S, Sharifdini M, Rostami A, Mirjalali H, Zali MR (2020b) The first report and molecular analysis of Enterocytozoon bieneusi from raccoon (Procyon lotor) in North of Iran. The J Eukaryot Microbiol 67(3):359–368. https://doi.org/10.1111/jeu.12786
Kresta AE, Henke SE, Pence DB (2009) Gastrointestinal helminths in raccoons in Texas. J Wild Dis 45(1):1–13
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Leśniańska K, Perec-Matysiak A, Hildebrand J, Buńkowska-Gawlik K, Piróg A, Popiołek M (2016) Cryptosporidium spp. and Enterocytozoon bieneusi in introduced raccoons (Procyon lotor)—first evidence from Poland and Germany. Parasitol Res 115(12):4535–4541
Li X, et al. (2020) Prevalence and genotypes of Cryptosporidium in wildlife populations co-located in a protected watershed in the pacific northwest, 2013 to 2016. Microorganisms 8(6). https://doi.org/10.3390/microorganisms8060914
Mahmoudi MR, Ongerth JE, Karanis P (2017) Cryptosporidium and cryptosporidiosis: the Asian perspective. Int J Hyg Environ Health 220(7):1098–1109. https://doi.org/10.1016/j.ijheh.2017.07.005
Perz JF, Le Blancq SM (2001) Cryptosporidium parvum infection involving novel genotypes in wildlife from lower New York State. Appl Environ Microbiol 67(3):1154–1162
Plutzer J, Karanis P (2007) Genotype and subtype analyses of Cryptosporidium isolates from cattle in Hungary. Vet Parasitol 146(3–4):357–362
Rahimi HM, Nemati S, Mirjalali H, Sharifdini M, Zali MR (2020) Molecular characterization and identification of Blastocystis and its subtypes from raccoon (Procyon lotor) in north of Iran. Parasitol Res 119(8):2741–2745
Rengifo-Herrera C et al (2011) Detection and characterization of a Cryptosporidium isolate from a southern elephant seal (Mirounga leonina) from the Antarctic Peninsula. Appl Environ Microbiol 77(4):1524–1527
Rentería-Solís Z, Meyer-Kayser E, Obiegala A, Ackermann F, Król N, Birka S (2020) Cryptosporidium sp. skunk genotype in wild raccoons (Procyon lotor) naturally infected with Baylisascaris procyonis from central Germany. Parasitol Int 79:102159
Robinson G, Elwin K, Chalmers RM (2008) Unusual Cryptosporidium genotypes in human cases of diarrhea. Emerg Infect Dis 14(11):1800
Rojas-Lopez L, Elwin K, Chalmers RM, Enemark HL, Beser J, Troell K (2020) Development of a gp60-subtyping method for Cryptosporidium felis. Parasite Vectors 13(1):1–8
Ryan U (2010) Cryptosporidium in birds, fish and amphibians. Exp Parasitol 124(1):113–120. https://doi.org/10.1016/j.exppara.2009.02.002
Ryan U, Fayer R, Xiao L (2014) Cryptosporidium species in humans and animals: current understanding and research needs. Parasitol 141(13):1667–1685. https://doi.org/10.1017/s0031182014001085
Ryan U, Paparini A, Monis P, Hijjawi N (2016) It’s official - Cryptosporidium is a gregarine: what are the implications for the water industry? Water Res 105:305–313. https://doi.org/10.1016/j.watres.2016.09.013
Squire SA, Ryan U (2017) Cryptosporidium and Giardia in Africa: current and future challenges. Parasite Vectors 10(1):195. https://doi.org/10.1186/s13071-017-2111-y
Stenger BLS et al (2015) North American tree squirrels and ground squirrels with overlapping ranges host different Cryptosporidium species and genotypes. Infect Gen Evol 36:287–293. https://doi.org/10.1016/j.meegid.2015.10.002
Stensvold C, Elwin K, Winiecka-Krusnell J, Chalmers R, Xiao L, Lebbad M (2015) Development and application of a gp60-based typing assay for Cryptosporidium viatorum. J Clin Microbiol 53:1891–1897
Taghipour A, Javanmard E, Haghighi A, Mirjalali H, Zali MR (2019) The occurrence of Cryptosporidium sp., and eggs of soil-transmitted helminths in market vegetables in the north of Iran. Gastroenterol Hepatol Bed Bench, 12 (4), pp. 364–369.
Widmer G, Köster PC, Carmena D (2020) Cryptosporidium hominis infections in non-human animal species: revisiting the concept of host specificity. Int J Parasitol 50(4):253–262. https://doi.org/10.1016/j.ijpara.2020.01.005
Xiao L, Feng Y (2017) Molecular epidemiologic tools for waterborne pathogens Cryptosporidium spp. and Giardia duodenalis. Food Waterborne Parasitol 8:14–32
Xiao L et al (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65(4):1578–1583. https://doi.org/10.1128/aem.65.4.1578-1583.1999
Yan W et al (2017) Subtype analysis of zoonotic pathogen Cryptosporidium skunk genotype. Infect Gene Evol 55:20–25
Zahedi A, Ryan U (2020) Cryptosporidium - an update with an emphasis on foodborne and waterborne transmission. Res Vet Sci 132:500–512. https://doi.org/10.1016/j.rvsc.2020.08.002
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. Int J Parasitol: Parasit Wild 5(1):88–109
Zhou L, Fayer R, Trout JM, Ryan UM, Schaefer FW 3rd, Xiao L (2004) Genotypes of Cryptosporidium species infecting fur-bearing mammals differ from those of species infecting humans. Appl Environ Microbiol 70(12):7574–7577. https://doi.org/10.1128/aem.70.12.7574-7577.2004
Ziegler PE, Wade SE, Schaaf SL, Stern DA, Nadareski CA, Mohammed HO (2007) Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York State. Vet Parasitol 147(1–2):176–184. https://doi.org/10.1016/j.vetpar.2007.03.024
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: HM MS. Performed the experiments: HMR SSJ. Analyzed the data: HM SN. Contributed reagents/materials/analysis tools/positive samples: MS MRZ. Wrote the paper: HM SSJ. All authors read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Ethical approval
The protocol of this study was approved by the Ethics Committee of Guilan University of Medical Sciences, Iran (IR.GUMS.REC.1394.185).
Conflict of interest
The authors declare no competing interests.
Informed consent
Not applicable.
Additional information
Section Editor: Daniel K Howe.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mohammad Rahimi, H., Soleimani Jevinani, S., Nemati, S. et al. Molecular characterization of Cryptosporidium skunk genotype in raccoons (Procyon lotor) in Iran: concern for zoonotic transmission. Parasitol Res 121, 483–489 (2022). https://doi.org/10.1007/s00436-021-07367-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07367-6