Hostname: page-component-7f64f4797f-fz5kh Total loading time: 0 Render date: 2025-11-04T09:18:54.872Z Has data issue: false hasContentIssue false
  • English
  • Français

Genotyping and subtyping of Giardia and Cryptosporidium isolates from commensal rodents in China

Published online by Cambridge University Press:  12 January 2015

Z. ZHAO ,
R. WANG ,
W. ZHAO ,
M. QI ,
J. ZHAO ,
L. ZHANG ,
J. LI  and
A. LIU
Z. ZHAO
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China
R. WANG
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China
W. ZHAO
Affiliation:
Department of Parasitology, Harbin Medical University, Harbin 150081, PR China
M. QI
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China
J. ZHAO
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China
L. ZHANG*
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China
J. LI
Affiliation:
College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China
A. LIU*
Affiliation:
Department of Parasitology, Harbin Medical University, Harbin 150081, PR China
*
* Corresponding authors. College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China, Department of Parasitology, Harbin Medical University, Harbin 150081, PR China E-mail: zhanglx8999@gmail.com and E-mail: liuaiqin1128@126.com
* Corresponding authors. College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, PR China, Department of Parasitology, Harbin Medical University, Harbin 150081, PR China E-mail: zhanglx8999@gmail.com and E-mail: liuaiqin1128@126.com
Get access Rights & Permissions [Opens in a new window]

Summary

Cryptosporidium and Giardia are two important zoonotic intestinal parasites responsible for diarrhoea in humans and other animals worldwide. Rodents, as reservoirs or carriers of Cryptosporidium and Giardia, are abundant and globally widespread. In the present study, we collected 232 fecal specimens from commensal rodents captured in animal farms and farm neighbourhoods in China. We collected 33 Asian house rats, 168 brown rats and 31 house mice. 6·0% (14/232) and 8·2% (19/232) of these rodents were microscopy-positive for Giardia cysts and Cryptosporidium oocysts, respectively. All 14 Giardia isolates were identified as Giardia duodenalis assemblage G at a minimum of one or maximum of three gene loci (tpi, gdh and bg). By small subunit rRNA (SSU rRNA) gene sequencing, Cryptosporidium parvum (n = 12) and Cryptosporidium muris (n = 7) were identified. The gp60 gene encoding the 60-kDa glycoprotein was successfully amplified and sequenced in nine C. parvum isolates, all of which belonged to the IIdA15G1 subtype. Observation of the same IIdA15G1 subtype in humans (previously) and in rodents (here) suggests that rodents infected with Cryptosporidium have the potential to transmit cryptosporidiosis to humans.

Keywords

CryptosporidiumGiardiagenotypingsubtypingrodent

Information

Type
Research Article
Information
Parasitology , Volume 142 , Issue 6 , May 2015 , pp. 800 - 806
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

REFERENCES

Ajjampur, S. S., Liakath, F. B., Kannan, A., Rajendran, P., Sarkar, R., Moses, P. D., Simon, A., Agarwal, I., Mathew, A., O'Connor, R., Ward, H. and Kang, G. (2010). Multisite study of cryptosporidiosis in children with diarrhea in India. Journal of Clinical Microbiology 48, 2075–2081.Google Scholar
Alves, M., Xiao, L., Sulaiman, I., Lal, A. A., Matos, O. and Antunes, F. (2003). Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. Journal of Clinical Microbiology 41, 2744–2747.Google Scholar
Azami, M., Moghaddam, D. D., Salehi, R. and Salehi, M. (2007). The identification of Cryptosporidium species (protozoa) in Ifsahan, Iran by PCR-RFLP analysis of the 18S rRNA gene. Molekuliarnaia Biologiia 41, 934–939 (in Russian).Google Scholar
Backhans, A., Jacobson, M., Hansson, I., Lebbad, M., Lambertz, S. T., Gammelgard, E., Saager, M., Akande, O. and Fellström, C. (2013). Occurrence of pathogens in wild rodents caught on Swedish pig and chicken farms. Epidemiology and Infection 141, 1885–1891.Google Scholar
Bednarska, M., Bajer, A., Sinski, E., Girouard, A. S., Tamang, L.and Graczyk, T. K. (2007). Fluorescent in situ hybridization as a tool to retrospectively identify Cryptosporidium parvum and Giardia lamblia in samples from terrestrial mammalian wildlife. Parasitology Research 100, 455–460.Google Scholar
Bitto, A. and Aldras, A. (2009). Prevalence of Giardia and Cryptosporidium in muskrats in northeastern Pennsylvania and New Jersey. Journal of Environmental Health 71, 20–26.Google Scholar
Brikan, F. A., Salem, H. S., Beeching, N. and Hilal, N. (2008). Multilocus genetic analysis of Cryptosporidium isolates from Saudi Arabia. Journal of the Egyptian Society of Parasitology 38, 645–658.Google ScholarPubMed
Cacciò, S. M., De Giacomo, M. and Pozio, E. (2002). Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. International Journal for Parasitology 32, 1023–1030.Google Scholar
Cacciò, S. M., Beck, R., Lalle, M., Marinculic, A. and Pozio, E. (2008). Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. International Journal for Parasitology 38, 1523–1531.Google Scholar
Elwin, K., Hadfield, S. J., Robinson, G., Crouch, N. D. and Chalmers, R. M. (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.Google Scholar
Fayer, R., Santín, M., Trout, J. M., DeStefano, S., Koenen, K. and Kaur, T. (2006). Prevalence of Microsporidia, Cryptosporidium spp., and Giardia spp. in beavers (Castor canadensis) in Massachusetts. Journal of Zoo and Wildlife Medicine 37, 492–497.Google Scholar
Feng, Y. and Xiao, L. (2011). Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Reviews 24, 110–140.CrossRefGoogle ScholarPubMed
Fernández-Álvarez, Á., Martín-Alonso, A., Abreu-Acosta, N., Feliu, C., Hugot, J. P., Valladares, B. and Foronda, P. (2014). Identification of a novel assemblage G subgenotype and a zoonotic assemblage B in rodent isolates of Giardia duodenalis in the Canary Islands, Spain. Parasitology 141, 206–215.CrossRefGoogle Scholar
Gatei, W., Ashford, R. W., Beeching, N. J., Kamwati, S. K., Greensill, J. and Hart, C. A. (2002). Cryptosporidium muris infection in an HIV-infected adult, Kenya. Emerging Infectious Diseases 8, 204–206.Google Scholar
Gatei, W., Greensill, J., Ashford, R. W., Cuevas, L. E., Parry, C. M., Cunliffe, N. A., Beeching, N. J. and Hart, C. A. (2003). Molecular analysis of the 18S rRNA gene of Cryptosporidium parasites from patients with or without human immunodeficiency virus infections living in Kenya, Malawi, Brazil, the United Kingdom, and Vietnam. Journal of Clinical Microbiology 41, 1458–1462.Google Scholar
Gatei, W., Wamae, C. N., Mbae, C., Waruru, A., Mulinge, E., Waithera, T., Gatika, S. M., Kamwati, S. K., Revathi, G. and Hart, C. A. (2006). Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in Kenya. American Journal of Tropical Medicine and Hygiene 75, 78–82.Google Scholar
Guyot, K., Follet-Dumoulin, A., Lelievre, E., Sarfati, C., Rabodonirina, M., Nevez, G., Cailliez, J. C., Camus, D. and Dei-Cas, E. (2001). Molecular characterization of Cryptosporidium isolates obtained from humans in France. Journal of Clinical Microbiology 39, 3472–3480.Google Scholar
Helmy, Y. A., Krücken, J., Nöckler, K., von Samson-Himmelstjerna, G. and Zessin, K. H. (2013). Molecular epidemiology of Cryptosporidium in livestock animals and humans in the Ismailia province of Egypt. Veterinary Parasitology 193, 15–24.Google Scholar
Katsumata, T., Hosea, D., Ranuh, I. G., Uga, S., Yanagi, T. and Kohno, S. (2000). Short report: possible Cryptosporidium muris infection in humans. American Journal of Tropical Medicine and Hygiene 62, 70–72.Google Scholar
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.Google Scholar
Kvác, M., Hofmannová, L., Bertolino, S., Wauters, L., Tosi, G. and Modrý, D. (2008). Natural infection with two genotypes of Cryptosporidium in red squirrels (Sciurus vulgaris) in Italy. Folia Parasitologica 55, 95–99.Google Scholar
Kváč, M., Hofmannová, L., Hlásková, L., Květoňová, D., Vítovec, J., McEvoy, J. and Sak, B. (2014). Cryptosporidium erinacei n. sp. (Apicomplexa: Cryptosporidiidae) in hedgehogs. Veterinary Parasitology 201, 9–17.CrossRefGoogle Scholar
Lalle, M., Pozio, E., Capelli, G., Bruschi, F., Crotti, D. and Cacciò, S. M. (2005). Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. International Journal for Parasitology 35, 207–213.Google Scholar
Lasek-Nesselquist, E., Welch, D. M., Thompson, R. C., Steuart, R. F. and Sogin, M. L. (2009). Genetic exchange within and between assemblages of Giardia duodenalis . Journal of Eukaryotic Microbiology 56, 504–518.Google Scholar
Lebbad, M., Mattsson, J. G., Christensson, B., Ljungström, B., Backhans, A., Andersson, J. O. and Svärd, S. G. (2010). From mouse to moose: multilocus genotyping of Giardia isolates from various animal species. Veterinary Parasitology 168, 231–239.Google Scholar
Levecke, B., Meulemans, L., Dalemans, T., Casaert, S., Claerebout, E. and Geurden, T. (2011). Mixed Giardia duodenalis assemblage A, B, C and E infections in pet chinchillas (Chinchilla lanigera) in Flanders (Belgium). Veterinary Parasitology 177, 166–170.CrossRefGoogle Scholar
Li, N., Xiao, L., Wang, L., Zhao, S., Zhao, X., Duan, L., Guo, M., Liu, L. and Feng, Y. (2012). Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Neglected Tropical Diseases 6, e1809.Google Scholar
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 a). Cryptosporidium spp. in wild, laboratory, and pet rodents in China: prevalence and molecular characterization. Applied and Environmental Microbiology 75, 7692–7699.Google Scholar
Lv, C. C., Feng, C., Qi, M., Yang, H. Y., Jian, F. C., Ning, C. S. and Zhang, L. X. (2009 b). Investigation on the prevalence of gastrointestinal parasites in pet hamsters. Chinese Journal of Parasitology and Parasitic Diseases 27, 279–280 (in Chinese).Google ScholarPubMed
Mi, R., Wang, X., Li, C., Huang, Y., Zhou, P., Li, Z., Lei, M., Cai, J. and Chen, Z. (2013). Prevalence and genetic characterization of Cryptosporidium in yaks in Qinghai Province of China. PLoS One 8, e74985.Google Scholar
Muthusamy, D., Rao, S. S., Ramani, S., Monica, B., Banerjee, I., Abraham, O. C., Mathai, D. C., Primrose, B., Muliyil, J., Wanke, C. A., Ward, H. D. and Kang, G. (2006). Multilocus genotyping of Cryptosporidium sp. isolates from human immunodeficiency virus-infected individuals in South India. Journal of Clinical Microbiology 44, 632–634.Google Scholar
Nahrevanian, H. and Assmar, M. (2008). Cryptosporidiosis in immunocompromised patients in the Islamic Republic of Iran. Journal of Microbiology, Immunology and Infection 41, 74–77.Google Scholar
Nazemalhosseini-Mojarad, E., Haghighi, A., Taghipour, N., Keshavarz, A., Mohebi, S. R., Zali, M. R. and Xiao, L. (2011). Subtype analysis of Cryptosporidium parvum and Cryptosporidium hominis isolates from humans and cattle in Iran. Veterinary Parasitology 179, 250–252.Google Scholar
Ng-Hublin, J. S., Singleton, G. R. 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
Palmer, C. J., Xiao, L., Terashima, A., Guerra, H., Gotuzzo, E., Saldías, G., Bonilla, J. A., Zhou, L., Lindquist, A. and Upton, S. J. (2003). Cryptosporidium muris, a rodent pathogen, recovered from a human in Perú. Emerging Infectious Diseases 9, 1174–1176.Google Scholar
Paparini, A., Jackson, B., Ward, S., Young, S. and Ryan, U. M. (2012). Multiple Cryptosporidium genotypes detected in wild black rats (Rattus rattus) from northern Australia. Experimental Parasitology 131, 404–412.Google Scholar
Quílez, J., Torres, E., Chalmers, R. M., Hadfield, S. J., Del Cacho, E. and Sánchez-Acedo, C. (2008). Cryptosporidium genotypes and subtypes in lambs and goat kids in Spain. Applied and Environmental Microbiology 74, 6026–6031.Google Scholar
Rajendran, P., Ajjampur, S. S., Chidambaram, D., Kattula, D., Rajan, D. P., Ward, H. and Kang, G. (2011). Investigation of potential zoonotic transmission of cryptosporidiosis in southern India. American Journal of Tropical Medicine and Hygiene 85, 657–659.Google Scholar
Ren, X., Zhao, J., Zhang, L., Ning, C., Jian, F., Wang, R., Lv, C., Wang, Q., Arrowood, M. J. and Xiao, L. (2012). Cryptosporidium tyzzeri n. sp. (Apicomplexa: Cryptosporidiidae) in domestic mice (Mus musculus). Experimental Parasitology 130, 274–281.Google Scholar
Silva, S. O., Richtzenhain, L. J., Barros, I. N., Gomes, A. M., Silva, A. V., Kozerski, N. D., de Araújo Ceranto, J. B., Keid, L. B. and Soares, R. M. (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.Google Scholar
Smith, H. and Nichols, R. A. (2006). Zoonotic protozoa – food for thought. Parassitologia 48, 101–104.Google Scholar
Sodqi, M., Marih, L., Lahsen, A. O., Bensghir, R., Chakib, A., Himmich, H. and El Filali, K. M. (2012). Causes of death among 91 HIV-infected adults in the era of potent antiretroviral therapy. Presse Medicale 41, e386–e390.Google Scholar
Sprong, H., Cacciò, S. M., van der Giessen, J. W. and ZOOPNET Network and Partners (2009). Identification of zoonotic genotypes of Giardia duodenalis . PLoS Neglected Tropical Diseases 3, e558.Google Scholar
Sulaiman, I. M., Fayer, R., Bern, C., Gilman, R. H., Trout, J. M., Schantz, P. M., Das, P., Lal, A. A. and Xiao, L. (2003). Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis . Emerging Infectious Diseases 9, 1444–1452.Google Scholar
Tiangtip, R. and Jongwutiwes, S. (2002). Molecular analysis of Cryptosporidium species isolated from HIV-infected patients in Thailand. Tropical Medicine and International Health 7, 357–364.Google Scholar
Veronesi, F., Piergili Fioretti, D., Morganti, G., Bietta, A., Moretta, I., Moretti, A. and Traversa, D. (2012). Occurrence of Giardia duodenalis infection in chinchillas (Chincilla lanigera) from Italian breeding facilities. Research in Veterinary Science 93, 807–810.Google Scholar
Wang, L., Zhang, H., Zhao, X., Zhang, L., Zhang, G., Guo, M., Liu, L., Feng, Y. and Xiao, L. (2013). Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. Journal of Clinical Microbiology 51, 557–563.Google Scholar
Wang, R., Wang, H., Sun, Y., Zhang, L., Jian, F., Qi, M., Ning, C. and Xiao, L. (2011). Characteristics of Cryptosporidium transmission in preweaned dairy cattle in Henan, China. Journal of Clinical Microbiology 49, 1077–1082.Google Scholar
Wang, R., Zhang, L., Axén, C., Bjorkman, C., Jian, F., Amer, S., Liu, A., Feng, Y., Li, G., Lv, C., Zhao, Z., Qi, M., Dong, H., Wang, H., Sun, Y., Ning, C. and Xiao, L. (2014). Cryptosporidium parvum IId family: clonal population and dispersal from Western Asia to other geographical regions. Scientific Reports 4, 4208.Google Scholar
Wielinga, P. R., de Vries, A., van der Goot, T. H., Mank, T., Mars, M. H., Kortbeek, L. M. and van der Giessen, J. W. (2008). Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. International Journal for Parasitology 38, 809–817.Google Scholar
Xiao, L. (2010). Molecular epidemiology of cryptosporidiosis: an update. Experimental Parasitology 124, 80–89.Google Scholar
Xiao, L. and Fayer, R. (2008). Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. International Journal for Parasitology 38, 1239–1255.Google Scholar
Xiao, L., Morgan, U. M., Limor, J., Escalante, A., Arrowood, M., Shulaw, W., Thompson, R. C., Fayer, R. and Lal, A. A. (1999). Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Applied and Environmental Microbiology 65, 3386–3391.CrossRefGoogle ScholarPubMed
Xiao, L., Lal, A. A. and Jiang, J. (2004). Detection and differentiation of Cryptosporidium oocysts in water by PCR-RFLP. Methods in Molecular Biology 268, 163–176.Google Scholar
Ye, J., Xiao, L., Ma, J., Guo, M., Liu, L. and Feng, Y. (2012). Anthroponotic enteric parasites in monkeys in public park, China. Emerging Infectious Diseases 18, 1640–1643.Google Scholar
Zhang, W., Yang, F., Liu, A., Wang, R., Zhang, L., Shen, Y., Cao, J. and Ling, H. (2013) Prevalence and genetic characterizations of Cryptosporidium spp. in pre-weaned and post-weaned piglets in Heilongjiang Province, China. PLoS One 8, e67564.Google Scholar
Zhao, Y., Cheng, P., Gong, M. and Hou, B. (2010). Summary of mouse-spread diseases and measures to control them. Journal of Pathogen Biology 5, 378–380 (in Chinese).Google Scholar