The Prevalence of Cryptosporidium spp. and Giardia duodenalis in Marmota himalayana (Rodentia: Sciuridae) in the Qinghai Tibetan Plateau area, China
-
Liqing Ma
,
Yingna Jian
,
Guanghua Wang
,
Qigang Cai
,
Geping Wang
,
Xiuping Li
,
Xueyong Zhang
,
Panagiotis Karanis
Abstract
Background: Cryptosporidium and Giardia are well-known important intestinal zoonotic pathogens that can infect various hosts and cause diarrhoeal diseases. We aimed to determine the epidemiological prevalence and molecular characterization of Cryptosporidium and Giardia species in Himalayan marmot (Marmota himalayana, class Marmota) in the Qinghai Tibetan Plateau Area of Qinghai Province, Northwest China.
Methods: Overall, 243 Himalayan marmot fecal samples were collected in 2017 and in 2019 and a two-step nested PCR technique was performed to amplify the fragments of the SSU rRNA gene of Cryptosporidium and 18S ribosomal RNA gene of Giardia. Molecular characterization of Cryptosporidium was performed with the primary primers N-DIAGF2 and N-DIAGR2, the secondary primers CPB-DIAGF and CPB-DIAGR. Similarly, molecular characterization of Giardia was used the first primers Gia2029 and Gia2150c, the secondary primers RH11 and RH4. The positive PCR products were sequenced and the sequences were processed by Clustal Omega and BLAST. Phylogenetic analysis was achieved by NJ method in MEGA.
Results: The infection rate of Cryptosporidium spp. and G. duodenalis was 4.9% (12/243) and 0.8% (2/243) in M. himalayana, respectively. Cryptosporidium spp. are characterized as novel genotypes Cryptosporidium marmot genotype I (n=3) and Cryptosporidium marmot genotype II (n=9); G. duodenalis assemblage A (n=2) was found in M. himalayana.
Conclusion: This is the first report of Cryptosporidium spp. and G. duodenalis infections in M. himalayana in Qinghai of Northwest China. The results indicate the existence of Cryptosporidium species and G. duodenalis infections that may have a potential public health significance.
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17. Koehler AV, Haydon SR, Jex AR, et al. Cryptosporidium and Giardia taxa in faecal samples from animals in catchments supplying the city of Melbourne with drinking water (2011 to 2015). Parasit Vector. 2016; 9(1):315.
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22. Ao YY, Yu JM, Li LL, et al. Diverse novel astroviruses identified in wild Himalayan marmots. J Gen Virol. 2017; 98(4):612-623.
23. Dai X, Shang G, Lu S, et al. A new subtype of eastern tick-borne encephalitis virus discovered in Qinghai-Tibet Plateau, China. Emerg Microbes Infect. 2018; 7(1):74.
24. Ge P, Xi J, Ding J, et al. Primary case of human pneumonic plague occurring in a Himalayan marmot natural focus area Gansu Province, China. Int J Infect Dis. 2015; 33:67-70.
25. Niu L, Hu S, Lu S, et al. Isolation and characterization of Streptococcus respiraculi sp. nov. from Marmota himalayana (Himalayan marmot) respiratory tract. Int J Syst Evol Microbiol. 2018; 68(6):2082-2087.
26. Bai L, Liu B, Ji C, et al. Hypoxic and cold adaptation insights from the Himalayan marmot genome. iScience. 2019; 11:519-530.
27. Karanis P, Plutzer J, Halim NA, et al. Molecular characterization of Cryptosporidium from animal sources in Qinghai province of China. Parasitol Res. 2007; 101(6):1575-1580.
28. Nichols RA, Campbell BM, Smith HV. Identification of Cryptosporidium spp. oocysts in United Kingdom noncarbonated natural mineral waters and drinking waters by using a modified nested PCR-restriction fragment length polymorphism assay. Appl Environ Microbiol. 2003; 69(7):4183-4189.
29. Appelbee AJ, Frederick LM, Heitman TL, et al. Prevalence and genotyping of Giardia duodenalis from beef calves in Alberta, Canada. Vet Parasitol. 2003; 112(4):289-294.
30. Zhao Z, Wang R, Zhao W, et al. Genotyping and subtyping of Giardia and Cryptosporidium isolates from commensal rodents in China. Parasitol. 2015; 142(6):800-806.
31. Perec-Matysiak A, Bunkowska-Gawlik K, Zalesny G, et al. Small rodents as reservoirs of Cryptosporidium spp. and Giardia spp. in south-western Poland. Ann Agric Environ Med. 2015; 22(1):1-5.
32. Kilonzo C, Li X, Vodoz T, et al. Quantitative shedding of multiple genotypes of Cryptosporidium and Giardia by deer mice (Peromyscus maniculatus) in a major agricultural region on the California central coast. J Food Prot. 2017; 80(5):819-828.
33. Rasambainarivo FT, Gillespie TR, Wright PC, et al. Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar. J Wildl Dis. 2013; 49(3):741-743.
34. Montecino-Latorre D, Li X, Xiao C, et al. Elevation and vegetation determine Cryptosporidium oocyst shedding by yellow-bellied marmots (Marmota flaviventris) in the Sierra Nevada Mountains. Int J Parasitol Parasites Wildl. 2015; 4(2):171-177.
2. Xiao L. Overview of Cryptosporidium presentations at the 10th International Workshops on Opportunistic Protists. Eukaryot Cell. 2009; 8(4):429-436.
3. Plutzer J, Törökné A, Karanis P. Combination of ARAD microfibre filtration and LAMP methodology for simple, rapid and cost-effective detection of human pathogenic Giardia duodenalis and Cryptosporidium spp. in drinking water. Lett Appl Microbiol. 2010; 50(1):82-88.
4. Karanis P, Kourenti C, Smith H. Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health. 2007; 5(1):1-38.
5. Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010. Water Res. 2011; 45(20):6603-6614.
6. Efstratiou A, Ongerth JE, Karanis P. Waterborne transmission of protozoan parasites: Review of worldwide outbreaks - An update 2011-2016. Water Res. 2017; 114:14-22.
7. Ahmed SA, Karanis P. An overview of methods/techniques for the detection of Cryptosporidium in food samples. Parasitol Res. 2018; 117(3):629-653.
8. Ryan U, Hijjawi N, Xiao L. Foodborne cryptosporidiosis. Int J Parasitol. 2018; 48(1):1-12.
9. Bajer A. Cryptosporidium and Giardia spp. infections in humans, animals and the environment in Poland. Parasitol Res. 2008; 104(1):1-17.
10. Itagaki T, Kinoshita S, Aoki M, et al. Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamete dehydrogenase gene sequencing. Vet Parasitol. 2005; 133(4):283-287.
11. Oates SC, Miller MA, Hardin D, et al. Prevalence, environmental loading, and molecular characterization of Cryptosporidium and Giardia isolates from domestic and wild animals along the Central California Coast. Appl Environ Microb. 2012; 78(24):8762-8772.
12. Robertson LJ, Forberg T, Hermansen L, et al. Giardia duodenalis cysts isolated from wild moose and reindeer in Norway: Genetic characterization by PCR-rflp and sequence analysis at two genes. J Wildl Dis. 2007; 43(4):576-585.
13. Ziegler PE, Wade SE, Schaaf SL, et al. Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York State. Vet Parasitol. 2007; 147(1-2):176-184.
14. Ryan U, Fayer R, Xiao L. Cryptosporidium species in humans and animals: Current understanding and research needs. Parasitol. 2014; 141(13):1667-1685.
15. Plutzer J, Karanis P. Genetic polymorphism in Cryptosporidium species: an update. Vet Parasitol. 2009; 165(3-4):187-199.
16. Ryan U, Zahedi A, Paparini A. Cryptosporidium in humans and animals-a one health approach to prophylaxis. Parasite Immunol. 2016; 38(9):535-547.
17. Koehler AV, Haydon SR, Jex AR, et al. Cryptosporidium and Giardia taxa in faecal samples from animals in catchments supplying the city of Melbourne with drinking water (2011 to 2015). Parasit Vector. 2016; 9(1):315.
18. Ryan UM, Feng Y, Fayer R, et al. Taxonomy and molecular epidemiology of Cryptosporidium and Giardia - a 50 year perspective (1971-2021). Int J Parasitol. 2021; 51(13-14):1099-1119.
19. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24(1):110-140.
20. Caccio SM, Ryan U. Molecular epidemiology of giardiasis. Mol Biochem Parasitol. 2008; 160(2):75-80.
21. Plutzer J, Ongerth J, Karanis P. Giardia taxonomy, phylogeny and epidemiology: Facts and open questions. Int J Hyg Environ Health. 2010; 213(5):321-333.
22. Ao YY, Yu JM, Li LL, et al. Diverse novel astroviruses identified in wild Himalayan marmots. J Gen Virol. 2017; 98(4):612-623.
23. Dai X, Shang G, Lu S, et al. A new subtype of eastern tick-borne encephalitis virus discovered in Qinghai-Tibet Plateau, China. Emerg Microbes Infect. 2018; 7(1):74.
24. Ge P, Xi J, Ding J, et al. Primary case of human pneumonic plague occurring in a Himalayan marmot natural focus area Gansu Province, China. Int J Infect Dis. 2015; 33:67-70.
25. Niu L, Hu S, Lu S, et al. Isolation and characterization of Streptococcus respiraculi sp. nov. from Marmota himalayana (Himalayan marmot) respiratory tract. Int J Syst Evol Microbiol. 2018; 68(6):2082-2087.
26. Bai L, Liu B, Ji C, et al. Hypoxic and cold adaptation insights from the Himalayan marmot genome. iScience. 2019; 11:519-530.
27. Karanis P, Plutzer J, Halim NA, et al. Molecular characterization of Cryptosporidium from animal sources in Qinghai province of China. Parasitol Res. 2007; 101(6):1575-1580.
28. Nichols RA, Campbell BM, Smith HV. Identification of Cryptosporidium spp. oocysts in United Kingdom noncarbonated natural mineral waters and drinking waters by using a modified nested PCR-restriction fragment length polymorphism assay. Appl Environ Microbiol. 2003; 69(7):4183-4189.
29. Appelbee AJ, Frederick LM, Heitman TL, et al. Prevalence and genotyping of Giardia duodenalis from beef calves in Alberta, Canada. Vet Parasitol. 2003; 112(4):289-294.
30. Zhao Z, Wang R, Zhao W, et al. Genotyping and subtyping of Giardia and Cryptosporidium isolates from commensal rodents in China. Parasitol. 2015; 142(6):800-806.
31. Perec-Matysiak A, Bunkowska-Gawlik K, Zalesny G, et al. Small rodents as reservoirs of Cryptosporidium spp. and Giardia spp. in south-western Poland. Ann Agric Environ Med. 2015; 22(1):1-5.
32. Kilonzo C, Li X, Vodoz T, et al. Quantitative shedding of multiple genotypes of Cryptosporidium and Giardia by deer mice (Peromyscus maniculatus) in a major agricultural region on the California central coast. J Food Prot. 2017; 80(5):819-828.
33. Rasambainarivo FT, Gillespie TR, Wright PC, et al. Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar. J Wildl Dis. 2013; 49(3):741-743.
34. Montecino-Latorre D, Li X, Xiao C, et al. Elevation and vegetation determine Cryptosporidium oocyst shedding by yellow-bellied marmots (Marmota flaviventris) in the Sierra Nevada Mountains. Int J Parasitol Parasites Wildl. 2015; 4(2):171-177.
| Files | ||
| Issue | Vol 19 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i2.15852 | |
| Keywords | ||
| Cryptosporidium Giardia Genotype Molecular prevalence China | ||
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How to Cite
1.
Ma L, Jian Y, Wang G, Cai Q, Wang G, Li X, Zhang X, Karanis P. The Prevalence of Cryptosporidium spp. and Giardia duodenalis in Marmota himalayana (Rodentia: Sciuridae) in the Qinghai Tibetan Plateau area, China. Iran J Parasitol. 2024;19(2):162-170.
