Seasonal Prevalence and Novel Multilocus Genotypes of Giardia duodenalis in Yaks (Bos grunniens) in Qinghai Province, Western China
-
Jun-ke Song
,
Dan Wang
,
Mei Ren
,
Fan Yang
,
Pin-Xue Wang
,
Min Zou
,
Guang-hui Zhao
,
Qing Lin
Abstract
Background: Giardia duodenalis is an important opportunistic zoonotic intestinal protozoon, which could parasitize yaks. However, a few studies have been conducted on the seasonal infection of G. duodenalis in yaks in China.
Methods: Overall, 1,027 fecal samples were collected from yaks of two age groups in seven cities of Qinghai Province, China at four seasons between May 2016 and Sep 2017. The prevalence and assemblages were analyzed by nested PCR and multilocus sequence typing (MLST).
Results: The overall prevalence of G. duodenalis was 2.04% (21/1027) based on triose phosphate isomease (tpi) locus. No significant differences in prevalence of the organism in yaks were found among different sampling areas. Additionally, same result was also presented in different seasons. However, there was statistically significant difference between young yaks within 6 months (8.33%, 4/48) and adult yaks over 6 months (1.73%, 17/979). The assemblage A recognized as a zoonotic assemblage (n=3) was found in yaks (>6 months) from Xining, while assemblage E (n=18) was detected from yaks in six cities. There were 5, 2 and 3 G. duodenalis subtypes detected positive at the tpi, the β-giardin (bg), and the glutamate dehydrogenase (gdh) loci, with 2, 2 and 3 novel subtypes, respectively. Three samples were successfully sequenced at all three loci, forming 1 assemblages A multilocus genotype (MLG) and 2 assemblages E MLGs, not reported.
Conclusion: This study indicated a zoonotic potential of G. duodenalis in yaks from Qinghai Province and provides basic information about the epidemiology of G. duodenalis.
1. Lee MF, Cadogan P, Eytle S, et al. Molecu-lar epidemiology and multilocus sequence analysis of potentially zoonotic Giardia spp. from humans and dogs in Jamaica. Parasi-tol Res. 2017; 116(1): 409-14.
2. Di Cristanziano V, Santoro M, Parisi F, et al. Genetic characterization of Giardia duo-denalis by sequence analysis in humans and animals in Pemba Island, Tanzania. Parasi-tol Int. 2014; 63(2): 438-41.
3. Squire SA, Yang R, Robertson I et al. Mo-lecular characterization of Cryptosporidium and Giardia in farmers and their ruminant livestock from the Coastal Savannah zone of Ghana. Infect Genet Evol. 2017; 55: 236-43.
4. Zheng G, Alsarakibi M, Liu Y, et al. Genotyping of Giardia duodenalis isolates from dogs in Guangdong, China based on multi-locus sequence. Korean J Parasi-tol. 2014; 52(3): 299-304.
5. Faubert G. Immune response to Giardia duodenalis. Clin Microbiol Rev. 2000; 13(1): 35-54.
6. Xiao S, Li G, Wang B, et al. Molecular identification of the first isolate of calf-derived Giardia from mainland of China. Chinese Journal of Zoonoses. 2006; 22(9): 861-3.
7. Plutzer J, Ongerth J, Karanis P. Giardia taxonomy, phylogeny and epidemiology: Facts and open questions. Int J Hyg Envi-ron Health. 2010; 213(3): 321-33.
8. Heyworth MF. Giardia duodenalis genetic assemblages and hosts. Parasite. 2016; 23: 13.
9. Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol. 2013; 43(12-13): 943-56.
10. Aloisio F, Filippini G, Antenucci P, et al. Severe weight loss in lambs infected with Giardia duodenalis assemblage B. Vet Parasi-tol. 2006; 142(1-2):154-8.
11. Qi M, Cai J, Wang R, et al. Molecular char-acterization of Cryptosporidium spp. and Gi-ardia duodenalis from yaks in the central western region of China. BMC Microbiol. 2015; 15: 108.
12. Jin Y, Fei J, Cai J, et al. Multilocus genotyp-ing of Giardia duodenalis in Tibetan sheep and yaks in Qinghai, China. Vet Parasitol. 2017; 247: 70-6.
13. Thompson RC. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol. 2004; 126(1-2):15-35.
14. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24(1): 110-40.
15. Asher AJ, Hose G, Power ML. Giardiasis in NSW: Identification of Giardia duodenalis assemblages contributing to human and cattle cases, and an epidemiological as-sessment of sporadic human giardiasis. Infect Genet Evol. 2016; 44: 157-61.
16. Song G, Qin S, Zhao G et al. Molecular characterization of Giardia duodenalis from white yaks in China. Acta Parasitol. 2016, 61(2): 397-400.
17. Wang G, Wang G, Li X et al. Detection of Giardia duodenalis assemblage E infections at the Tibetan Plateau Area: Yaks are suita-ble hosts. Acta Trop. 2017; 169: 157-62.
18. Feng Y, Gong X, Zhu K, et al. Prevalence and genotypic identification of Cryptosporid-ium spp., Giardia duodenalis and Enterocytozoon bieneusi in pre-weaned dairy calves in Guangdong, China. Parasites & Vectors. 2019; 12(1): 41.
19. Jian Y, Zhang X, Li X, et al. Prevalence and molecular characterization of Giardia duodenalis in cattle and sheep from the Qinghai-Tibetan Plateau Area (QTPA), northwestern China. Vet Parasitol. 2018; 250: 40-4.
20. Wang G, Wang G, Li X, et al. Prevalence and molecular characterization of Cryptos-poridium spp. and Giardia duodenalis in 1-2-month-old highland yaks in Qinghai Prov-ince, China. Parasitol Res. 2018; 117(6): 1793-800.
21. Li K, Shahzad M, Zhang H, et al. Socio-economic burden of parasitic infections in yaks from 1984 to 2017 on Qinghai Tibet-an Plateau of China-A review. Acta Trop. 2018; 183: 103-9.
22. Wang H, Zhao G, Chen G, et al. Multi-locus genotyping of Giardia duodenalis in dairy cattle in Henan, China. PLoS One. 2014; 9(6): e100453.
23. Minetti C, Taweenan W, Hogg R et al. Oc-currence and diversity of Giardia duodenalis assemblages in livestock in the UK. Transbound Emerg Dis. 2014; 61(6): e60-7.
24. Hu S, Liu Z, Yan F, et al. Zoonotic and host-adapted genotypes of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in dairy cattle in Hebei and Tianjin, China. Vet Parasitol. 2017; 248: 68-73.
25. Zhang X, Tan Q, Zhao G, et al. Preva-lence, Risk Factors and Multilocus Geno-typing of Giardia intestinalis in Dairy Cattle, Northwest China. J Eukaryot Microbiol. 2016; 63(4): 498-504.
26. Wang X, Wang R, Ren G et al. Multilocus genotyping of Giardia duodenalis and Entero-cytozoon bieneusi in dairy and native beef (Qinchuan) calves in Shaanxi province, northwestern China. Parasitol Res. 2016; 115(3): 1355-61.
27. Fan Y, Wang T, Koehler AV, et al. Mo-lecular investigation of Cryptosporidium and Giardia in pre- and post-weaned calves in Hubei Province, China. Parasites & Vec-tors volume. 2017; 10(1): 519.
28. Li J, Wang H, Wang R, et al. Giardia duode-nalis Infections in Humans and Other An-imals in China. Front Microbiol. 2017; 8: 2004.
29. Cacciò SM, Ryan, U. Molecular epidemiol-ogy of giardiasis. Mol Biochem Parasitol. 2008; 160(2): 75-80.
30. Sulaiman IM, Fayer R, Bern C, et al. Tri-osephosphate isomerase gene characteriza-tion and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis. 2003; 9(11): 1444-52.
31. Gillhuber J, Pallant L, Ash A, et al. Mo-lecular identification of zoonotic and live-stock-specific Giardia-species in faecal samples of calves in Southern Germany. Parasit Vectors. 2013; 6(1): 346.
32. Lalle M, Jimenez-Cardosa E, Cacciò S M, et al. Genotyping of Giardia duodenalis from humans and dogs from Mexico using a beta-giardin nested polymerase chain reac-tion assay. J Parasitol. 2005; 91(1): 203-5.
33. Cacciò S M, Beck R, Lalle M, et al. Multi-locus genotyping of Giardia duodenalis re-veals striking differences between assem-blages A and B. Int J Parasitol. 2008; 38(13): 1523-31.
34. Wang X, Cai M, Jiang W, et al. High genet-ic diversity of Giardia duodenalis assemblage E in pre-weaned dairy calves in Shanghai, China, revealed by multilocus genotyping. Parasitol Res. 2017; 116(8): 2101-10.
35. Uehlinger FD, Greenwood SJ, O'Handley R, et al. Prevalence and genotypes of Giar-dia duodenalis in dairy and beef cattle in farms around Charlottetown, Prince Ed-ward Island, Canada. Can Vet J. 2011; 52(9): 967-72.
36. Kakandelwa C, Siwila J, Nalubamba KS, et al. Prevalence of Giardia in dairy cattle in Lusaka and Chilanga districts, Zambia. Vet Parasitol. 2016; 215: 114-6.
37. Huang J, Yue D, Qi M, et al. Prevalence and molecular characterization of Cryptos-poridium spp. and Giardia duodenalis in dairy cattle in Ningxia, northwestern China. BMC Vet Res. 2014; 10: 292.
38. Liu G, Su Y, Zhou M, et al. Prevalence and molecular characterization of Giardia duode-nalis isolates from dairy cattle in northeast China. Exp Parasitol. 2015; 154: 20-4.
39. Xiao L, Fayer R. Molecular characterization of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol. 2008; 38(11): 1239-55.
40. Volotão AC, Costa-Macedo LM, Haddad FS, et al. Genotyping of Giardia duodenalis from human and animal samples from Brazil using beta-giardin gene: a phyloge-netic analysis. Acta Trop. 2007; 102(1): 10-9.
41. Traversa D, Otranto D, Milillo P, et al. Giardia duodenalis sub-Assemblage of ani-mal and human origin in horses. Infect Genet Evol. 2012; 12(8): 1642-6.
42. Gomez-Puerta LA, Lopez-Urbina MT, Alarcon V, et al. Occurrence of Giardia du-odenalis assemblages in alpacas in the An-dean region. Parasitol Int. 2014; 63(1): 31-4.
2. Di Cristanziano V, Santoro M, Parisi F, et al. Genetic characterization of Giardia duo-denalis by sequence analysis in humans and animals in Pemba Island, Tanzania. Parasi-tol Int. 2014; 63(2): 438-41.
3. Squire SA, Yang R, Robertson I et al. Mo-lecular characterization of Cryptosporidium and Giardia in farmers and their ruminant livestock from the Coastal Savannah zone of Ghana. Infect Genet Evol. 2017; 55: 236-43.
4. Zheng G, Alsarakibi M, Liu Y, et al. Genotyping of Giardia duodenalis isolates from dogs in Guangdong, China based on multi-locus sequence. Korean J Parasi-tol. 2014; 52(3): 299-304.
5. Faubert G. Immune response to Giardia duodenalis. Clin Microbiol Rev. 2000; 13(1): 35-54.
6. Xiao S, Li G, Wang B, et al. Molecular identification of the first isolate of calf-derived Giardia from mainland of China. Chinese Journal of Zoonoses. 2006; 22(9): 861-3.
7. Plutzer J, Ongerth J, Karanis P. Giardia taxonomy, phylogeny and epidemiology: Facts and open questions. Int J Hyg Envi-ron Health. 2010; 213(3): 321-33.
8. Heyworth MF. Giardia duodenalis genetic assemblages and hosts. Parasite. 2016; 23: 13.
9. Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol. 2013; 43(12-13): 943-56.
10. Aloisio F, Filippini G, Antenucci P, et al. Severe weight loss in lambs infected with Giardia duodenalis assemblage B. Vet Parasi-tol. 2006; 142(1-2):154-8.
11. Qi M, Cai J, Wang R, et al. Molecular char-acterization of Cryptosporidium spp. and Gi-ardia duodenalis from yaks in the central western region of China. BMC Microbiol. 2015; 15: 108.
12. Jin Y, Fei J, Cai J, et al. Multilocus genotyp-ing of Giardia duodenalis in Tibetan sheep and yaks in Qinghai, China. Vet Parasitol. 2017; 247: 70-6.
13. Thompson RC. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol. 2004; 126(1-2):15-35.
14. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24(1): 110-40.
15. Asher AJ, Hose G, Power ML. Giardiasis in NSW: Identification of Giardia duodenalis assemblages contributing to human and cattle cases, and an epidemiological as-sessment of sporadic human giardiasis. Infect Genet Evol. 2016; 44: 157-61.
16. Song G, Qin S, Zhao G et al. Molecular characterization of Giardia duodenalis from white yaks in China. Acta Parasitol. 2016, 61(2): 397-400.
17. Wang G, Wang G, Li X et al. Detection of Giardia duodenalis assemblage E infections at the Tibetan Plateau Area: Yaks are suita-ble hosts. Acta Trop. 2017; 169: 157-62.
18. Feng Y, Gong X, Zhu K, et al. Prevalence and genotypic identification of Cryptosporid-ium spp., Giardia duodenalis and Enterocytozoon bieneusi in pre-weaned dairy calves in Guangdong, China. Parasites & Vectors. 2019; 12(1): 41.
19. Jian Y, Zhang X, Li X, et al. Prevalence and molecular characterization of Giardia duodenalis in cattle and sheep from the Qinghai-Tibetan Plateau Area (QTPA), northwestern China. Vet Parasitol. 2018; 250: 40-4.
20. Wang G, Wang G, Li X, et al. Prevalence and molecular characterization of Cryptos-poridium spp. and Giardia duodenalis in 1-2-month-old highland yaks in Qinghai Prov-ince, China. Parasitol Res. 2018; 117(6): 1793-800.
21. Li K, Shahzad M, Zhang H, et al. Socio-economic burden of parasitic infections in yaks from 1984 to 2017 on Qinghai Tibet-an Plateau of China-A review. Acta Trop. 2018; 183: 103-9.
22. Wang H, Zhao G, Chen G, et al. Multi-locus genotyping of Giardia duodenalis in dairy cattle in Henan, China. PLoS One. 2014; 9(6): e100453.
23. Minetti C, Taweenan W, Hogg R et al. Oc-currence and diversity of Giardia duodenalis assemblages in livestock in the UK. Transbound Emerg Dis. 2014; 61(6): e60-7.
24. Hu S, Liu Z, Yan F, et al. Zoonotic and host-adapted genotypes of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in dairy cattle in Hebei and Tianjin, China. Vet Parasitol. 2017; 248: 68-73.
25. Zhang X, Tan Q, Zhao G, et al. Preva-lence, Risk Factors and Multilocus Geno-typing of Giardia intestinalis in Dairy Cattle, Northwest China. J Eukaryot Microbiol. 2016; 63(4): 498-504.
26. Wang X, Wang R, Ren G et al. Multilocus genotyping of Giardia duodenalis and Entero-cytozoon bieneusi in dairy and native beef (Qinchuan) calves in Shaanxi province, northwestern China. Parasitol Res. 2016; 115(3): 1355-61.
27. Fan Y, Wang T, Koehler AV, et al. Mo-lecular investigation of Cryptosporidium and Giardia in pre- and post-weaned calves in Hubei Province, China. Parasites & Vec-tors volume. 2017; 10(1): 519.
28. Li J, Wang H, Wang R, et al. Giardia duode-nalis Infections in Humans and Other An-imals in China. Front Microbiol. 2017; 8: 2004.
29. Cacciò SM, Ryan, U. Molecular epidemiol-ogy of giardiasis. Mol Biochem Parasitol. 2008; 160(2): 75-80.
30. Sulaiman IM, Fayer R, Bern C, et al. Tri-osephosphate isomerase gene characteriza-tion and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis. 2003; 9(11): 1444-52.
31. Gillhuber J, Pallant L, Ash A, et al. Mo-lecular identification of zoonotic and live-stock-specific Giardia-species in faecal samples of calves in Southern Germany. Parasit Vectors. 2013; 6(1): 346.
32. Lalle M, Jimenez-Cardosa E, Cacciò S M, et al. Genotyping of Giardia duodenalis from humans and dogs from Mexico using a beta-giardin nested polymerase chain reac-tion assay. J Parasitol. 2005; 91(1): 203-5.
33. Cacciò S M, Beck R, Lalle M, et al. Multi-locus genotyping of Giardia duodenalis re-veals striking differences between assem-blages A and B. Int J Parasitol. 2008; 38(13): 1523-31.
34. Wang X, Cai M, Jiang W, et al. High genet-ic diversity of Giardia duodenalis assemblage E in pre-weaned dairy calves in Shanghai, China, revealed by multilocus genotyping. Parasitol Res. 2017; 116(8): 2101-10.
35. Uehlinger FD, Greenwood SJ, O'Handley R, et al. Prevalence and genotypes of Giar-dia duodenalis in dairy and beef cattle in farms around Charlottetown, Prince Ed-ward Island, Canada. Can Vet J. 2011; 52(9): 967-72.
36. Kakandelwa C, Siwila J, Nalubamba KS, et al. Prevalence of Giardia in dairy cattle in Lusaka and Chilanga districts, Zambia. Vet Parasitol. 2016; 215: 114-6.
37. Huang J, Yue D, Qi M, et al. Prevalence and molecular characterization of Cryptos-poridium spp. and Giardia duodenalis in dairy cattle in Ningxia, northwestern China. BMC Vet Res. 2014; 10: 292.
38. Liu G, Su Y, Zhou M, et al. Prevalence and molecular characterization of Giardia duode-nalis isolates from dairy cattle in northeast China. Exp Parasitol. 2015; 154: 20-4.
39. Xiao L, Fayer R. Molecular characterization of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol. 2008; 38(11): 1239-55.
40. Volotão AC, Costa-Macedo LM, Haddad FS, et al. Genotyping of Giardia duodenalis from human and animal samples from Brazil using beta-giardin gene: a phyloge-netic analysis. Acta Trop. 2007; 102(1): 10-9.
41. Traversa D, Otranto D, Milillo P, et al. Giardia duodenalis sub-Assemblage of ani-mal and human origin in horses. Infect Genet Evol. 2012; 12(8): 1642-6.
42. Gomez-Puerta LA, Lopez-Urbina MT, Alarcon V, et al. Occurrence of Giardia du-odenalis assemblages in alpacas in the An-dean region. Parasitol Int. 2014; 63(1): 31-4.
| Files | ||
| Issue | Vol 16 No 4 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v16i4.7865 | |
| Keywords | ||
| Giardia duodenalis Multilocus sequence typing (MLST) Yaks Prevalence | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Song J- ke, Wang D, Ren M, Yang F, Wang P-X, Zou M, Zhao G- hui, Lin Q. Seasonal Prevalence and Novel Multilocus Genotypes of Giardia duodenalis in Yaks (Bos grunniens) in Qinghai Province, Western China. Iran J Parasitol. 2021;16(4):548-554.
