Abstract
Giardia duodenalis is an intestinal protozoan that can infect both humans and animals, leading to public health issues and economic losses in the livestock industry. G. duodenalis has been reported to infect dairy cattle, but there is limited information available on large-scale dairy farms in Xinjiang, China. The study collected 749 fresh faecal samples from five large-scale cattle farms in Xinjiang, China. The study used a nested PCR assay of the small subunit ribosomal RNA (SSU rRNA*) gene to determine the presence of G. duodenalis. The results showed that 24.0% (180/749) of dairy cattle were positive for G. duodenalis, with the highest infection rate observed in pre-weaned calves (45.1%, 69/153). Among the 180 G. duodenalis positive samples, three assemblages were identified: assemblage E (n = 176), assemblage A (n = 3) and assemblage B (n = 1). Sixty-nine, 67 and 49 sequences were obtained for the beta-giardin (bg*) gene, the glutamate dehydrogenase (gdh*) gene and the triose phosphate isomerase (tpi*) gene, respectively. Thirteen novel sequences of assemblage E were identified, including five sequences from the bg* gene, four sequences from the gdh* gene and four sequences from the tpi* gene. This study found that 32 G. duodenalis assemblage E isolates formed 26 MLGs, indicating genetic variation and geographic isolation-based differentiation in bovine-derived G. duodenalis assemblage E. These findings provide fundamental insights into the genetic diversity of G. duodenalis in dairy cattle and can aid in the prevention and control of its occurrence in large-scale dairy cattle farms.
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Data availability
The nucleotide sequences reported in this study have been deposited in the GenBank database of the National Center for Biotechnology Information under accession numbers OR538008–OR538020.
References
Abdel-Moein KA, Saeed H (2016) The zoonotic potential of Giardia intestinalis assemblage E in rural settings. Parasitol Res 115:3197–3202. https://doi.org/10.1007/s00436-016-5081-7
Appelbee AJ, Frederick LM, Heitman TL, Olson ME (2003) Prevalence and genotyping of Giardia duodenalis from beef calves in Alberta, Canada. Vet Parasitol 112:289–294. https://doi.org/10.1016/s0304-4017(02)00422-3
Baroudi D, Khelef D, Hakem A, Abdelaziz A, Chen X, Lysen C, Roellig D, Xiao L (2017) Molecular characterization of zoonotic pathogens Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in calves in Algeria. Veterinary Parasitology, Regional Studies and Reports 8:66–69. https://doi.org/10.1016/j.vprsr.2017.02.005
Berrilli F, D’Alfonso R, Giangaspero A, Marangi M, Brandonisio O, Kaboré Y, Glé C, Cianfanelli C, Lauro R, Di Cave D (2012) Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Côte d’Ivoire: occurrence and evidence for environmental contamination. Trans R Soc Trop Med Hyg 106:191–195. https://doi.org/10.1016/j.trstmh.2011.12.005
Brooks-Pollock E, Keeling M (2009) Herd size and bovine tuberculosis persistence in cattle farms in Great Britain. Prev Vet Med 92:360–365. https://doi.org/10.1016/j.prevetmed.2009.08.022
Cacciò SM, Beck R, Lalle M, Marinculic A, Pozio E (2008) Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol 38:1523–1531. https://doi.org/10.1016/j.ijpara.2008.04.008
Coklin T, Farber J, Parrington L, Dixon B (2007) Prevalence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in dairy cattle in Ontario. Canada Vet Parasitol 150:297–305. https://doi.org/10.1016/j.vetpar.2007.09.014
Cui Z, Wang L, Cao L, Sun M, Liang N, Wang H, Chang Y, Lin X, Yu L, Wang R, Zhang S, Ning C, Zhang L (2018) Genetic characteristics and geographic segregation of Giardia duodenalis in dairy cattle from Guangdong Province, southern China. Infection, Infect Genet Evol 66:95–100. https://doi.org/10.1016/j.meegid.2018.09.019
Dan J, Zhang X, Ren Z, Wang L, Cao S, Shen L, Deng J, Zuo Z, Yu S, Wang Y, Ma X, Liu H, Zhou Z, Hu Y, Fu H, He C, Geng Y, Gu X, Peng G, Zhong Z (2019) Occurrence and multilocus genotyping of Giardia duodenalis from post-weaned dairy calves in Sichuan province. China Plos One 14:e0224627. https://doi.org/10.1371/journal.pone.0224627
Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM (2016) Identification of Giardia lamblia Assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis 214:1256–1259. https://doi.org/10.1093/infdis/jiw361
Feng Y, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24:110–140. https://doi.org/10.1128/CMR.00033-10
Fu Y, Dong H, Bian X, Qin Z, Han H, Lang J, Zhang J, Zhao G, Li J, Zhang L (2022) Molecular characterizations of Giardia duodenalis based on multilocus genotyping in sheep, goats, and beef cattle in Southwest Inner Mongolia. China Parasite 29:33. https://doi.org/10.1051/parasite/2022036
Geng HL, Yan WL, Wang JM, Meng JX, Zhang M, Zhao JX, Shang KM, Liu J, Liu WH (2023) Meta-analysis of the prevalence of Giardia duodenalis in sheep and goats in China. Microb Pathog 179:106097. https://doi.org/10.1016/j.micpath.2023.106097
Heng ZJ, Yang JF, Xie XY, Xu CR, Chen JR, Ma J, He JJ, Mao HM (2022) Prevalence and multilocus genotyping of Giardia duodenalis in Holstein cattle in Yunnan. China Front Vet Sci 9:949462. https://doi.org/10.3389/fvets.2022.949462
Heyworth MF (2016) Giardia duodenalis genetic assemblages and hosts. Parasite 23:13. https://doi.org/10.1051/parasite/2016013
Huang J, Yue D, Qi M, Wang R, Zhao J, Li J, Shi K, Wang M, Zhang L (2014) Prevalence and molecular characterization of Cryptosporidium spp and Giardia duodenalis in dairy cattle in Ningxia, northwestern China. BMC Vet Res 10:292. https://doi.org/10.1186/s12917-014-0292-6
Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Cacciò SM (2005) Genetic heterogeneity at the bata-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 35:207–213. https://doi.org/10.1016/j.ijpara.2004.10.022
Lam HYP, Chen TT, Tseng YC, Chang KC, Yang TH, Peng SY (2021) Detection and genotyping of Giardia duodenalis from cattle and pigs in Hualien country, Eastern Taiwan. J Microbiol Immunol Infec 54:718–727. https://doi.org/10.1016/j.jmii.2020.05.009
Liu G, Su Y, Zhou M, Zhao J, Zhang T, Ahmad W, Lu H, Jiang N, Chen Q, Xiang M, Yin J (2015) Prevalence and molecular characterization of Giardia duodenalis isolates from dairy cattle in northeast China. Exp Parasitol 154:20–24. https://doi.org/10.1016/j.exppara.2015.03.020
Meng XZ, Kang C, Wei J, Ma H, Liu G, Zhao JP, Zhang HS, Yang XB, Wang XY, Yang LH, Geng HL, Cao H (2023) Meta-analysis of the prevalence of Giardia duodenalis in cattle in China. Foodborne Pathog Dis 20:17–31. https://doi.org/10.1089/fpd.2022.0052
Nakao JH, Collier SA, Gargano JW (2017) Giardiasis and subsequent irritable bowel syndrome: a longitudinal cohort study using health insurance data. J Infect Dis 215:798–805. https://doi.org/10.1093/infdis/jiw621
O’Handley RM, Olson ME (2006) Giardiasis and cryptosporidiosis in ruminants. Vet Clin North Am Food Anim Pract 22:623–643. https://doi.org/10.1016/j.cvfa.2006.07.002
Painter JE, Collier SA, Gargano JW (2017) Association between Giardia and arthritis or joint pain in a large health insurance cohort: could it be reactive arthritis? Epidemiol Infect 145:471–477. https://doi.org/10.1017/S0950268816002120
Qi M, Wang H, Jing B, Wang R, Jian F, Ning C, Zhang L (2016) Prevalence and multilocus genotyping of Giardia duodenalis in dairy calves in Xinjiang. Northwestern China Parasite Vectors 9:546. https://doi.org/10.1186/s13071-016-1828-3
Robertson LJ (2009) Giardia and Cryptosporidium infections in sheep and goats: a review of the potential for transmission to humans via environmental contamination. Epidemiol Infect 137:913–921. https://doi.org/10.1017/S0950268809002295
Rojas-López L, Marques RC, Svärd SG (2022) Giardia duodenalis. Trends Parasitol 38:605–606. https://doi.org/10.1016/j.pt.2022.01.001
Ryan U, Cacciò SM (2013) Zoonotic potential of Giardia. Int J Parasitol 43:943–956. https://doi.org/10.1016/j.ijpara.2013.06.001
Ryan UM, Feng Y, Fayer R, Xiao L (2021) Taxonomy and molecular epidemiology of Cryptosporidium and Giardia—a 50 year perspective (1971–2021). Int J Parasitol 51:1099–1119. https://doi.org/10.1016/j.ijpara.2021.08.007
Santín M, Trout JM, Fayer R (2009) A longitudinal study of Giardia duodenalis genotypes in dairy cows from birth to 2 years of age. Vet Parasitol 162:40–45. https://doi.org/10.1016/j.vetpar.2009.02.008
Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM, Das P, Lal AA, Xiao L (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis 9:1444–1452. https://doi.org/10.3201/eid0911.030084
Taghipour A, Sharbatkhori M, Tohidi F, Ghanbari MR, Karanis P, Olfatifar M, Majidiani H, Khazaei S, Bahadory S, Javanmard E (2022) Global prevalence of Giardia duodenalis in cattle: a systematic review and meta-analysis. Prev Vet Med 203:105632. https://doi.org/10.1016/j.prevetmed.2022.105632
Tram NT, Phuc PD, Phi NH, Trang LT, Nga TT, Ha HTT, Cam PD, Canh TQ, Karanis P (2022) Cryptosporidium and Giardia in biogas wastewater: management of manure livestock and hygiene aspects using influent, effluent, sewage canal samples, vegetable, and soil samples. Pathogens 11:174. https://doi.org/10.3390/pathogens11020174
Wang H, Zhao G, Chen G, Jian F, Zhang S, Feng C, Wang R, Zhu J, Dong H, Hua J, Wang M, Zhang L (2014) Multilocus genotyping of Giardia duodenalis in dairy cattle in Henan. China Plos One 9:e100453. https://doi.org/10.1371/journal.pone.0100453
Wang X, Cai M, Jiang W, Wang Y, Jin Y, Li N, Guo Y, Feng Y, Xiao L (2017) High genetic diversity of Giardia duodenalis assemblage E in pre-weaned dairy calves in Shanghai, China, revealed by multilocus genotyping. Parasitol Res 116:2101–2110. https://doi.org/10.1007/s00436-017-5509-8
Wang R, Li N, Jiang W, Guo Y, Wang X, Jin Y, Feng Y, Xiao L (2019) Infection patterns, clinical significance, and genetic characteristics of Enterocytozoon bieneusi and Giardia duodenalis in dairy cattle in Jiangsu, China. Parasitol Res 118:3053–3060. https://doi.org/10.1007/s00436-019-06426-3
Zahedi A, Field D, Ryan U (2017) Molecular typing of Giardia duodenalis in humans in Queensland—first report of Assemblage E. Parasitology 144:1154–1161. https://doi.org/10.1017/S0031182017000439
Zhao L, Zhang ZS, Han WX, Yang B, Chai HL, Wang MY, Wang Y, Zhang S, Zhao WH, Ma YM, Zhan YJ, Wang LF, Ding YL, Wang JL, Liu YH (2023a) Prevalence and molecular characterization of Giardia duodenalis in dairy cattle in Central Inner Mongolia. Northern China Sci Rep 13:13960. https://doi.org/10.1038/s41598-023-40987-9
Zhao Q, Lu C, Pei Z, Gong P, Li J, Jian F, Jing B, Qi M, Ning C (2023b) Giardia duodenalis in Hu sheep: occurrence and environmental contamination on large-scale housing farms. Parasite 30:2. https://doi.org/10.1051/parasite/2023004
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This work was supported by the National Natural Science Foundation of China (31960704) and the Key Technologies R&D Programme of Xinjiang Production & Construction Corps (2020AB025).
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Bo Jing and Zhenjie Zhang contributed to the conception and design of the experiments. Meigui Huang performed the experiments. Bin Yang helped in interpretation of data. Qianming Zhao, Meng Qi and Chunyan Xu interpreted the results and drafted the manuscript. All of the authors read and approved the final version of the manuscript.
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Zhao, Q., Yang, B., Huang, M. et al. Molecular detection and genetic characteristics of Giardia duodenalis in dairy cattle from large-scale breeding farms in Xinjiang, China. Parasitol Res 123, 106 (2024). https://doi.org/10.1007/s00436-024-08123-2
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DOI: https://doi.org/10.1007/s00436-024-08123-2