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High genetic diversity of Giardia duodenalis assemblage E in pre-weaned dairy calves in Shanghai, China, revealed by multilocus genoty**

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Abstract

Giardia duodenalis is a common parasitic protozoan in human and animals. Epidemiological and molecular data are available from dairy cattle in many industrialized countries, but information on genetic diversity at multiple genetic loci is limited, especially in pre-weaned dairy calves. In this study, 818 fecal specimens were collected from five dairy cattle farms located in suburbs of Shanghai, China, with two to five samplings per farm. G. duodenalis assemblages and subtypes were determined using multilocus genoty** (MLG) at the β-giardin (bg), glutamate dehydrogenase (gdh), and triosephosphate isomerase (tpi) loci. The overall prevalence was 60.1% (492/818) combining data from the three genetic loci. Three G. duodenalis assemblages were detected, including E (n = 482), A (n = 5), and B (n = 1), with the concurrence of A and E in a few animals (n = 4). Intra-genotypic sequence diversity was high for assemblage E, showing 12, 13, and 17 subtypes at the bg, gdh, and tpi loci, including four, six, and eight new subtypes, respectively. All dominant subtypes (E3, E2, and E8 at the bg locus; E1 and E3 at the gdh locus; and E11 and E3 at the tpi locus) were detected on all farms at most sampling occasions, and only limited differences in subtype distribution were observed among five farms. Altogether, 58 assemblage E MLGs were identified, all of which had not been reported before, and seven (MLG-E1–MLG-E7) were each seen on multiple farms. These results indicate a high occurrence of G. duodenalis in dairy calves, the existence of high genetic heterogeneity of assemblage E on five farms, and frequent exchange of parasite populations among farms within a small geographic area. The clinical and epidemiologic significance of these observations warrants further investigations.

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References

  • Aguiar JM, Silva SO, dos Santos VA, Taniwaki SA, Oliveira TMFD, Ferreira HL, Keid LB, Gregori F, Soares RM (2016) Evidence of heterozygosity and recombinant alleles in single cysts of Giardia duodenalis. Rev Bras Parasitol 25:187–195

    Article  Google Scholar 

  • Asher AJ, Hose G, Power ML (2016) Giardiasis in NSW: identification of Giardia duodenalis assemblages contributing to human and cattle cases, and an epidemiological assessment of sporadic human giardiasis. Infect Genet Evol 44:157–161

    Article  CAS  PubMed  Google Scholar 

  • Becher KA, Robertson ID, Fraser DM, Palmer DG, Thompson RC (2004) Molecular epidemiology of Giardia and Cryptosporidium infections in dairy calves originating from three sources in Western Australia. Vet Parasitol 123:1–9

    Article  CAS  PubMed  Google Scholar 

  • Caccio SM, Sprong H (2010) Giardia duodenalis: genetic recombination and its implications for taxonomy and molecular epidemiology. Exp Parasitol 124:107–112

    Article  CAS  PubMed  Google Scholar 

  • Caccio SM, Beck R, Lalle M, Marinculic A, Pozio E (2008) Multilocus genoty** of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol 38:1523–1531

    Article  CAS  PubMed  Google Scholar 

  • Cardona GA, de Lucio A, Ballo B, Cano L, de Fuentes I, Carmena D (2015) Unexpected finding of feline-specific Giardia duodenalis assemblage F and Cryptosporidium felis in asymptomatic adult cattle in Northern Spain. Vet Parasitol 209:258–263

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Di Giovanni GD, Betancourt WQ, Hernandez J, Assadian NW, Margez JPF, Lopez EJ (2006) Investigation of potential zooanthroponotic transmission of cryptosporidiosis and giardiasis through agricultural use of reclaimed wastewater. Int J Environ Heath Res 16:405–418

    Article  CAS  Google Scholar 

  • Dixon B, Parrington L, Cook A, Pintar K, Pollari F, Kelton D, Farber J (2011) The potential for zoonotic transmission of Giardia duodenalis and Cryptosporidium spp. from beef and dairy cattle in Ontario, Canada. Vet Parasitol 175:20–26

    Article  PubMed  Google Scholar 

  • Fayer R, Trout JM, Graczyk TK, Lewis EJ (2000) Prevalence of Cryptosporidium, Giardia and Eimeria infections in post-weaned and adult cattle on three Maryland farms. Vet Parasitol 9:103–112

    Article  Google Scholar 

  • Feng Y, **ao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24:110–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Ortega Y, Cama V, Terrell J, **ao L (2008) High intragenotypic diversity of Giardia duodenalis in dairy cattle on three farms. Parasitol Res 103:87–92

    Article  PubMed  Google Scholar 

  • Geurden T, Geldhof P, Levecke B, Martens C, Berkvens D, Casaert S, Vercruysse J, Claerebout E (2008) Mixed Giardia duodenalis assemblage a and E infections in calves. Int J Parasitol 38:259–264

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Yue D, Qi M, Wang R, Zhao J, Li JQ, 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Kakandelwa C, Siwila J, Nalubamba KS, Muma JB, Phiri IGK (2016) Prevalence of Giardia in dairy cattle in Lusaka and Chilanga districts, Zambia. Vet Parasitol 215:114–116

    Article  PubMed  Google Scholar 

  • Karim MR, Zhang S, Jian F, Li J, Zhou C, Zhang L, Sun M, Yang G, Zou F et al (2014) Multilocus ty** of Cryptosporidium spp. and Giardia duodenalis from non-human primates in China. Int J Parasitol 44:1039–1047

    Article  CAS  PubMed  Google Scholar 

  • Lalle M, Jimenez-Cardosa E, Caccio SM, Pozio E (2005) Genoty** of Giardia duodenalis from humans and dogs from Mexico using a beta-giardin nested polymerase chain reaction assay. J Parasitol 91:203–205

    Article  CAS  PubMed  Google Scholar 

  • Lebbad M, Mattsson JG, Christensson B, Ljungstrom B, Backhans A, Andersson JO, Svard SG (2010) From mouse to moose: multilocus genoty** of Giardia isolates from various animal species. Vet Parasitol 168:231–239

    Article  PubMed  Google Scholar 

  • Lebbad M, Petersson I, Karlsson L, Botero-Kleiven S, Andersson JO, Svenungsson B, Svard SG (2011) Multilocus genoty** of human Giardia isolates suggests limited zoonotic transmission and association between assemblage B and flatulence in children. PLoS Negl Trop Dis 5(8):e1262

    Article  PubMed  PubMed Central  Google Scholar 

  • Li F, Wang H, Zhang Z, Li J, Wang C, Zhao J, Hu S, Wang R, Zhang L et al (2016) Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in dairy cattle in Bei**g, China. Vet Parasitol 228:69–69

    Article  PubMed  Google Scholar 

  • Liu A, Zhang X, Zhang L, Wang R, Li X, Shu J, Zhang X, Shen Y, Zhang W et al (2012) Occurrence of bovine giardiasis and endemic genetic characterization of Giardia duodenalis isolates in Heilongjiang Province, in the northeast of China. Parasitol Res 111:655–661

    Article  PubMed  Google Scholar 

  • Liu G, Su Y, Zhou M, Zhao J, Zhang T, Ahmad W, Lu H, Jiang N, Chen Q et al (2015) Prevalence and molecular characterization of Giardia duodenalis isolates from dairy cattle in northeast China. Exp Parasitol 154:20–24

    Article  CAS  PubMed  Google Scholar 

  • Qi M, Cai J, Wang R, Li J, Jian F, Huang J, Zhou H, Zhang L (2015) Molecular characterization of Cryptosporidium spp. and Giardia duodenalis from yaks in the central western region of China. BMC Microbiol 15:1–7

    Article  Google Scholar 

  • Qi M, Wang H, **g B, Wang R, Jian F, Ning C, Zhang L (2016) Prevalence and multilocus genoty** of Giardia duodenalis in dairy calves in **njiang, northwestern China. Parasit Vectors 9:546

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiz A, Foronda P, Gonzalez JF, Guedes A, Abreu-Acosta N, Molina JM, Valladares B (2008) Occurrence and genotype characterization of Giardia duodenalis in goat kids from the Canary Islands, Spain. Vet Parasitol 154:137–141

    Article  CAS  PubMed  Google Scholar 

  • Ryan U, Caccio SM (2013) Zoonotic potential of Giardia. Int J Parasitol 43:943–956

    Article  CAS  PubMed  Google Scholar 

  • Santin M, Dargatz D, Fayer R (2012) Prevalence of Giardia duodenalis assemblages in weaned cattle on cow-calf operations in the United States. Vet Parasitol 183:231–236

    Article  PubMed  Google Scholar 

  • Scalia LAM, Fava NMN, Soares RM, Limongi JE, da Cunha MJR, Pena IF, Kalapothakis E, Cury MC (2016) Multilocus genoty** of Giardia duodenalis in Brazilian children. Trans R Soc Trop Med Hyg 110:343–349

    Article  PubMed  Google Scholar 

  • Silva FMPE, Lopes RS, Araujo JP (2012) Genetic characterisation of Giardia duodenalis in dairy cattle in Brazil. Folia Parasitol 59:15–20

    Article  Google Scholar 

  • Solarczyk P, Majewska AC, Moskwa B, Cabaj W, Dabert M, Nowosad P (2012) Multilocus genoty** of Giardia duodenalis isolates from red deer (Cervus elaphus) and roe deer (Capreolus capreolus) from Poland. Folia Parasitol 59:237–240

    Article  PubMed  Google Scholar 

  • Thompson RCA, Ash A (2016) Molecular epidemiology of Giardia and Cryptosporidium infections. Infect Genet Evol 40:315–323

    Article  CAS  PubMed  Google Scholar 

  • Trout JM, Santin M, Greiner E, Fayer R (2004) Prevalence of Giardia duodenalis genotypes in pre-weaned dairy calves. Vet Parasitol 124:179–186

    Article  PubMed  Google Scholar 

  • Uehlinger FD, Greenwood SJ, O’Handley R, McClure JT, Coklin T, Dixon BR, de Boer M, Zwiers H, Barkema HW (2011) Prevalence and genotypes of Giardia duodenalis in dairy and beef cattle in farms around Charlottetown, Prince Edward Island, Canada. Can Vet J 52:967–972

    PubMed  PubMed Central  Google Scholar 

  • Wang H, Zhao G, Chen G, Jian F, Zhang S, Feng C, Wang R, Zhu J, Dong H et al (2014) Multilocus genoty** of Giardia duodenalis in dairy cattle in Henan, China. PLoS One 9(6):e100453

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang H, Qi M, Zhang K, Li JQ, Huang J, Ning C, Zhang L (2016a) Prevalence and genoty** of Giardia duodenalis isolated from sheep in Henan Province, central China. Infect Genet Evol 39:330–335

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang R, Ren G, Yu Z, Zhang L, Zhang S, Lu H, Peng X, Zhao G (2016b) Multilocus genoty** of Giardia duodenalis and Enterocytozoon bieneusi in dairy and native beef (Qinchuan) calves in Shaanxi province, northwestern China. Parasitol Res 115:1355–1361

    Article  CAS  PubMed  Google Scholar 

  • Wegayehu T, Karim MR, Erko B, Zhang L, Tilahun G (2016) Multilocus genoty** of Giardia duodenalis isolates from calves in Oromia special zone, Central Ethiopia. Infect Genet Evol 43:281–288

    Article  PubMed  Google Scholar 

  • Winkworth CL, Learmonth JJ, Matthaei CD, Townsend CR (2008) Molecular characterization of Giardia isolates from calves and humans in a region in which dairy farming has recently intensified. Appl Environ Microbiol 74:5100–5105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye J, **ao L, Wang Y, Guo Y, Roellig DM, Feng Y (2015) Dominance of Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotype BEB6 in sheep in Inner Mongolia, China. Vet Parasitol 210:235–239

    Article  PubMed  Google Scholar 

  • Zhang X, Tan Q, Zhao G, Ma J, Zheng W, Ni X, Zhao Q, Zhou D, Zhu X (2016) Prevalence, risk factors and multilocus genoty** of Giardia intestinalis in dairy cattle, Northwest China. J Eukaryot Microbiol 63:498–504

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31630078, 31425025, and 31602042), the China Postdoctoral Science Foundation (2016M601531), and the Fundamental Research Funds for the Central Universities, China (WB1714039).

The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

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Correspondence to Yaoyu Feng.

Ethics declarations

This study was approved by the Ethic Committee of the East China University of Science and Technology (Permit No. 2015015 approved on January 3, 2015). The dairy calves were handled in accordance with the Animal Ethics Procedures and Guidelines of the People’s Republic of China. Permissions were obtained from the management of dairy farms before specimen collections.

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  • DOI: https://doi.org/10.1007/s00436-017-5509-8

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