Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Prevalence and Multilocus Genotyping of Giardia lamblia in Cattle in Jiangxi Province, China: Novel Assemblage E Subtypes Identified

  • Li, Sen (Jiangxi Provincial Key Laboratory for Animal Health, College of Animal Science and Technology, Jiangxi Agricultural University) ;
  • Zou, Yang (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Xue-Liang (Nanchang Bureau of Agriculture and Rural Affairs) ;
  • Wang, Ping (Jiangxi Provincial Key Laboratory for Animal Health, College of Animal Science and Technology, Jiangxi Agricultural University) ;
  • Chen, Xiao-Qing (Jiangxi Provincial Key Laboratory for Animal Health, College of Animal Science and Technology, Jiangxi Agricultural University) ;
  • Zhu, Xing-Quan (State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences)
  • Received : 2020.08.17
  • Accepted : 2020.11.08
  • Published : 2020.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Giardia lamblia is a common enteric pathogen associated with diarrheal diseases. There are some reports of G. lamblia infection among different breeds of cattle in recent years worldwide. However, it is yet to know whether cattle in Jiangxi province, southeastern China is infected with G. lamblia. The objectives of the present study were to investigate the prevalence and examine the multilocus genotypes of G. lamblia in cattle in Jiangxi province. A total of 556 fecal samples were collected from 3 cattle breeds (dairy cattle, beef cattle, and buffalo) in Jiangxi province, and the prevalence and genotypes of G. lamblia were determined by the nested PCR amplification of the beta-giardin (bg) gene. A total of 52 samples (9.2%) were positive for G. lamblia. The highest prevalence of G. lamblia was detected in dairy cattle (20.0%), followed by that in beef cattle (6.4%), and meat buffalo (0.9%). Multilocus sequence typing of G. lamblia was performed based on sequences of the bg, triose phosphate isomerase and glutamate dehydrogenase loci, and 22, 42, and 52 samples were amplifiable, respectively, forming 15 MLGs. Moreover, one mixed G. lamblia infection (assemblages A and E) was found in the present study. Altogether, 6 novel assemblage E subtypes (E41*-E46*) were identified for the first time. These results not only provided baseline data for the control of G. lamblia infection in cattle in this southeastern province of China, but also enriched the molecular epidemiological data and genetic diversity of G. lamblia in cattle.

Keywords

References

  1. Feng YY, Xiao LH. Zoonotic potential and molecular epidemiology of Giardia species and Giardiasis. Clin Microbiol Rev 2011; 24: 110-140. https://doi.org/10.1128/CMR.00033-10
  2. Bartelt LA, Sartor RB. Advances in understanding Giardia: determinants and mechanisms of chronic sequelae. F1000Prime Rep 2015; 7: 62. https://doi.org/10.12703/P7-62
  3. Ryan U, Caccio SM. Zoonotic potential of Giardia. Int J Parasitol 2013; 43: 110-140. https://doi.org/10.1016/j.ijpara.2013.06.001
  4. Thompson RCA, Ash A. Molecular epidemiology of Giardia and Cryptosporidium infections. Infect Genet Evol 2016; 40: 315-323. https://doi.org/10.1016/j.meegid.2015.09.028
  5. Abdel-Moein KA, Saeed H. The zoonotic potential of Giardia intestinalis assemblage E in rural settings. Parasitol Res 2016; 115: 3197-3202. https://doi.org/10.1007/s00436-016-5081-7
  6. Hogan JN, Miller WA, Cranfield MR, Ramer J, Hassell J, Noheri JB, Conrad PA, Gilardi KV. Giardia in mountain gorillas (Gorilla beringei beringei), forest buffalo (Syncerus caffer), and domestic cattle in Volcanoes National Park, Rwanda. J Wildl Dis 2014; 50: 21-30. https://doi.org/10.7589/2012-09-229
  7. Feng Y, Gong X, Zhu K, Li N, Yu Z, Guo Y, Weng Y, Kvac M, Feng Y, Xiao L. Prevalence and genotypic identification of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in preweaned dairy calves in Guangdong, China. Parasit Vectors 2019; 12: 41. https://doi.org/10.1186/s13071-019-3310-5
  8. Wang R, Li N, Jiang W, Guo Y, Wang X, Jin Y, Feng Y, Xiao L. Infection patterns, clinical significance, and genetic characteristics of Enterocytozoon bieneusi and Giardia duodenalis in dairy cattle in Jiangsu, China. Parasitol Res 2019; 118: 3053-3060. https://doi.org/10.1007/s00436-019-06426-3
  9. Bartley PM, Roehe BK, Thomson S, Shaw HJ, Peto F, Innes EA, Katzer F. Detection of potentially human infectious assemblages of Giardia duodenalis in fecal samples from beef and dairy cattle in Scotland. Parasitology 2019; 146: 1123-1130. https://doi.org/10.1017/S0031182018001117
  10. Lee YJ, Han DG, Ryu JH, Chae JB, Chae JS, Yu DH, Park J, Park BK, Kim HC, Choi KS. Identification of zoonotic Giardia duodenalis in Korean native calves with normal feces. Parasitol Res 2018; 117: 1969-1973. https://doi.org/10.1007/s00436-018-5863-1
  11. Wang X, Cai M, Jiang W, Wang Y, Jin Y, Li N, Guo Y, Feng Y, Xiao L. High genetic diversity of Giardia duodenalis assemblage E in pre-weaned dairy calves in Shanghai, China, revealed by multilocus genotyping. Parasitol Res 2017; 116: 2101-2110. https://doi.org/10.1007/s00436-017-5509-8
  12. Yu F, Li D, Chang Y, Wu Y, Guo Z, Jia L, Xu J, Li J, Qi M, Wang R, Zhang L. Molecular characterization of three intestinal protozoans in hospitalized children with different disease backgrounds in Zhengzhou, central China. Parasit Vectors 2019; 12: 543. https://doi.org/10.1186/s13071-019-3800-5
  13. Wang T, Fan YY, Koehler AV, Ma GX, Li T, Hu M, Gasser RB. First survey of Cryptosporidium, Giardia and Enterocytozoon in diarrhoeic children from Wuhan, China. Infect Genet Evol 2017; 51: 127-131. https://doi.org/10.1016/j.meegid.2017.03.006
  14. Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM. Identification of Giardia lamblia assemblage E in human points to a new anthropozoonotic cycle. J Infect Dis 2016; 214: 1256-1259. https://doi.org/10.1093/infdis/jiw361
  15. Zahedi A, Field D, Ryan U. Molecular typing of Giardia duodenalis in humans in Queensland-first report of assemblage E. Parasitology 2017; 144: 1154-1161. https://doi.org/10.1017/S0031182017000439
  16. Di Piazza F, Di Benedetto MA, Maida CM, Glorioso S, Adamo G, Mazzola T, Firenze A. A study on occupational exposure of Sicilian farmers to Giardia and Cryptosporidium. J Prev Med Hyg 2013; 54: 212-217.
  17. Mahato MK, Singh DK, Rana HB, Acharya KP. Prevalence and risk factors associated with Giardia duodenalis infection in dairy cattle of Chitwan, Nepal. J Parasit Dis 2018; 42: 122-126. https://doi.org/10.1007/s12639-017-0975-6
  18. Wang H, Zhao G, Chen G, Jian F, Zhang S, Feng C, Wang R, Zhu J, Dong H, Hua J, Wang M, Zhang L. Multilocus genotyping of Giardia duodenalis in dairy cattle in Henan, China. PLoS One 2014; 9: e100453. https://doi.org/10.1371/journal.pone.0100453
  19. Li J, Wang H, Wang R, Zhang L. Giardia duodenalis Infections in Humans and other animals in China. Front Microbiol 2017; 8: 2004. https://doi.org/10.3389/fmicb.2017.02004
  20. Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Caccio SM. Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 2005; 35: 207-213. https://doi.org/10.1016/j.ijpara.2004.10.022
  21. Azcona-Gutierrez JM, de Lucio A, Hernandez-de-Mingo M, Garcia-Garcia C, Soria-Blanco LM, Morales L, Aguilera M, Fuentes I, Carmena D. Molecular diversity and frequency of the diarrheagenic enteric protozoan Giardia duodenalis and Cryptosporidium spp. in a hospital setting in northern Spain. PLoS One 2017; 12: e0178575. https://doi.org/10.1371/journal.pone.0178575
  22. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25: 4876-4882. https://doi.org/10.1093/nar/25.24.4876.
  23. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4: 406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
  24. Burland TG. DNASTAR's Lasergene sequence analysis software. Methods Mol Biol 2000; 132: 71-91. https://doi.org/10.1385/1-59259-192-2:71
  25. Zhang XX, Tan QD, Zhao GH, Ma JG, Zheng WB, Ni XT, Zhao Q, Zhou DH, Zhu XQ. Prevalence, risk factors and multilocus genotyping of Giardia intestinalis in dairy cattle, Northwest China. J Eukaryot Microbiol 2016; 63: 498-504. https://doi.org/10.1111/jeu.12293
  26. Mahato MK, Singh DK, Rana HB, Acharya KP. Prevalence and risk factors associated with Giardia duodenalis infection in dairy cattle of Chitwan. Nepal. J Parasit Dis 2018; 42: 122-126. https://doi.org/10.1007/s12639-017-0975-6
  27. Maddox-Hyttel C, Langkjaer RB, Enemark HL, Vigre H. Cryptosporidium and Giardia in different age groups of Danish cattle and pigs-occurrence and management associated risk factors. Vet Parasitol 2006; 141: 48-59. https://doi.org/10.1016/j.vetpar.2006.04.032
  28. 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. Genetic characteristics and geographic segregation of Giardia duodenalis in dairy cattle from Guangdong Province, southern China. Infect Genet Evol 2018; 66: 95-100. https://doi.org/10.1016/j.meegid.2018.09.019
  29. Wang G, Wang G, Li X, Zhang X, Karanis G, Jian Y, Ma L, Karanis P. Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in 1-2-month-old highland yaks in Qinghai Province, China. Parasitol Res 2018; 117: 1793-1800. https://doi.org/10.1007/s00436-018-5861-3
  30. Kiani-Salmi N, Fattahi-Bafghi A, Astani A, Sazmand A, Zahedi A, Firoozi Z, Ebrahimi B, Dehghani-Tafti A, Ryan U, Akrami-Mohajeri F. Molecular typing of Giardia duodenalis in cattle, sheep and goats in an arid area of central Iran. Infect Genet Evol 2019; 75: 104021. https://doi.org/10.1016/j.meegid.2019.104021
  31. Inpankaew T, Jiyipong T, Thadtapong N, Kengradomkij C, Pinyopanuwat N, Chimnoi W, Jittapalapong S. Prevalence and genotype of Giardia duodenalis in dairy cattle from northern and northeastern part of Thailand. Acta Parasitol 2015; 60: 459-461. https://doi.org/10.1515/ap-2015-0063
  32. Malekifard F, Ahmadpour M. Molecular detection and identification of Giardia duodenalis in cattle of Urmia, northwest of Iran. Vet Res Forum 2018; 9: 81-85.
  33. Fan Y, Wang T, Koehler AV, Hu M, Gasser RB. Molecular investigation of Cryptosporidium and Giardia in pre- and post-weaned calves in Hubei Province, China. Parasit Vectors 2017; 10: 519. https://doi.org/10.1186/s13071-017-2463-3
  34. Zhong Z, Dan J, Yan G, Tu R, Tian Y, Cao S, Shen L, Deng J, Yu S, Geng Y, Gu X, Wang Y, Liu H, Peng G. Occurrence and genotyping of Giardia duodenalis and Cryptosporidium in pre-weaned dairy calves in central Sichuan province, China. Parasite 2018; 25: 45. https://doi.org/10.1051/parasite/2018046
  35. Naguib D, El-Gohary AH, Mohamed AA, Roellig DM, Arafat N, Xiao L. Age patterns of Cryptosporidium species and Giardia duodenalis in dairy calves in Egypt. Parasitol Int 2018; 67: 736-741. https://doi.org/10.1016/j.parint.2018.07.012
  36. Lee YJ, Han DG, Ryu JH, Chae JB, Chae JS, Yu DH, Park J, Park BK, Kim HC, Choi KS. Identification of zoonotic Giardia duodenalis in Korean native calves with normal feces. Parasitol Res 2018; 117: 1969-1973. https://doi.org/10.1007/s00436-018-5863-1
  37. Wegayehu T, Karim MR, Erko B, Zhang L, Tilahun G. Multilocus genotyping of Giardia duodenalis isolates from calves in Oromia Special Zone, Central Ethiopia. Infect Genet Evol 2016; 43: 281-288. https://doi.org/10.1016/j.meegid.2016.06.005
  38. Nguyen ST, Fukuda Y, Nguyen DT, Tada C, Nakai Y. Prevalence and first genotyping of Giardia duodenalis in beef calves in Vietnam. Trop Anim Health Prod 2016; 48: 837-841. https://doi.org/10.1007/s11250-016-1013-x
  39. Zhang HJ, Song JK, Wu XM, Li YH, Wang Y, Lin Q, Zhao GH. First report of Giardia duodenalis genotypes in Zangxiang pigs from China. Parasitol Res 2019; 118: 2305-2310. https://doi.org/10.1007/s00436-019-06340-8
  40. Chen D, Zou Y, Li Z, Wang SS, Xie SC, Shi LQ, Zou FC, Yang JF, Zhao GH, Zhu XQ. Occurrence and multilocus genotyping of Giardia duodenalis in black-boned sheep and goats in southwestern China. Parasit Vectors 2019; 12: 102. https://doi.org/10.1186/s13071-019-3367-1
  41. Minetti C, Taweenan W, Hogg R, Featherstone C, Randle N, Latham SM, Wastling JM. Occurrence and diversity of Giardia duodenalis assemblages in livestock in the UK. Transbound Emerg Dis 2014; 61: 60-67. https://doi.org/10.1111/tbed.12075
  42. Xie SC, Zou Y, Chen D, Jiang MM, Yuan XD, Li Z, Zou FC, Yang JF, Sheng JL, Zhu XQ. Occurrence and Multilocus Genotyping of Giardia duodenalis in Yunnan Black Goats in China. Biomed Res Int 2018; 2018: 4601737. https://doi.org/10.1155/2018/4601737
  43. Wang SS, Yuan YJ, Yin YL, Hu RS, Song JK, Zhao GH. Prevalence and multilocus genotyping of Giardia duodenalis in pigs of Shaanxi Province, northwestern China. Parasit Vectors 2017; 10: 490. https://doi.org/10.1186/s13071-017-2418-8
  44. Roegner AF, Daniels ME, Smith WA, Gottdenker N, Schwartz LM, Liu J, Campbell A, Fiorello CV. Giardia infection and Trypanosoma cruzi exposure in dogs in the Bosawas biosphere reserve, Nicaragua. Ecohealth 2019; 16: 512-522. https://doi.org/10.1007/s10393-019-01434-2
  45. Huang J, Zhang Z, Zhang Y, Yang Y, Zhao J, Wang R, Jian F, Ning C, Zhang W, Zhang L. Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in deer in Henan and Jilin, China. Parasit Vectors 2018; 11: 239. https://doi.org/10.1186/s13071-018-2813-9
  46. Caccio SM, Beck R, Lalle M, Marinculic A, Pozio E. Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol 2008; 38: 1523-1531. https://doi.org/10.1016/j.ijpara.2008.04.008

Cited by

  1. Multilocus Genotyping of Giardia duodenalis Occurring in Korean Native Calves vol.8, pp.7, 2020, https://doi.org/10.3390/vetsci8070118