Skip to main content

Advertisement

SpringerLink
Log in

First report of Giardia duodenalis genotypes in Zangxiang pigs from China

  • Protozoology - Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Giardia duodenalis is an important zoonotic intestinal protozoan of animals and humans. We collected 450 faecal specimens from four age groups (pre-weaned piglets, weaned piglets, juveniles, adults) of Zangxiang pigs from Shaanxi and Qinghai provinces, to investigate the prevalence and genetic diversity of G. duodenalis at the β-giardin (bg), triosephosphate isomerase (tpi) and glutamate dehydrogenase (gdh) loci using nested PCRs in the present study. A total of 28 faecal samples were positive for presence of G. duodenalis, with an overall prevalence of 6.2%. Giardia duodenalis was detected in pigs from all age groups and in both investigated provinces. Significant differences (P < 0.0001) in prevalence were observed among the four age groups with prevalence decreasing with age. Sequence analysis indicated existence of genetic diversity of G. duodenalis isolates from Zangxiang pigs, with 4, 2 and 4 haplotypes at the bg, tpi and gdh loci, respectively. Two assemblages were identified, including the zoonotic assemblage B and assemblage E, with the latter as the predominant assemblage found in both locations and all age groups except adults. The present study expanded the host range of G. duodenalis and provided fundamental data for controlling G. duodenalis infection in Zangxiang pigs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Abdel-Moein KA, Saeed H (2016) The zoonotic potential of Giardia intestinalis assemblage E in rural settings. Parasitol Res 115:3197–3202

    Article  PubMed  Google Scholar 

  • Akinkuotu OA, Takeet MI, Otesile EB, Olufemi F, Greenwood SJ, McClure JT (2019) Prevalence and mulilocus genotypes of Giardia duodenalis infecting pigs in Ogun state, Nigeria. Infect Genet Evol 70:53–60

    Article  PubMed  Google Scholar 

  • Armson A, Yang R, Thompson J, Johnson J, Reid S, Ryan UM (2009) Giardia genotypes in pigs in western Australia: prevalence and association with diarrhea. Exp Parasitol 121:381–383

    Article  PubMed  Google Scholar 

  • Asher AJ, Holt DC, Andrews RM, Power ML (2014) Distribution of Giardia duodenalis assemblages A and B among children living in a remote indigenous community of the northern territory, Australia. PLoS One 9:e112058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azcona-Gutiérrez JM, de Lucio A, Hernández-de-Mingo M, García-García C, Soria-Blanco LM, Morales L, Aguilera M, Fuentes I, Carmena D (2017) Molecular diversity and frequency of the diarrheagenic enteric protozoan Giardia duodenalis and Cryptosporidium spp. in a hospital setting in northern Spain. PLoS One 12:e0178575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bian B (2013) Epidemic status and control strategies of cysticercosis in Zangxiang pigs. J Contemp Anim Husb 10:10–13 in Chinese

    Google Scholar 

  • Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91

    CAS  PubMed  Google Scholar 

  • Cacciò SM, De Giacomo M, Pozio E (2002) Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. Int J Parasitol 32:1023–1030

    Article  PubMed  Google Scholar 

  • Cacciò SM, Lalle M, Svärd SG (2018) Host specificity in the Giardia duodenalis species complex. Infect Genet Evol 66:335–345

    Article  PubMed  Google Scholar 

  • Castro-Hermida JA, García-Presedo I, Almeida A, González-Warleta M, Correia Da Costa JM, Mezo M (2011) Cryptosporidium spp. and Giardia duodenalis in two areas of Galicia (NW Spain). Sci Total Environ 409:2451–2459

    Article  CAS  PubMed  Google Scholar 

  • Elmberg J, Berg C, Lerner H, Waldenström J, Hessel R (2017) Potential disease transmission from wild geese and swans to livestock, poultry and humans: a review of the scientific literature from a one health perspective. Infect Ecol Epidemiol 7:1300450

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Faria CP, Zanini GM, Dias GS, da Silva S, Sousa MDC (2017) New multilocus genotypes of Giardia lamblia human isolates. Infect Genet Evol 54:128–137

    Article  CAS  PubMed  Google Scholar 

  • Farzan A, Parrington L, Coklin T, Cook A, Pintar K, Pollari F, Friendship R, Farber J, Dixon B (2011) Detection and characterization of Giardia duodenalis and Cryptosporidium spp. on swine farms in Ontario, Canada. Foodborne Pathog Dis 8:1207–1213

    Article  PubMed  Google Scholar 

  • Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, Faria ES, Cunha MJ, Couto TR, Cury MC (2013) Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int 2013:875048

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Xiao 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, Gong X, Zhu K, Li N, Yu Z, Guo Y, Weng Y, Kváč M, Feng Y, Xiao L (2019) Prevalence and genotypic identification of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in pre-weaned dairy calves in Guangdong, China. Parasit Vectors 12:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Foronda P, Bargues MD, Abreu-Acosta N, Periago MV, Valero MA, Valladares B, Mas-Coma S (2008) Identification of genotypes of Giardia intestinalis of human isolates in Egypt. Parasitol Res 103:1177–1181

    Article  CAS  PubMed  Google Scholar 

  • Helmy YA, Klotz C, Wilking H, Krücken J, Nöckler K, Von Samson-Himmelstjerna G, Zessin KH, Aebischer T (2014) Epidemiology of Giardia duodenalis infection in ruminant livestock and children in the Ismailia province of Egypt: insights by genetic characterization. Parasit Vectors 7:321

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunter PR, Thompson RC (2005) The zoonotic transmission of Giardia and Cryptosporidium. Int J Parasitol 35:1181–1190

    Article  PubMed  Google Scholar 

  • Jiang LL, Si KZ, Xu JE, Yu B, Zhou SX, Xiao FP (2014) Diagnosis and treatment of porcine pseudorabies, porcine cirovirus disease mixed infections with porcine eperythrozoonosis in a Zangxiang pig. Chin Anim Husb Vet Med 41:225–229 in Chinese

    CAS  Google Scholar 

  • Jin Y, Fei J, Cai J, Wang X, Li N, Guo Y, Feng Y, Xiao L (2017) Multilocus genotyping of Giardia duodenalis in Tibetan sheep and yaks in Qinghai, China. Vet Parasitol 247:70–76

    Article  CAS  PubMed  Google Scholar 

  • Johargy A, Ghazi H, Mumenah A (2010) Frequency of viral, bacterial and parasitic enteropathogens among young children with acute diarrhoea in Saudi Arabia. J Pak Med Assoc 60(6):456–459

    PubMed  Google Scholar 

  • Li CX (2018) Biological characteristics and feeding management of Zangxiang pigs. Chin Abstr Anim Husb Vet Med 34:88 in Chinese

    CAS  Google Scholar 

  • Li W, Deng L, Wu K, Huang X, Song Y, Su H, Hu Y, Fu H, Zhong Z, Peng G (2017) Presence of zoonotic Cryptosporidium scrofarum, Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotypes in captive Eurasian wild boars (Sus scrofa) in China: potential for zoonotic transmission. Parasit Vectors 10:10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Wang Y, Zhang HJ, Wu HX, Zhao GH (2018) First report of Giardia duodenalis infection in bamboo rats. Parasit Vectors 11:520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minetti C, Taweenan W, Hogg R, Featherstone C, Randle N, Latham SM, Wastling JM (2014) Occurrence and diversity of Giardia duodenalis assemblages in livestock in the UK. Transbound Emerg Dis 61:e60–e67

    Article  CAS  PubMed  Google Scholar 

  • Naguib D, El-Gohary AH, Mohamed AA, Roellig DM, Arafat N, Xiao L (2018) Age patterns of Cryptosporidium species and Giardia duodenalis in dairy calves in Egypt. Parasitol Int 67:736–741

    Article  PubMed  Google Scholar 

  • Omarova A, Tussupova K, Berndtsson R, Kalishev M, Sharapatova K (2018) Protozoan parasites in drinking water: a system approach for improved water, sanitation and hygiene in developing countries. Int J Environ Res Public Health 15:E495

  • Petersen HH, Jianmin W, Katakam KK, Mejer H, Thamsborg SM, Dalsgaard A, Olsen A, Enemark HL (2015) Cryptosporidium and Giardia in Danish organic pig farms: seasonal and age-related variation in prevalence, infection intensity and species/genotypes. Vet Parasitol 214:29–39

    Article  PubMed  Google Scholar 

  • Ramírez JD, Heredia RD, Hernández C, León CM, Moncada LI, Reyes P, Pinilla AE, Lopez MC (2015) Molecular diagnosis and genotype analysis of Giardia duodenalis in asymptomatic children from a rural area in central Colombia. Infect Genet Evol 32:208–213

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Rivera LD, Cummings KJ, McNeely I, Suchodolski JS, Scorza AV, Lappin MR, Mesenbrink BT, Leland BR, Bodenchuk MJ (2016) Prevalence and diversity of Cryptosporidium and Giardia identified among feral pigs in Texas. Vector Borne Zoonotic Dis 16:765–768

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schär F, Inpankaew T, Traub RJ, Khieu V, Dalsgaard A, Chimnoi W, Chhoun C, Sok D, Marti H, Muth S, Odermatt P (2014) The prevalence and diversity of intestinal parasitic infections in humans and domestic animals in a rural Cambodian village. Parasitol Int 63:597–603

    Article  PubMed  Google Scholar 

  • Siwila J, Mwape KE (2012) Prevalence of Cryptosporidium spp. and Giardia duodenalis in pigs in Lusaka, Zambia. Onderstepoort J Vet Res 79:E1–E5

    Article  PubMed  Google Scholar 

  • Song SG, An XP, Zhao HB, Liu HY, Cao BY (2011) Analysis of slaughter traits and meat quality in Zangxiang pigs. Acta Agri Boreali-Occidentalis Sinica 20:26–32 in Chinese

    Google Scholar 

  • Song GY, Qin SY, Zhao GH, Zhu XQ, Zhou DH, Song MX (2016) Molecular characterization of Giardia duodenalis from white yaks in China. Acta Parasitol 61:397–400

    CAS  PubMed  Google Scholar 

  • Tang W (2012) Diagnosis and treatment of mixed infection of Actinobacillus pleuropneumoniae with Trichuris spp. in Zangxiang pigs. J Modern Anim Husb Vet Med 7:43–44 in Chinese

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres-Romero JC, Euan-Canto AJ, Benito-González N, Padilla-Montaño N, Huchin-Chan C, Lara-Riegos J, Cedillo-Rivera R (2014) Intestinal parasites and genotyping of Giardia duodenalis in children: first report of genotype B in isolates from human clinical samples in Mexico. Mem Inst Oswaldo Cruz 109:388–390

    Article  PubMed  PubMed Central  Google Scholar 

  • Vasco K, Graham JP, Trueba G (2016) Detection of zoonotic enteropathogens in children and domestic animals in a semirural community in Ecuador. Appl Environ Microbiol 82:4218–4224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SS, Yuan YJ, Yin YL, Hu RS, Song JK, Zhao GH (2017) Prevalence and multilocus genotyping of Giardia duodenalis in pigs of Shaanxi Province, northwestern China. Parasit Vectors 10:490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XP, Zhang YF (2015) Breeding technology and status of Zangxiang pigs. Xinjiang Husb Sci Technol 5:33–34 in Chinese

    Google Scholar 

  • Yang WP, Meng FX, Ma L, Ji SY, Cao BY (2014) Isolation, identification and enzymatic characteristics analysis of cellulolytic bacterium from Zangxiang pigs. Chin J Anim Nutrit 26:620–629 in Chinese

    CAS  Google Scholar 

  • Yin YL, Zhang HJ, Yuan YJ, Tang H, Chen D, Jing S, Wu HX, Wang SS, Zhao GH (2018) Prevalence and multi-locus genotyping of Giardia duodenalis from goats in Shaanxi province, northwestern China. Acta Trop 182:202–206

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Qi M, Jing B, Yu F, Wu Y, Chang Y, Zhao A, Wei Z, Dong H, Zhang L (2018) Molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in rabbits in Xinjiang, China. J Eukaryot Microbiol 65:854–859

    Article  CAS  PubMed  Google Scholar 

  • 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 (2018a) Occurrence and genotyping of Giardia duodenalis and Cryptosporidium in pre-weaned dairy calves in central Sichuan province, China. Parasite 25:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhong Z, Tu R, Ou H, Yan G, Dan J, Xiao Q, Wang Y, Cao S, Shen L, Deng J, Zuo Z, Ma X, Zhou Z, Liu H, Yu S, Ren Z, Hu Y, Peng G (2018b) Occurrence and genetic characterization of Giardia duodenalis and Cryptosporidium spp. from adult goats in Sichuan Province, China. PLoS One 13:e0199325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Prof. Una Ryan from Murdoch University of Australia and Prof. Xian-Ming Chen from Creighton University of USA for assistance in improvement of the language of this study.

Author information

Author notes

  1. H. J. Zhang, J. K. Song and X. M. Wu contributed equally to this work.

Authors and Affiliations

  1. College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People’s Republic of China

    H. J. Zhang, J. K. Song, X. M. Wu, Y. H. Li, Y. Wang, Q. Lin & G. H. Zhao

Authors
  1. H. J. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. K. Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. X. M. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Y. H. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Y. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Q. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. H. Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Q. Lin or G. H. Zhao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study including the collection of faecal samples were permitted by the farm owners. The protocols in this study were approved by the Guidance of Laboratory Animal Care and Use of Chinese Ministry of Health, China, and the Research Ethics Committee of Northwest A&F University.

Additional information

Section Editor: Lihua Xiao

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H.J., Song, J.K., Wu, X.M. et al. First report of Giardia duodenalis genotypes in Zangxiang pigs from China. Parasitol Res 118, 2305–2310 (2019). https://doi.org/10.1007/s00436-019-06340-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06340-8

Keywords

Search

Navigation