Skip to main content
SpringerLink
Log in

Occurrence of Cryptosporidium and Giardia in wild birds from Qinghai Lake on the Qinghai-Tibetan Plateau, China

  • Protozoology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Cryptosporidium and Giardia are important intestinal zoonotic pathogens that can infect various hosts and cause diarrhoeal diseases. There are few reports of the epidemiological prevalence and molecular characterization of Cryptosporidium and Giardia in wild birds around Qinghai Lake and in the surrounding areas on the Qinghai-Tibetan Plateau, Northwest China. Therefore, the aim of this study was to determine the Cryptosporidium spp. and Giardia duodenalis genotypes and their epidemiological prevalence in wild birds by PCR amplification. To our knowledge, this is the first report of a variety of Cryptosporidium spp. and G. duodenalis infections in wild birds from that area, with overall prevalence rates of 8.98% (61/679) and 3.39% (23/679), respectively. Furthermore, PCR sequencing confirmed the presence of Cryptosporidium baileyi (n = 3), Cryptosporidium parvum (n = 58), and G. duodenalis assemblage B (n = 19) and E (n = 4) in wild birds from the areas around Qinghai Lake. The results of the present study demonstrated the wide distribution of Cryptosporidium and Giardia among wild birds, which has potential public health significance. Moreover, the study findings also provided useful molecular epidemiological data for monitoring and investigating the two parasitic protozoa in wild animals and surrounding environments.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amer S, Wang C, He H (2010) First detection of Cryptosporidium baileyi in Ruddy Shelduck (Tadorna ferruginea) in China. J Vet Med Sci 72:935–938

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Azmanis P, di Somma A, Pappalardo L, Silvanose CD, Bangoura B (2018) First detection of Cryptosporidium parvum in falcons (Falconiformes): diagnosis, molecular sequencing, therapeutic trial and epidemiological assessment of a possible emerging disease in captive falcons. Vet Parasitol 252:167–172

    Article  PubMed  Google Scholar 

  • Batz MB, Hoffmann S, Morris JG Jr (2012) Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot 75:1278–1291

    Article  PubMed  Google Scholar 

  • Bomfim TCB (2013) The importance of poultry in environmental dissemination of Cryptosporidium spp.. Open Vet. Sci J 7: 12–17

  • Braima K, Zahedi A, Oskam C, Reid S, Pingault N, Xiao L, Ryan U (2019) Retrospective analysis of Cryptosporidium species in Western Australian human populations (2015-2018), and emergence of the C. hominis IfA12G1R5 subtype. Infect Genet Evol 73:306–313

    Article  PubMed  Google Scholar 

  • Briceno C, Surot D, Gonzalez-Acuna D, Martinez FJ, Fredes F (2017) Parasitic survey on introduced monk parakeets (Myiopsitta monachus) in Santiago, Chile. Rev Bras Parasitol Vet 26:129–135

    Article  PubMed  Google Scholar 

  • Cano L, de Lucio A, Bailo B, Cardona GA, Muadica AS, Lobo L, Carmena D (2016) Identification and genotyping of Giardia spp. and Cryptosporidium spp. isolates in aquatic birds in the Salburua wetlands, Alava, Northern Spain. Vet Parasitol 221:144–148

    Article  PubMed  Google Scholar 

  • Chelladurai JJ, Clark ME, Kvac M, Holubova N, Khan E, Stenger BL, Giddings CW, McEvoy J (2016) Cryptosporidium galli and novel Cryptosporidium avian genotype VI in North American red-winged blackbirds (Agelaius phoeniceus). Parasitol Res 115:1901–1906

    Article  PubMed  Google Scholar 

  • Cui Z, Song D, Qi M, Zhang S, Wang R, Jian F, Ning C, Zhang L (2018) Revisiting the infectivity and pathogenicity of Cryptosporidium avium provides new information on parasitic sites within the host. Parasit Vectors 11:514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • da Cunha MJR, Cury MC, Santin M (2017) Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds. Parasitol Res 116:487–493

    Article  PubMed  Google Scholar 

  • da Cunha MJR, Cury MC, Santin M (2018) Molecular characterization of Cryptosporidium spp. in poultry from Brazil. Res Vet Sci 118:331–335

    Article  PubMed  CAS  Google Scholar 

  • Dong J, Bo H, Zhang Y, Dong L, Zou S, Huang W, Liu J, Wang D, Shu Y (2017) Characteristics of influenza H13N8 subtype virus firstly isolated from Qinghai Lake region, China. Virol J 14:180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elmore SA, Lalonde LF, Samelius G, Alisauskas RT, Gajadhar AA, Jenkins EJ (2013) Endoparasites in the feces of arctic foxes in a terrestrial ecosystem in Canada. Int J Parasitol Parasites Wildl 2:90–96

    Article  PubMed  PubMed Central  Google Scholar 

  • Erlandsen SL, Bemrick WJ, Wells CL, Feely DE, Knudson L, Campbell SR, van Keulen H, Jarroll EL (1990) Axenic culture and characterization of Giardia ardeae from the great blue heron (Ardea herodias). J Parasitol 76:717–724

    Article  CAS  PubMed  Google Scholar 

  • Ewald MPC, Martins FDC, Caldart ET, Vieira FEG, Yamamura MH, Sasse JP, Barros LD, Freire RL, Navarro IT, Garcia JL (2017) The first study of molecular prevalence and species characterization of Cryptosporidium in free-range chicken (Gallus gallus domesticus) from Brazil. Rev Bras Parasitol Vet 26:472–478

    Article  PubMed  CAS  Google Scholar 

  • Feng Y, Ryan UM, Xiao L (2018) Genetic diversity and population structure of Cryptosporidium. Trends Parasitol 34:997–1011

    Article  CAS  PubMed  Google Scholar 

  • Ferrari ED, Nakamura AA, Nardi ARM, Santana BN, da Silva CV, Nagata WB, Bresciani KDS, Meireles MV (2018) Cryptosporidium spp. in caged exotic psittacines from Brazil: evaluation of diagnostic methods and molecular characterization. Exp Parasitol 184:109–114

    Article  CAS  PubMed  Google Scholar 

  • Forshaw D, Palmer DG, Halse SA, Hopkins RM, Thompson RC (1992) Giardia in straw-necked ibis (Threskiornis spinicollis) in Western Australia. Vet Rec 131:267–268

    Article  CAS  PubMed  Google Scholar 

  • Franssen FF, Hooimeijer J, Blankenstein B, Houwers DJ (2000) Giardiasis in a white stork in The Netherlands. J Wildl Dis 36:764–766

    Article  CAS  PubMed  Google Scholar 

  • Helmy YA, Krucken J, Abdelwhab EM, von Samson-Himmelstjerna G, Hafez HM (2017) Molecular diagnosis and characterization of Cryptosporidium spp. in turkeys and chickens in Germany reveals evidence for previously undetected parasite species. PLoS One 12: e0177150

  • Heyworth MF (2016) Giardia duodenalis genetic assemblages and hosts. Paras 23:13

    Article  Google Scholar 

  • Holubova N, Sak B, Hlaskova L, Kvetonova D, Hanzal V, Rajsky D, Rost M, McEvoy J, Kvac M (2018) Host specificity and age-dependent resistance to Cryptosporidium avium infection in chickens, ducks and pheasants. Exp Parasitol 191:62–65

    Article  PubMed  Google Scholar 

  • Holubova N, Zikmundova V, Limpouchova Z, Sak B, Konecny R, Hlaskova L, Rajsky D, Kopacz Z, McEvoy J, Kvac M (2019) Cryptosporidium proventriculi sp. n. (Apicomplexa: Cryptosporidiidae) in psittaciformes birds. Eur J Protistol 69:70–87

    Article  PubMed  Google Scholar 

  • Hu S, Liu Z, Yan F, Zhang Z, Zhang G, Zhang L, Jian F, Zhang S, Ning C, Wang R (2017) Zoonotic and host-adapted genotypes of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in dairy cattle in Hebei and Tianjin, China. Vet Parasitol 248:68–73

    Article  PubMed  Google Scholar 

  • Ichikawa RS, Santana BN, Ferrari ED, do Nascimento IG, Nakamura AA, Nardi ARM, Meireles MV (2019) Detection and molecular characterization of Giardia spp. in captive psittaciformes in Brazil. Prev Vet Med 164: 10–12

  • Iijima Y, Itoh N, Phrompraphai T, Ito Y, Kimura Y, Kameshima S (2018) Molecular prevalence of Cryptosporidium spp. among companion birds kept in pet shops in Japan. Kor J Parasitol 56:281–285

    Article  Google Scholar 

  • Itagaki T, Kinoshita S, Aoki M, Itoh N, Saeki H, Sato N, Uetsuki J, Izumiyama S, Yagita K, Endo T (2005) Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamate dehydrogenase gene sequencing. Vet Parasitol 133:283–287

    Article  CAS  PubMed  Google Scholar 

  • Jellison KL, Distel DL, Hemond HF, Schauer DB (2004) Phylogenetic analysis of the hypervariable region of the 18S rRNA gene of Cryptosporidium oocysts in feces of Canada geese (Branta canadensis): evidence for five novel genotypes. Appl Environ Microbiol 70:452–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jian Y, Zhang X, Li X, Karanis G, Ma L, Karanis P (2018) Prevalence and molecular characterization of Giardia duodenalis in cattle and sheep from the Qinghai-Tibetan plateau area (QTPA), northwestern China. Vet Parasitol 250:40–44

    Article  PubMed  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 

  • Karanis P, Plutzer J, Halim NA, Igori K, Nagasawa H, Ongerth J, Liqing M (2007) Molecular characterization of Cryptosporidium from animal sources in Qinghai province of China. Parasitol Res 101:1575–1580

    Article  PubMed  Google Scholar 

  • Kassa H, Harrington BJ, Bisesi MS (2004) Cryptosporidiosis: a brief literature review and update regarding Cryptosporidium in feces of Canada geese (Branta canadensis). J Environ Health 66(34–40):45

    Google Scholar 

  • Koompapong K, Mori H, Thammasonthijarern N, Prasertbun R, Pintong AR, Popruk S, Rojekittikhun W, Chaisiri K, Sukthana Y, Mahittikorn A (2014) Molecular identification of Cryptosporidium spp. in seagulls, pigeons, dogs, and cats in Thailand. Paras21: 52

  • Kuhn RC, Rock CM, Oshima KH (2002) Occurrence of Cryptosporidium and Giardia in wild ducks along the Rio Grande River valley in southern New Mexico. Appl Environ Microbiol 68:161–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larki S, Alborzi A, Chegini R, Amiri R (2018) A preliminary survey on gastrointestinal parasites of domestic ducks in Ahvaz, Southwest Iran. Iran J Parasitol 13:137–144

    PubMed  PubMed Central  Google Scholar 

  • Li J, Lin X, Zhang L, Qi N, Liao S, Lv M, Wu C, Sun M (2015) Molecular characterization of Cryptosporidium spp. in domestic pigeons (Columba livia domestica) in Guangdong Province, southern China. Parasitol Res 114:2237–2241

    Article  PubMed  Google Scholar 

  • Li F, Wang H, Zhang Z, Li J, Wang C, Zhao J, Hu S, Wang R, Zhang L, Wang M (2016a) Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in dairy cattle in Beijing, China. Vet Parasitol 219:61–65

    Article  PubMed  CAS  Google Scholar 

  • Li P, Cai J, Cai M, Wu W, Li C, Lei M, Xu H, Feng L, Ma J, Feng Y, Xiao L (2016b) Distribution of Cryptosporidium species in Tibetan sheep and yaks in Qinghai, China. Vet Parasitol 215:58–62

    Article  PubMed  Google Scholar 

  • Liao C, Wang T, Koehler AV, Fan Y, Hu M, Gasser RB (2018) Molecular investigation of Cryptosporidium in farmed chickens in Hubei Province, China, identifies 'zoonotic' subtypes of C. meleagridis. Parasit Vectors 11: 484

  • Ma J, Cai J, Ma J, Feng Y, Xiao L (2014a) Occurrence and molecular characterization of Cryptosporidium spp. in yaks (Bos grunniens) in China. Vet Parasitol 202:113–118

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Sotiriadou I, Cai Q, Karanis G, Wang G, Wang G, Lu Y, Li X, Karanis P (2014b) Detection of Cryptosporidium and Giardia in agricultural and water environments in the Qinghai area of China by IFT and PCR. Parasitol Res 113:3177–3184

    Article  PubMed  Google Scholar 

  • Ma L, Zhang X, Jian Y, Li X, Wang G, Hu Y, Karanis P (2019) Detection of Cryptosporidium and Giardia in the slaughterhouse, sewage and river waters of the Qinghai Tibetan plateau area (QTPA), China. Parasitol Res 118:2041–2051

    Article  PubMed  Google Scholar 

  • Majewska AC, Graczyk TK, Slodkowicz-Kowalska A, Tamang L, Jedrzejewski S, Zduniak P, Solarczyk P, Nowosad A, Nowosad P (2009) The role of free-ranging, captive, and domestic birds of Western Poland in environmental contamination with Cryptosporidium parvum oocysts and Giardia lamblia cysts. Parasitol Res 104:1093–1099

    Article  PubMed  Google Scholar 

  • McEvoy JM, Giddings CW (2009) Cryptosporidium in commercially produced turkeys on-farm and post slaughter. Lett Appl Microbiol 48:302–306

    Article  CAS  PubMed  Google Scholar 

  • McRoberts KM, Meloni BP, Morgan UM, Marano R, Binz N, Eriandsen SL, Halse SA, Thompson RC (1996) Morphological and molecular characterization of Giardia isolated from the straw-necked ibis (Threskiornis spinicollis) in Western Australia. J Parasitol 82:711–718

    Article  CAS  PubMed  Google Scholar 

  • Medema G (1999) Cryptosporidium and Giardia: new challenges to the water industry. University of Utrecht, Dissertation

    Google Scholar 

  • Mi R, Wang X, Li C, Huang Y, Zhou P, Li Z, Lei M, Cai J, Chen Z (2013) Prevalence and genetic characterization of Cryptosporidium in yaks in Qinghai Province of China. PLoS One 8:e74985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura AA, Meireles MV (2015) Cryptosporidium infections in birds--a review. Rev Bras Parasitol Vet 24:253–267

    Article  CAS  PubMed  Google Scholar 

  • Nakamura AA, Simoes DC, Antunes RG, da Silva DC, Meireles MV (2009) Molecular characterization of Cryptosporidium spp. from fecal samples of birds kept in captivity in Brazil. Vet Parasitol 166:47–51

    Article  CAS  PubMed  Google Scholar 

  • Ng J, Pavlasek I, Ryan U (2006) Identification of novel Cryptosporidium genotypes from avian hosts. Appl Environ Microbiol 72:7548–7553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oates SC, Miller MA, Hardin D, Conrad PA, Melli A, Jessup DA, Dominik C, Roug A, Tinker MT, Miller WA (2012) Prevalence, environmental loading, and molecular characterization of Cryptosporidium and Giardia isolates from domestic and wild animals along the Central California coast. Appl Environ Microbiol 78:8762–8772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira BCM, Ferrari ED, da Cruz Panegossi MF, Nakamura AA, Corbucci FS, Nagata WB, Dos Santos BM, Gomes JF, Meireles MV, Widmer G, Bresciani KDS (2017a) First description of Cryptosporidium parvum in carrier pigeons (Columba livia). Vet Parasitol 243:148–150

    Article  PubMed  Google Scholar 

  • Oliveira BCM, Nagata WB, Arana DG, Ferreira GC, Sitton HA, de Oliveira MRF, Meireles MV (2017b) Cryptosporidium baileyi in wild captive psittacines in Brazil. Vet Parasitol Reg Stud Reports 10:154–156

    PubMed  Google Scholar 

  • Pavlasek I (1993) The black-headed gull (Larus ridibundus L.), a new host for Cryptosporidium baileyi (Apicomplexa: Cryptosporidiidae). Vet Med (Praha) 38:629–638

    CAS  Google Scholar 

  • 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 

  • Plutzer J, Karanis P (2009) Genetic polymorphism in Cryptosporidium species: an update. Vet Parasitol 165:187–199

    Article  CAS  PubMed  Google Scholar 

  • Plutzer J, Tomor B (2009) The role of aquatic birds in the environmental dissemination of human pathogenic Giardia duodenalis cysts and Cryptosporidium oocysts in Hungary. Parasitol Int 58:227–231

    Article  PubMed  Google Scholar 

  • Plutzer J, Torokne A, Karanis P (2010) Combination of ARAD microfibre filtration and LAMP methodology for simple, rapid and cost-effective detection of human pathogenic Giardia duodenalis and Cryptosporidium spp. in drinking water. Lett Appl Microbiol 50:82–88

    Article  CAS  PubMed  Google Scholar 

  • Qi M, Zhou H, Wang H, Wang R, Xiao L, Arrowood MJ, Li J, Zhang L (2015) Molecular identification of Cryptosporidium spp. and Giardia duodenalis in grazing horses from Xinjiang, China. Vet Parasitol 209:169–172

    Article  CAS  PubMed  Google Scholar 

  • Qi M, Zhang Z, Zhao A, Jing B, Guan G, Luo J, Zhang L (2019) Distribution and molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi amongst grazing adult sheep in Xinjiang, China. Parasitol Int 71:80–86

    Article  PubMed  Google Scholar 

  • Rao JR, Cherie Millar B, Moore JE (2009) Avian influenza, migratory birds and emerging zoonoses: unusual viral RNA, enteropathogens and Cryptosporidium in poultry litter. Biosci Hypotheses 2:363–369

    Article  PubMed  PubMed Central  Google Scholar 

  • Reboredo-Fernandez A, Ares-Mazas E, Caccio SM, Gomez-Couso H (2015) Occurrence of Giardia and Cryptosporidium in wild birds in Galicia (Northwest Spain). Parasitol 142:917–925

    Article  CAS  Google Scholar 

  • Ren M, Wu F, Wang D, Li LY, Chang JJ, Lin Q (2019) Molecular typing of Cryptosporidium species identified in fecal samples of yaks (Bos grunniens) of Qinghai Province, China. J Parasitol 105:195–198

    Article  CAS  PubMed  Google Scholar 

  • Richter D, Wiegand-Tripp G, Burkhardt E, Kaleta EF (1994) Natural infections by Cryptosporidium sp. in farm-raised ducks and geese. Avian Pathol 23:277–286

    Article  CAS  PubMed  Google Scholar 

  • Ryan U (2010) Cryptosporidium in birds, fish and amphibians. Exp Parasitol 124:113–120

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ryan U, Xiao L, Read C, Zhou L, Lal AA, Pavlasek I (2003) Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl Environ Microbiol 69:4302–4307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan U, Fayer R, Xiao L (2014) Cryptosporidium species in humans and animals: current understanding and research needs. Parasitol 141:1667–1685

    Article  Google Scholar 

  • Rzymski P, Slodkowicz-Kowalska A, Klimaszyk P, Solarczyk P, Poniedzialek B (2017) Screening of protozoan and microsporidian parasites in feces of great cormorant (Phalacrocorax carbo). Environ Sci Pollut Res Int 24:9813–9819

    Article  PubMed  PubMed Central  Google Scholar 

  • Santana BN, Kurahara B, Nakamura AA, da Silva CV, Ferrari ED, da Silva GS, Nagata WB, Meireles MV (2018) Detection and characterization of Cryptosporidium species and genotypes in three chicken production systems in Brazil using different molecular diagnosis protocols. Prev Vet Med 151:73–78

    Article  PubMed  Google Scholar 

  • Shemshadi B, Ranjbar-bahadori S, Faghihzadeh-gorji S (2014) Occurrence of parasitic protozoa in wild waterfowl in southern coastal Caspian Sea lagoons. Iran J Vet Med 8:261–267

    Google Scholar 

  • Shemshadi B, Ranjbar-bahadori S, Delfan-abazari M (2016) Prevalence and intensity of parasitic infection in domestic ducks (Anas platyrhynchas) in Gilan Province, Northern Iran. Compar Clin Pathol 26:165–167

    Article  Google Scholar 

  • Smith HV, Brown J, Coulson JC, Morris GP, Girdwood RW (1993) Occurrence of oocysts of Cryptosporidium spp. in Larus spp. gulls. Epidemiol Infect 110:135–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squire SA, Yang R, Robertson I, Ayi I, Ryan U (2017) Molecular characterization of Cryptosporidium and Giardia in farmers and their ruminant livestock from the coastal Savannah zone of Ghana. Infect Genet Evol 55:236–243

    Article  CAS  PubMed  Google Scholar 

  • Una MM, Paul TM, Lihua X, Josef L, Irshad S, Shane R, Peter OD, Robin G, Allan M, Ronald F, Byron LB, Altaf AL (2001) Molecular and phylogenetic characterisation of Cryptosporidium from birds. Int J Parasit 31:289–296

    Article  Google Scholar 

  • Wang R, Jian F, Sun Y, Hu Q, Zhu J, Wang F, Ning C, Zhang L, Xiao L (2010) Large-scale survey of Cryptosporidium spp. in chickens and Pekin ducks (Anas platyrhynchos) in Henan, China: prevalence and molecular characterization. Avian Pathol 39:447–451

    Article  PubMed  CAS  Google Scholar 

  • Wang R, Wang F, Zhao J, Qi M, Ning C, Zhang L, Xiao L (2012) Cryptosporidium spp. in quails (Coturnix coturnix japonica) in Henan, China: molecular characterization and public health significance. Vet Parasitol 187:534–537

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Wang GP, Li XP, Ma LQ, Karanis G, Christodoulou-Vafeiadou E, Karanis P (2017) Detection of Giardia duodenalis assemblage E infections at the Tibetan Plateau Area: yaks are suitable hosts. Acta Trop 169:157–162

    Article  PubMed  Google Scholar 

  • Wang G, Wang G, Li X, Zhang X, Karanis G, Jian Y, Ma L, Karanis P (2018a) Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in 1-2-month-old highland yaks in Qinghai Province, China. Parasitol Res 117:1793–1800

    Article  PubMed  Google Scholar 

  • Wang H, Zhang Y, Wu Y, Li J, Qi M, Li T, Wang J, Wang R, Zhang S, Jian F, Ning C, Zhang L (2018b) Occurrence, molecular characterization, and assessment of zoonotic risk of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in pigs in Henan, Central China. J Eukaryot Microbiol 65:893–901

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Gazizova A, Wang Y, Zhang K, Zhang Y, Chang Y, Cui Y, Zhang Y, Zhang S, Zhang L (2019) First detection of Cryptosporidium spp. in migratory whooper swans (Cygnus cygnus) in China. Microorg 8: 6

  • Xiang L, Guo F, Yu Y, Parson LS, LaCoste L, Gibson A, Presley SM, Peterson M, Craig TM, Rollins D, Fedynich AM, Zhu G (2017) Multiyear survey of coccidia, Cryptosporidia, Microsporidia, Histomona, and Hematozoa in wild quail in the rolling plains ecoregion of Texas and Oklahoma, USA. J Eukar Microbiol 64:4–17

    Article  Google Scholar 

  • Xiao L, Sulaiman IM, Ryan UM, Zhou L, Atwill ER, Tischler ML, Zhang X, Fayer R, Lal AA (2002) Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. Int J Parasitol 32:1773–1785

    Article  PubMed  Google Scholar 

  • Yao QX, Zhang XX, Chen K, Ma JG, Zheng WB, Xu XQ, Zhu XQ (2017) Prevalence and genetic characterization of Cryptosporidium infection in Java sparrows (Lonchura oryzivora) in Northern China. Biomed Res Int 2017:2318476

    PubMed  PubMed Central  Google Scholar 

  • Zhang XX, Zhang NZ, Zhao GH, Zhao Q, Zhu XQ (2015) Prevalence and genotyping of Cryptosporidium infection in pet parrots in North China. Biomed Res Int 2015:549798

    PubMed  PubMed Central  Google Scholar 

  • Zhang X, Jian Y, Li X, Ma L, Karanis G, Karanis P (2018a) The first report of Cryptosporidium spp. in Microtus fuscus (Qinghai vole) and Ochotona curzoniae (wild plateau pika) in the Qinghai-Tibetan Plateau area, China. Parasitol Res 117:1401–1407

    Article  PubMed  Google Scholar 

  • Zhang X, Jian Y, Li X, Ma L, Karanis G, Qigang C, Karanis P (2018b) Molecular detection and prevalence of Cryptosporidium spp. infections in two types of domestic farm animals in the Qinghai-Tibetan Plateau Area (QTPA) in China. Parasitol Res 117:233–239

    Article  PubMed  Google Scholar 

  • Zhang HJ, Song JK, Wu XM, Li YH, Wang Y, Lin Q, Zhao GH (2019) First report of Giardia duodenalis genotypes in Zangxiang pigs from China. Parasitol Res 118:2305–2310

    Article  CAS  PubMed  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 (2018) Occurrence and genetic characterization of Giardia duodenalis and Cryptosporidium spp. from adult goats in Sichuan Province, China. PLoS One 13:e0199325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou L, Kassa H, Tischler ML, Xiao L (2004) Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Appl Environ Microbiol 70:4211–4215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziegler PE, Wade SE, Schaaf SL, Stern DA, Nadareski CA, Mohammed HO (2007) Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York state. Vet Parasitol 147:176–184

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to the staff Yubang He, Yonglin Wu, and Yuansheng Hou working in Qinghai Lake National Nature Reserve Administration for their assistance with collecting the samples.

Funding

The research was supported by the National Natural Science Foundation of China (no. 32060804), the Young and Middle-Aged Research Funding Project from Qinghai University (2017-QNY-1) and the One Thousand Talents Plan (P. Karanis) of the Chinese Government (no. WQ2013630172).

Author information

Author notes

  1. Yingna Jian and Xueyong Zhang contributed equally to this work.

Authors and Affiliations

  1. Qinghai Academy of Animal Sciences and Veterinary Medicine, Qinghai University, State Key Laboratory of Plateau Ecology and Agriculture Qinghai University, Center for Biomedicine and Infectious Diseases, Xining, 810016, People’s Republic of China

    Yingna Jian, Xueyong Zhang, Xiuping Li, Liqing Ma & Panagiotis Karanis

  2. Medical Faculty and University Hospital Cologne, University of Cologne, Cologne, Germany

    Chad Schou & Panagiotis Karanis

  3. Department of Life and Health Sciences, School of Sciences and Engineering, University of Nicosia, 2417, Nicosia, Cyprus

    Iris Charalambidou

  4. Department of Basic and Clinical Sciences, Anatomy Centre, University of Nicosia Medical School, Nicosia, Cyprus

    Panagiotis Karanis

Authors
  1. Yingna Jian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xueyong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiuping Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chad Schou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Iris Charalambidou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Liqing Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Panagiotis Karanis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Panagiotis Karanis.

Additional information

Handling Editor: Julia Walochnik

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

Jian, Y., Zhang, X., Li, X. et al. Occurrence of Cryptosporidium and Giardia in wild birds from Qinghai Lake on the Qinghai-Tibetan Plateau, China. Parasitol Res 120, 615–628 (2021). https://doi.org/10.1007/s00436-020-06993-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06993-w

Keywords

Search

Navigation