Skip to main content
Download PDF
  • Research article
  • Open access
  • Published:

Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalisin dairy cattle in Ningxia, northwestern China

BMC Veterinary Research volume 10, Article number: 292 (2014) Cite this article

Abstract

Background

Cryptosporidium spp. and Giardia duodenalis are important gastrointestinal protists in humans and animals worldwide. In China, bovine cryptosporidiosis and giardiasis are of increasing concern because cattle are important reservoirs of these parasites, which have become potential threats to public health and to large numbers of cattle in recent years.

Results

A total of 1366 fecal samples from the Ningxia Autonomous Region were examined. The overall infection rates for Cryptosporidium spp. and G. duodenalis were 1.61% and 2.12%, respectively. Cryptosporidium was only detected in preweaned calves and adults older than 2 years, whereas G. duodenalis was only detected in calves aged less than 11 months. Cryptosporidium spp. were characterized with a PCR–restriction fragment length polymorphism analysis and DNA sequence analysis of the small subunit rRNA gene. Three Cryptosporidium species were identified: C. parvum (n = 15) and C. bovis (n = 4) in preweaned calves, and C. andersoni (n = 4) in adults aged over 2 years. A DNA sequence analysis of the gp60 gene suggested that the 15 C. parvum isolates all belonged to subtype IIdA15G1. Twenty-nine G. duodenalis isolates were analyzed by DNA sequencing of the triosephosphate isomerase (tpi) and glutamate dehydrogenase (gdh) genes. Two G. duodenalis assemblages were identified, assemblages E (n = 15) and B (n = 4, one subtype B1 and three subtype B2) in preweaned calves, and assemblage E (n = 10) in 3–11-month-old calves.

Conclusions

The predominance of C. parvum detected in preweaned calves and the first identified subtype IIdA15G1 in dairy cattle, and the dominant G. duodenalis assemblage E in this study differed considerably from those found in Henan, Heilongjiang, and Shannxi Provinces. Our findings further confirm the dominance of C. parvum IId subtypes in China.

Background

Cryptosporidium and Giardia are important gastrointestinal protists with a wide spectrum of hosts, including humans, livestock, companion animals, and wildlife. Infection is acquired via the fecal–oral route following the ingestion of infective oocysts or cysts, by either direct contact or the ingestion of contaminated food or water [1],[2]. Diarrhea is the typical clinical symptom of human and animal cryptosporidiosis or giardiasis, as well as dehydration, fever, nausea, and anorexia.

Cattle are mammalian species commonly infected with Cryptosporidium, and preweaned calves are considered the most important reservoir for zoonotic infections. Large numbers of studies have suggested that C. parvum, C. bovis, C. andersoni, and C. ryanae are the most common species infecting cattle, although C. felis, C. hominis, C. suis, C. scrofarum (formerly pig genotype II), and C. suis-like genotype have also been detected [3]. The four common Cryptosporidium species have age-associated distributions. Cryptosporidium parvum is usually found in preweaned calves and is a significant cause of diarrhea. However, C. bovis and C. ryanae usually infect postweaned calves and yearlings, and C. bovis is detected more frequently than C. ryanae, although neither is associated with diarrhea [4]. In contrast, C. andersoni is commonly seen in adult cattle and is associated with gastritis, reduced milk yield, and poor weight gain [5].

Among the six known Giardia species, only G. duodenalis is recovered from humans and most other mammals [6]. Its molecular characterization has shown that G. duodenalis is a species complex comprising eight distinct ‘assemblages’ or genotypes: A to H [2]. Most of the assemblages (C to H) seem to be host specific for nonhuman species: assemblages C and D are specific for dogs, E for hoofed livestock, F for cats, G for rats, and H for seals. In cattle, the prevalence of giardiasis ranges from 2.2% to 50.7% worldwide, and assemblages A, B, and E have been detected, with assemblage E the predominant genotype in most countries [1],[2].

In China, bovine cryptosporidiosis and giardiasis are of increasing concern because cattle are important reservoirs of these parasites, which have become potential threats to public health and to large numbers of cattle in recent years. Several studies of Cryptosporidium and Giardia infections in several areas have been published in the English language [7]-[11], and differences in Cryptosporidium distributions have been noted in different locations. For example, C. bovis rather than C. parvum is the predominant species in preweaned calves in Henan, whereas C. andersoni is the most common species of cattle in Heilongjiang and Shannxi Provinces [7],[12]. Thus, the distributions of Cryptosporidium spp. and the C. parvum subtype (all belonging to IIdA19G1) in dairy cattle differ considerably from those in other countries [9],[10]. In contrast, there have been few molecular epidemiological studies of G. duodenalis in cattle [10],[13]. The objective of this study was to identify the species of Cryptosporidium and Giardia present in dairy cattle in the Ningxia Autonomous Region, northwest China.

Methods

Ethics statement

This study was conducted in accordance with the Chinese Laboratory Animal Administration Act of 1988. The research protocol was reviewed and approved by the Research Ethics Committee of the Henan Agricultural University. Permission was obtained from farm owners before collection of fecal samples.

Sample collection and examination

A fresh fecal sample was collected from each animal using a sterile disposal latex glove immediately after its defecation onto the ground, and was then placed individually into a disposable plastic bag. In total, 1366 fecal samples were collected between December 2011 and October 2012 from dairy cattle on 20 scale farms in the Ningxia Autonomous Region, northwestern China (Table 1). The Cryptosporidium oocysts in the fecal materials were concentrated with Sheather’s sugar flotation technique, with a further formalin–ethyl acetate sedimentation step included for the preweaned calf samples [9]. Giardia cysts were detected with Lugol’s iodine staining. Cryptosporidium- or Giardia-positive samples were stored in 2.5% potassium dichromate at 4°C before DNA extraction.

Table 1 Numbers of fecal samples examined with microscopy for Cryptosporidium oocysts and Giardia cysts on Chinese farms
Full size table

DNA extraction

The Cryptosporidium or Giardia-positive fecal specimens were washed three times with distilled water, and the genomic DNA was extracted from the fecal pellets with the E.Z.N.A.® Stool DNA Kit (Omega Biotek Inc., Norcross, GA, USA), according to the manufacturer’s recommendations.

Cryptosporidium/Giardiagenotyping and subtyping

The Cryptosporidium species were identified with PCR–restriction fragment length polymorphism (RFLP) analysis and DNA sequence analysis of the small subunit (SSU) rRNA gene [14]. Cryptosporidium parvum was subtyped with nested PCR targeting the gp60 gene, and the previously established nomenclature system was used to name the C. parvum subtype families and subtypes [15],[16]. The Giardia duodenalis genotypes/subtypes were identified by sequencing the triosephosphate isomerase (tpi) and glutamate dehydrogenase (gdh) genes [17], and the genotype/subtype identities of the G. duodenalis samples were established by direct comparison of these sequences with reference sequences downloaded from the GenBank database.

DNA sequence analysis

PCR products were sequenced on an ABI Prism™ 3730 XL DNA Analyzer using the BigDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems, Foster, CA, USA). Sequence accuracy was confirmed with bi-directional sequencing and by sequencing a new PCR product if necessary. The sequences were aligned with the ClustalX 1.83 program. Representative nucleotide sequences have been deposited in GenBank under accession numbers KM067089–KM067096.

Statistical analysis

The χ2 test was used to compare the Cryptosporidium infection rates. Differences were considered significant at P <0.05.

Results

Prevalence of Cryptosporidium and Giardia

Microscopic analysis of 1366 fecal samples showed the presence of Cryptosporidium oocysts in 23 samples (1.68%) from nine farms, and the highest infection rate was 9.38% on farm 2 (Table 1). The infection rates of Cryptosporidium spp. were 10.22%, 0%, 0%, and 0.69% in preweaned, 3–11-month-old, 1–2-year-old, and > 2-year-old cattle, respectively (χ2 = 95.52, P <0.01).

Similarly, 29 samples from 12 farms were positive for Giardia, with an average infection rate of 2.12% (Table 1). The highest infection rate for Giardia was 7.94% on farm 5. The infection rates for Giardia were 10.22%, 2.53%, 0%, and 0% in preweaned, 3–11-month-old, 1–2-year-old, and > 2-year-old cattle, respectively (χ2 = 75.93, P <0.01).

Distribution of Cryptosporidium species/subtypes and G. duodenalisassemblages

The SSU rRNA genes of Cryptosporidium spp. in all 23 microscopy-positive samples were successfully amplified with nested PCR. RFLP and DNA sequence analyses of the SSU rRNA gene fragments revealed the presence of three Cryptosporidium species: C. parvum (n = 15) on six farms, C. bovis (n = 4) on three farms, and C. andersoni (n = 4) on one farm (Table 1). With the exception of farm 2, only one Cryptosporidium species was detected on all the Cryptosporidium-positive farms (Table 1). The gp60 sequencing analysis showed that the 15 C. parvum isolates all belonged to subtype IIdA15G1.

Sequencing analyses of the tpi and gdh genes in G. duodenalis identified two assemblages: E (n = 25) on 10 farms and B (n = 4) on three farms (Table 1). Only farm 3 had both assemblages E and B.

Age distributions of Cryptosporidium and G. duodenalis

Cryptosporidium parvum was the most commonly identified Cryptosporidium species, responsible for 65.2% of all Cryptosporidium infections, and was only found in preweaned calves (Table 2). Cryptosporidium bovis and C. andersoni were found in preweaned calves and > 2-year-old cattle, respectively. In contrast, no Cryptosporidium-positive sample was identified in cattle aged between 3 months and 2 years.

Table 2 Cryptosporidium species identified in dairy cattle in different age groups
Full size table

Giardia duodenalis was only detected in preweaned and 3–11-month-old calves. Among these calves, G. duodenalis assemblage E was the dominant assemblage, responsible for 86.2% (25/29) of all Giardia-positive samples. In contrast, only four assemblage B infections (one subtype B1 and three subtype B2) were found in preweaned calves. Four mixed infections of Cryptosporidium and G. duodenalis were found in preweaned calves (Table 2).

Discussion

The overall infection rate for Cryptosporidium spp. was 1.68%, which is lower than those in Henan (13.0%, 276/2116) [8],[9], Heilongjiang (15.0%, 99/658) [7],[11], Shannxi (3.4%, 70/2071) [12], Anhui (14.9%, 52/350), Jiangsu (20.7%, 251/1215), and Shanghai (12.5%, 55/440) [18]. The average infection rate for G. duodenalis was 2.12%, which is lower than those in Heilongjiang (5.2%, 42/814) [10] and Henan (7.2%, 128/1777) [13]. Oocysts shed at low intensity may be contributed to the low detecting rates of both parasites by microscopy. In general, it is difficult to explain the actual discrepancies in the prevalence of Cryptosporidium spp. and G. duodenalis among different studies because the infection rates are related to many factors, including the examination methods, age distributions of the animals, sample sizes, host health status at the time of sampling, the timing of specimen collection, and geo-ecological conditions. Nevertheless, the infection rates of both parasites were always higher in preweaned calves than in any other age group, which is consistent with previous observations [8]-[10],[19],[20].

Among the preweaned calves, C. parvum was the predominant Cryptosporidium species, rather than C. bovis. This result clearly differs from the results reported in Henan and Heilongjiang, where C. bovis was the dominant species, and in Shannxi, where only C. andersoni was detected [9],[11],[12]. The results of most previous studies, conducted in numerous countries, suggest that C. parvum is the predominant Cryptosporidium species in preweaned calves [9]. In contrast, only C. andersoni was detected in adult cattle in the present study, which was basically similar to the reports of Cryptosporidium infections in cattle in Henan, Heilongjiang, Shannxi, and other countries [7],[8],[12],[21].

The 15 C. parvum isolates were identified as subtype IIdA15G1 based on a sequence analysis of the gp60 gene, which differed from subtype IIdA19G1 found in dairy cattle in Henan and Heilongjiang provinces, China [9],[11]. In fact, except for C. parvum IIa subtypes found in yaks [22], the C. parvum isolates characterized in China thus far have belonged to the IId subtypes, including IIdA15G1 in rodents [23], IIdA19G1 in cattle, humans, and urban wastewater [9],[11],[24],[25]. Thus, the characteristics of C. parvum subtypes appear to be unique in China. Sequence analysis of the gp60 gene has been used extensively to characterize the molecular epidemiology of cryptosporidiosis in animals and humans, and at least 14 C. parvum subtype families have been identified: IIa, IIb, IIc, IId, IIe, IIf, IIg, IIh, IIi, IIk, IIl, IIm, IIn, and IIo [1],[16]. Of these, IIa is the predominant subtype family in animals and humans worldwide, and IId is another major zoonotic subtype family reported in Europe (Hungary, Germany, Portugal, Sweden, Ireland, Spain, Belgium, Romania, United Kingdom, Netherlands, Slovenia, Serbia, and Montenegro), Asia (Kuwait, Iran, Jordan, India, Malaysia, and China), Egypt, and Australia [9],[26]-[29]. In contrast, IIc and IIe are anthroponotic subtype families. Other subtype families of C. parvum are occasionally -seen in various animals or humans around the world [9],[16].

Sequence analyses of the tpi and gdh genes showed that most of the dairy cattle were infected with livestock-specific G. duodenalis assemblage E (86.2%). This result is consistent with a previous study conducted in Heilongjiang and Henan, China [10],[13]. The results of most studies conducted in numerous countries, including Belgium, Denmark, Portugal, Spain, Sweden, Germany, UK, USA, Canada, Brazil, Australia, Rwanda, Egypt, Sri Lanka, and Malaysia, suggest that assemblage E is the predominant Giardia assemblage in cattle [2],[30]-[39].

Giardia duodenalis assemblage B was only found in four preweaned calves in this study. In a previous study conducted in Heilongjiang Province, a higher rate of assemblage B was identified (18/43) in dairy cattle [10], whereas no assemblage B was found in Henan Province [13]. In general, assemblage B has been detected in only a small number of cattle in a few studies worldwide, including in Europe, Italy, Portugal, Uganda, New Zealand, and Canada [2],[30]. Assemblage B, one of the two major assemblages causing human giardiasis, has a broad host range, including cattle, sheep, pigs, horses, dogs, cats, and rabbits [2]. Although no strong evidence supporting the direct zoonotic transmission of G. duodenalis from animals to humans has been reported, case–control studies have shown that contact with farm animals increases the infection rate of human giardiasis [40],[41]. Considering how large the cattle industry is and the close contact that occurs between cattle and humans, assemblage B G. duodenalis identified in cattle may emerge as an important zoonotic pathogen in some areas of China.

Conclusion

In summary, C. parvum is the predominant species in preweaned calves in the study area, which clearly differs from the situation in Henan, Heilongjiang, and Shannxi Provinces. The presence of C. parvum subtype IIdA15G1, together with subtypes IIdA15G1 and IIdA19G1, previously found in rodents, ruminants, and humans, further confirms the dominance of the C. parvum IId subtypes in China. The dominant G. duodenalis assemblage, assemblage E, is similar to the dominant assemblages in other areas or countries.

References

  1. Xiao L, Ryan U: Molecular epidemiology. In Cryptosporidium and Cryptosporidiosis. 2nd edition. Edited by Fayer R, Xiao L. Boca Raton: CRC Press and IWA Publishing; 2008:119–151

    Google Scholar 

  2. Feng Y, Xiao L: Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011, 24: 110-140. 10.1128/CMR.00033-10.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Trout JM, Santín M: Livestock. In Cryptosporidium and Cryptosporidiosis. 2nd edition. Edited by Fayer R, Xiao L. Boca Raton: CRC Press and IWA Publishing; 2008:451–483.

    Google Scholar 

  4. Santín M, Trout JM, Fayer R: A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age. Vet Parasitol. 2008, 155: 15-23. 10.1016/j.vetpar.2008.04.018.

    Article  PubMed  Google Scholar 

  5. Esteban E, Anderson BC: Cryptosporidium muris: prevalence, persistency, and detrimental effect on milk production in a drylot dairy. J Dairy Sci. 1995, 78: 1068-1072. 10.3168/jds.S0022-0302(95)76723-6.

    Article  CAS  PubMed  Google Scholar 

  6. Adam RD: Biology of Giardia lamblia . Clin Microbiol Rev. 2001, 14: 447-475. 10.1128/CMR.14.3.447-475.2001.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Liu A, Wang R, Li Y, Zhang L, Shu J, Zhang W, Feng YY, Xiao LH, Ling H: Prevalence and distribution of Cryptosporidium spp. in dairy cattle in Heilongjiang Province, China. Parasitol Res. 2009, 105: 797-802. 10.1007/s00436-009-1457-2.

    Article  PubMed  Google Scholar 

  8. Wang R, Ma G, Zhao J, Lu Q, Wang H, Zhang L, Jian F, Ning C, Xiao L: Cryptosporidium andersoni is the predominant species in post-weaned and adult dairy cattle in China. Parasitol Int. 2011, 60: 1-4. 10.1016/j.parint.2010.09.002.

    Article  CAS  PubMed  Google Scholar 

  9. Wang R, Wang H, Sun Y, Zhang L, Jian F, Qi M, Ning C, Xiao L: Characteristics of Cryptosporidium transmission in preweaned dairy cattle in henan, China. J Clin Microbiol. 2011, 49: 1077-1082. 10.1128/JCM.02194-10.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Liu A, Zhang X, Zhang L, Wang R, Li X, Shu J, Zhang X, Shen Y, Zhang W, Ling H: Occurrence of bovine giardiasis and endemic genetic characterization of Giardia duodenalis isolates in Heilongjiang Province, in the Northeast of China. Parasitol Res. 2012, 111: 655-661. 10.1007/s00436-012-2883-0.

    Article  PubMed  Google Scholar 

  11. Zhang W, Wang R, Yang F, Zhang L, Cao J, Zhang X, Ling H, Liu A, Shen Y: Distribution and genetic characterizations of Cryptosporidium spp. in pre-weaned dairy calves in Northeastern China’s Heilongjiang Province. PLoS One. 2013, 8: e54857-10.1371/journal.pone.0054857.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Zhao G, Ren W, Gao M, Bian Q, Hu B, Cong M, Lin Q, Wang R, Qi M, Qi M, Zhu X, Zhang L: Genotyping Cryptosporidium andersoni in cattle in Shaanxi province, Northwestern China. PLoS One. 2013, 8: e60112-10.1371/journal.pone.0060112.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. 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: e100453-10.1371/journal.pone.0100453.

    Article  PubMed  Google Scholar 

  14. Feng Y, Ortega Y, He G, Das P, Xu M, Zhang X, Fayer R, Gatei W, Cama V, Xiao L: Wide geographic distribution of Cryptosporidium bovis and the deer-like genotype in bovines. Vet Parasitol. 2007, 144: 1-9. 10.1016/j.vetpar.2006.10.001.

    Article  PubMed  Google Scholar 

  15. Sulaiman IM, Hira PR, Zhou L, Al-Ali FM, Al-Shelahi FA, Shweiki HM, Iqbal J, Khalid N, Xiao L: Unique endemicity of cryptosporidiosis in children in Kuwait. J Clin Microbiol. 2005, 43: 2805-2809. 10.1128/JCM.43.6.2805-2809.2005.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Xiao L: Molecular epidemiology of cryptosporidiosis: An update. Exp Parasitol. 2010, 124: 80-89. 10.1016/j.exppara.2009.03.018.

    Article  CAS  PubMed  Google Scholar 

  17. 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. 10.1016/j.ijpara.2008.04.008.

    Article  CAS  PubMed  Google Scholar 

  18. Chen F, Huang K: Prevalence and molecular characterization of Cryptosporidium spp. in dairy cattle from farms in China. J Vet Sci. 2012, 13: 15-22. 10.4142/jvs.2012.13.1.15.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Geurden T, Vanderstichel R, Pohle H, Ehsan A, von Samson-Himmelstjerna G, Morgan ER, Camuset P, Capelli G, Vercruysse J, Claerebout E: A multicentre prevalence study in Europe on Giardia duodenalis in calves, with molecular identification and risk factor analysis. Vet Parasitol. 2012, 190: 383-390. 10.1016/j.vetpar.2012.06.039.

    Article  CAS  PubMed  Google Scholar 

  20. 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 in press.

  21. Xiao L, Fayer R: Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol. 2008, 38: 1239-1255. 10.1016/j.ijpara.2008.03.006.

    Article  CAS  PubMed  Google Scholar 

  22. Mi R, Wang X, Li C, Huang Y, Zhou P, Li Z, Lei M, Cai J, Chen Z: Prevalence and genetic characterization of Cryptosporidium in yaks in Qinghai Province of China. PLoS One. 2013, 8: e74985-10.1371/journal.pone.0074985.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Lv C, Zhang L, Wang R, Jian F, Zhang S, Ning C, Wang H, Feng C, Wang X, Ren X, Qi M, Xiao L: Cryptosporidium spp. in wild, laboratory, and pet rodents in china: prevalence and molecular characterization. Appl Environ Microbiol. 2009, 75: 7692-7699. 10.1128/AEM.01386-09.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Li N, Xiao L, Wang L, Zhao S, Zhao X, Duan L, Guo M, Liu L, Feng Y: Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Negl Trop Dis. 2012, 6: e1809-10.1371/journal.pntd.0001809.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Wang L, Zhang H, Zhao X, Zhang L, Zhang G, Guo M, Liu L, Feng Y, Xiao L: Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J Clin Microbiol. 2013, 51: 557-563. 10.1128/JCM.02758-12.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Insulander M, Silverlås C, Lebbad M, Karlsson L, Mattsson JG, Svenungsson B: Molecular epidemiology and clinical manifestations of human cryptosporidiosis in Sweden. Epidemiol Infect. 2013, 141: 1009-1020. 10.1017/S0950268812001665.

    Article  CAS  PubMed  Google Scholar 

  27. Amer S, Zidan S, Feng Y, Adamu H, Li N, Xiao L: Identity and public health potential of Cryptosporidium spp. in water buffalo calves in Egypt. Vet Parasitol. 2013, 191: 123-127. 10.1016/j.vetpar.2012.08.015.

    Article  PubMed  Google Scholar 

  28. Iqbal A, Lim YA, Surin J, Sim BL: High diversity of Cryptosporidium subgenotypes identified in Malaysian HIV/AIDS individuals targeting gp60 gene. PLoS One. 2012, 7: e31139-10.1371/journal.pone.0031139.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Imre K, Luca C, Costache M, Sala C, Morar A, Morariu S, Ilie MS, Imre M, Dărăbuş G: Zoonotic Cryptosporidium parvum in Romanian newborn lambs (Ovis aries). Vet Parasitol. 2013, 191: 119-122. 10.1016/j.vetpar.2012.08.020.

    Article  CAS  PubMed  Google Scholar 

  30. Budu-Amoako E, Greenwood SJ, Dixon BR, Barkema HW, McClure JT: Giardia and Cryptosporidium on dairy farms and the role these farms may play in contaminating water sources in Prince Edward Island, Canada. J Vet Intern Med. 2012, 26: 668-673. 10.1111/j.1939-1676.2012.00930.x.

    Article  CAS  PubMed  Google Scholar 

  31. Mark-Carew MP, Wade SE, Chang YF, Schaaf S, Mohammed HO: Prevalence of Giardia duodenalis assemblages among dairy herds in the New York City Watershed. Vet Parasitol. 2012, 185: 151-157. 10.1016/j.vetpar.2011.09.030.

    Article  PubMed  Google Scholar 

  32. Muhid A, Robertson I, Ng J, Yang R, Ryan U: Prevalence of Giardia spp. infection in pre-weaned and weaned calves in relation to management factors. Vet J. 2012, 191: 135-137. 10.1016/j.tvjl.2011.01.007.

    Article  PubMed  Google Scholar 

  33. Silva FM P e, Lopes RS, Araújo JP: Genetic characterisation of Giardia duodenalis in dairy cattle in Brazil. Folia Parasitol (Praha). 2012, 59: 15-20. 10.14411/fp.2012.003.

    Article  Google Scholar 

  34. Santin M, Dargatz D, Fayer R: Prevalence of Giardia duodenalis assemblages in weaned cattle on cow-calf operations in the United States. Vet Parasitol. 2012, 183: 231-236. 10.1016/j.vetpar.2011.07.042.

    Article  PubMed  Google Scholar 

  35. Amer SE: Genotypic and phylogenetic characterization of Giardia intestinalis from human and dairy cattle in Kafr El Sheikh Governorate, Egypt. J Egypt Soc Parasitol. 2013, 43: 133-146.

    Article  PubMed  Google Scholar 

  36. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, Faria ES, Cunha MJ, Couto TR, Cury MC: 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, 2013: 875048-10.1155/2013/875048.

    Article  PubMed Central  PubMed  Google Scholar 

  37. Gillhuber J, Pallant L, Ash A, Thompson RC, Pfister K, Scheuerle MC: Molecular identification of zoonotic and livestock-specific Giardia-species in faecal samples of calves in Southern Germany. Parasitol Vectors. 2013, 6: 346-10.1186/1756-3305-6-346.

    Article  Google Scholar 

  38. Abeywardena H, Jex AR, Koehler AV, Rajapakse RP, Udayawarna K, Haydon SR, Stevens MA, Gasser RB: First molecular characterization of Cryptosporidium and Giardia from bovines (Bos taurus and Bubalus bubalis) in Sri Lanka: unexpected absence of C. parvum from pre-weaned calves. Parasitol Vectors. 2014, 7: 75-10.1186/1756-3305-7-75.

    Article  Google Scholar 

  39. 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. 10.7589/2012-09-229.

    Article  PubMed  Google Scholar 

  40. Hoque ME, Hope VT, Kjellstrom T, Scragg R, Lay-Yee R: Risk of giardiasis in Aucklanders: a case–control study. Int J Infect Dis. 2002, 6: 191-197. 10.1016/S1201-9712(02)90110-4.

    Article  PubMed  Google Scholar 

  41. Hoque ME, Hope VT, Scragg R, Kjellstrom T: Children at risk of giardiasis in Auckland: a case–control analysis. Epidemiol Infect. 2003, 131: 655-662. 10.1017/S0950268803008598.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported, in part, by the National Natural Science Foundation of China (U1204328 and 31302079), the Specialized Research Fund for the Doctoral Program of Higher Education (20124105120003), and the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-37).

Author information

Authors and Affiliations

  1. College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou, 450002, China

    Jianying Huang, Daoyou Yue, Meng Qi, Rongjun Wang, Jinfeng Zhao, Junqiang Li, Ke Shi & Longxian Zhang

  2. International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou, 450002, China

    Jianying Huang, Daoyou Yue, Meng Qi, Rongjun Wang, Junqiang Li, Ke Shi & Longxian Zhang

  3. College of Veterinary Medicine, China Agricultural University, Beijing, 100193, China

    Ming Wang

Authors
  1. Jianying Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daoyou Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rongjun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinfeng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Junqiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ke Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Longxian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Rongjun Wang or Longxian Zhang.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

LXZ and RJW designed the experiments; JYH, DYY, and MQ performed the study; JFZ and JQL analyzed the data; KS and MW contributed reagents/materials/analysis tools; RJW, LXZ, and JYH wrote the paper. All authors have read and approved the final version of the manuscript.

Rights and permissions

Open Access  This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.

The Creative Commons Public Domain Dedication waiver (https://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, J., Yue, D., Qi, M. et al. Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalisin dairy cattle in Ningxia, northwestern China. BMC Vet Res 10, 292 (2014). https://doi.org/10.1186/s12917-014-0292-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12917-014-0292-6

Keywords

BMC Veterinary Research

ISSN: 1746-6148

Contact us