Prevalence and genotypic identification of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in pre-weaned dairy calves in Guangdong, China

. 2019 Jan 17 ; 12 (1) : 41. [epub] 20190117

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30654832

Grantová podpora
31820103014 National Natural Science Foundation of China
31630078 National Natural Science Foundation of China

Odkazy

PubMed 30654832
PubMed Central PMC6337774
DOI 10.1186/s13071-019-3310-5
PII: 10.1186/s13071-019-3310-5
Knihovny.cz E-zdroje

BACKGROUND: Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi are common enteric pathogens in humans and animals. Data on the transmission of these pathogens are scarce from Guangdong, China, which has a subtropical monsoon climate and is the epicenter for many emerging infectious diseases. This study was conducted to better understand the prevalence and identity of the three pathogens in pre-weaned dairy calves in Guangdong. METHODS: The occurrence and genetic identity of three pathogens were analyzed by polymerase chain reaction. PCR-positive products were sequenced to determine the species and genotypes. A Chi-square test was used to compare the prevalence of pathogens among sampling dates, age groups, or clinical signs. RESULTS: The detection rates of Cryptosporidium spp., G. duodenalis and E. bieneusi were 24.0% (93/388), 74.2% (288/388) and 15.7% (61/388), respectively. Three Cryptosporidium species were detected, including C. bovis (n = 73), C. parvum (n = 12) and C. ryanae (n = 7); one animal had concurrence of C. bovis and C. parvum. C. parvum was the dominant species during the first two weeks of life, whereas C. bovis and C. ryanae were mostly seen at 3-9 weeks of age. Sequence analysis identified the C. parvum as subtype IIdA19G1. Assemblage E (n = 282), assemblage A (n = 1), and concurrence of A and E (n = 5) were identified among G. duodenalis-positive animals using multilocus genotyping (MLG). Altogether, 15, 10 and 17 subtypes of assemblage E were observed at the bg, gdh and tpi loci, respectively, forming 49 assemblage E MLGs. The highest detection rate of G. duodenalis was found in winter. Sequence analysis identified genotypes J (n = 57), D (n = 3) and one concurrence of J and D among E. bieneusi-positive animals. The detection rate of E. bieneusi was significantly higher in spring (38.0%; 41/108) than in summer (7.2%; 8/111) and winter (7.1%; 12/169). CONCLUSIONS: These results indicate a common occurrence of C. parvum subtype IIdA19G1, G. duodenalis assemblage E, and E. bieneusi genotype J in pre-weaned dairy calves in Guangdong. More studies are needed to understand the unique genetic characteristics and zoonotic potential of the three enteric pathogens in the province.

Zobrazit více v PubMed

Santín M, Fayer R. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci. 2011;90:363–371. doi: 10.1016/j.rvsc.2010.07.014. PubMed DOI

Feng YY, Xiao LH. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbio Rev. 2011;24:110–140. doi: 10.1128/CMR.00033-10. PubMed DOI PMC

Xiao LH. Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol. 2010;124:80–89. doi: 10.1016/j.exppara.2009.03.018. PubMed DOI

Feng Y, Xiao L. Molecular epidemiology of cryptosporidiosis in China. Front Microbiol. 2017;8:1701. doi: 10.3389/fmicb.2017.01701. PubMed DOI PMC

Ryan U, Fayer R, Xiao LH. Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology. 2014;141:1667–1685. doi: 10.1017/S0031182014001085. PubMed DOI

Wang RJ, Zhao GH, Gong YY, Zhang LX. Advances and perspectives on the epidemiology of bovine Cryptosporidium in China in the past 30 years. Front Microbiol. 2017;8:1823. doi: 10.3389/fmicb.2017.01823. PubMed DOI PMC

Wang RJ, Wang HL, Sun YR, Zhang LX, Jian FC, Qi M, et al. Characteristics of Cryptosporidium transmission in preweaned dairy cattle in Henan, China. J Clin Microbiol. 2011;49:1077–1082. doi: 10.1128/JCM.02194-10. PubMed DOI PMC

Ma J, Li P, Zhao X, Xu H, Wu W, Wang Y, et al. Occurrence and molecular characterization of Cryptosporidium spp. and Enterocytozoon bieneusi in dairy cattle, beef cattle and water buffaloes in China. Vet Parasitol. 2015;207:220–227. doi: 10.1016/j.vetpar.2014.10.011. PubMed DOI

Qi MZ, Fang YQ, Wang XT, Zhang LX, Wang RJ, Du SZ, et al. Molecular characterization of Cryptosporidium spp. in pre-weaned calves in Shaanxi Province, north-western China. J Med Microbiol. 2015;64:111–116. doi: 10.1099/jmm.0.079327-0. PubMed DOI

Zhang XX, Tan QD, Zhou DH, Ni XT, Liu GX, Yang YC, et al. Prevalence and molecular characterization of Cryptosporidium spp. in dairy cattle, northwest China. Parasitol Res. 2015;114:2781–2787. doi: 10.1007/s00436-015-4537-5. PubMed DOI

Cai M, Guo YQ, Pan BL, Li N, Wang XL, Tang CX, et al. Longitudinal monitoring of Cryptosporidium species in pre-weaned dairy calves on five farms in Shanghai, China. Vet Parasitol. 2017;241:14–19. doi: 10.1016/j.vetpar.2017.05.005. PubMed DOI

Fan YY, 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. doi: 10.1186/s13071-017-2463-3. PubMed DOI PMC

Zhong ZJ, Dan JM, Yan GW, Tu R, Tian YA, Cao SZ, et al. Occurrence and genotyping of Giardia duodenalis and Cryptosporidium in pre-weaned dairy calves in central Sichuan Province, China. Parasite. 2018;25:45. doi: 10.1051/parasite/2018046. PubMed DOI PMC

Huang J, Yue D, Qi M, Wang R, Zhao J, Li J, et al. Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in dairy cattle in Ningxia, northwestern China. BMC Vet Res. 2014;10:292. doi: 10.1186/s12917-014-0292-6. PubMed DOI PMC

Qi M, Wang H, Jing B, Wang D, Wang R, Zhang L. Occurrence and molecular identification of Cryptosporidium spp. in dairy calves in Xinjiang, northwestern China. Vet Parasitol. 2015;212:404–7. PubMed

Li F, Wang H, Zhang Z, Li J, Wang C, Zhao J, et al. Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in dairy cattle in Beijing, China. Vet Parasitol. 2016;219:61–65. doi: 10.1016/j.vetpar.2016.01.023. PubMed DOI

Hu S, Liu Z, Yan F, Zhang Z, Zhang G, Zhang L, et al. Zoonotic and host-adapted genotypes of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in dairy cattle in Hebei and Tianjin, China. Vet Parasitol. 2017;248:68–73. doi: 10.1016/j.vetpar.2017.10.024. PubMed DOI

Tao W, Li Y, Yang H, Song M, Lu Y, Li W. Widespread occurrence of zoonotic Cryptosporidium species and subtypes in dairy cattle from northeast China: public health concerns. J Parasitol. 2018;104:10–7. PubMed

Silverlås C, Näslund K, Björkman C, Mattsson JG. Molecular characterisation of Cryptosporidium isolates from Swedish dairy cattle in relation to age, diarrhoea and region. Vet Parasitol. 2010;169:289–295. doi: 10.1016/j.vetpar.2010.01.003. PubMed DOI

Muhid A, Robertson I, Ng J, Ryan U. Prevalence of and management factors contributing to Cryptosporidium spp. infection in pre-weaned and post-weaned calves in Johor, Malaysia. Exp Parasitol. 2011;127:534–8. PubMed

Amer S, Zidan S, Feng YY, Adamu H, Li N, Xiao LH. Identity and public health potential of Cryptosporidium spp. in water buffalo calves in Egypt. Vet Parasitol. 2013;191:123–127. doi: 10.1016/j.vetpar.2012.08.015. PubMed DOI

Becher KA, Robertson ID, Fraser DM, Palmer DG, Thompson RCA. Molecular epidemiology of Giardia and Cryptosporidium infections in dairy calves originating from three sources in Western Australia. Vet Parasitol. 2004;123:1–9. doi: 10.1016/j.vetpar.2004.05.020. PubMed DOI

Azcona-Gutierrez JM, de Lucio A, Hernandez-de-Mingo M, Garcia-Garcia C, Soria-Blanco LM, Morales L, et al. 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. PubMed PMC

Wang XL, Cai M, Jiang W, Wang YP, Jin Y, Li N, et al. 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. doi: 10.1007/s00436-017-5509-8. PubMed DOI

Meng Q, Wang H, Jing B, Wang R, Jian F, Ning C, et al. Prevalence and multilocus genotyping of Giardia duodenalis in dairy calves in Xinjiang, northwestern China. Parasit Vectors. 2016;9:546. PubMed PMC

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. doi: 10.1007/s11250-016-1013-x. PubMed DOI

Wang XT, Wang RJ, Ren GJ, Yu ZQ, Zhang LX, Zhang SY, et al. Multilocus genotyping of Giardia duodenalis and Enterocytozoon bieneusi in dairy and native beef (Qinchuan) calves in Shaanxi Province, northwestern China. Parasitol Res. 2016;115:1355–1361. doi: 10.1007/s00436-016-4908-6. PubMed DOI

Wegayehu T, Karim MR, Erko B, Zhang LX, Tilahun G. Multilocus genotyping of Giardia duodenalis isolates from calves in Oromia Special Zone, central Ethiopia. Infect Genet Evol. 2016;43:281–8. PubMed

Jian Y, Zhang X, Li X, Karanis G, Ma L, Karanis P. Prevalence and molecular characterization of Giardia duodenalis in cattle and sheep from the Qinghai-Tibetan Plateau Area (QTPA), northwestern China. Vet Parasitol. 2018;250:40–44. doi: 10.1016/j.vetpar.2017.12.001. PubMed DOI

Abeywardena H, Jex AR, Koehler AV, Rajapakse RP, Udayawarna K, Haydon SR, et al. 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. Parasit Vectors. 2014;7:75. doi: 10.1186/1756-3305-7-75. PubMed DOI PMC

Winkworth CL, Learmonth JJ, Matthaei CD, Townsend CR. Molecular characterization of Giardia isolates from calves and humans in a region in which dairy farming has recently intensified. Appl Environ Microb. 2008;74:5100–5105. doi: 10.1128/AEM.00232-08. PubMed DOI PMC

Wang HY, Zhao GH, Chen GY, Jian FC, Zhang SM, Feng C, et al. Multilocus genotyping of Giardia duodenalis in dairy cattle in Henan, China. PLoS One. 2014;9:e100453. doi: 10.1371/journal.pone.0100453. PubMed DOI PMC

Abdel-Moein KA, Saeed H. The zoonotic potential of Giardia intestinalis assemblage E in rural settings. Parasitol Res. 2016;115:3197–3202. doi: 10.1007/s00436-016-5081-7. PubMed DOI

Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM. Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis. 2016;214:1256–1259. doi: 10.1093/infdis/jiw361. PubMed DOI

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. doi: 10.1017/S0031182017000439. PubMed DOI

Jiang Y, Tao W, Wan Q, Li Q, Yang Y, Lin Y, et al. Zoonotic and potentially host-adapted Enterocytozoon bieneusi genotypes in sheep and cattle in northeast China and an increasing concern about the zoonotic importance of previously considered ruminant-adapted genotypes. Appl Environ Microbio. 2015;81:3326–3335. doi: 10.1128/AEM.00328-15. PubMed DOI PMC

Del Coco VF, Córdoba MA, Bilbao G, De ACP, Basualdo JA, Santín M. First report of Enterocytozoon bieneusi from dairy cattle in Argentina. Vet Parasitol. 2014;199:112–115. doi: 10.1016/j.vetpar.2013.09.024. PubMed DOI

Matos O, Lobo ML, Xiao L. Epidemiology of Enterocytozoon bieneusi infection in humans. J Parasitol Res. 2012;2012:981424. doi: 10.1155/2012/981424. PubMed DOI PMC

Tang C, Cai M, Wang L, Guo Y, Li N, Feng Y, et al. Genetic diversity within dominant Enterocytozoon bieneusi genotypes in pre-weaned calves. Parasit Vectors. 2018;11:170. doi: 10.1186/s13071-018-2768-x. PubMed DOI PMC

Qi M, Jing B, Jian F, Wang R, Zhang S, Wang H, et al. Dominance of Enterocytozoon bieneusi genotype J in dairy calves in Xinjiang, northwest China. Parasitol Int. 2017;66:960–3. PubMed

Li J, Luo N, Wang C, Meng Q, Cao J, Cui Z, et al. Occurrence, molecular characterization and predominant genotypes of Enterocytozoon bieneusi in dairy cattle in Henan and Ningxia, China. Parasit Vectors. 2016;9:142. doi: 10.1186/s13071-016-1425-5. PubMed DOI PMC

Da SFV, Lopes CW, de Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol. 2016;216:46–51. doi: 10.1016/j.vetpar.2015.12.008. PubMed DOI

Liang N, Wu Y, Sun M, Chang Y, Lin X, Yu L, et al. Molecular epidemiology of Cryptosporidium spp. in dairy cattle in Guangdong Province, south China. Parasitology. 2018. 10.1017/S0031182018001129. PubMed

Zhang XX, Tan QD, Zhao GH, Ma JG, Zheng WB, Ni XT, et al. Prevalence, risk factors and multilocus genotyping of Giardia intestinalis in dairy cattle, northwest China. J Eukaryot Microbiol. 2016;63:498–504. doi: 10.1111/jeu.12293. PubMed DOI

Qi M, Wang RJ, Jing B, Jian FC, Ning CS, Zhang LX. Prevalence and multilocus genotyping of Cryptosporidium andersoni in dairy cattle and He cattle in Xinjiang. China. Infect Genet Evol. 2016;44:313–7. PubMed

Zhao W, Zhang W, Yang F, Zhang L, Wang R, Cao J, et al. Enterocytozoon bieneusi in dairy cattle in the northeast of China: genetic diversity of ITS gene and evaluation of zoonotic transmission potential. J Eukaryot Microbiol. 2015;62:553–560. doi: 10.1111/jeu.12210. PubMed DOI

Cui Z, Wang L, Cao L, Sun M, Liang N, Wang H, et al. Genetic characteristics and geographic segregation of Giardia duodenalis in dairy cattle from Guangdong Province, southern China. Infect Genet Evol. 2018;66:95–100. doi: 10.1016/j.meegid.2018.09.019. PubMed DOI

Jiang JL, Alderisio KA, Singh A, Xiao LH. Development of procedures for direct extraction of Cryptosporidium DNA from water concentrates and for relief of PCR inhibitors. Appl Environ Microb. 2005;71:1135–1141. doi: 10.1128/AEM.71.3.1135-1141.2005. PubMed DOI PMC

Ryan U, Xiao LH, Read C, Zhou L, Lal AA, Pavlasek I. Identification of novel Cryptosporidium genotypes from the Czech Republic. Appl Environ Microb. 2003;69:4302–4307. doi: 10.1128/AEM.69.7.4302-4307.2003. PubMed DOI PMC

Feng YY, Li N, Duan LP, Xiao LH. Cryptosporidium genotype and subtype distribution in raw wastewater in Shanghai, China: evidence for possible unique Cryptosporidium hominis transmission. J Clin Microbiol. 2009;47:153–157. doi: 10.1128/JCM.01777-08. PubMed DOI PMC

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. doi: 10.1016/j.ijpara.2008.04.008. PubMed DOI

Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW, Xiao L. Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl Environ Microbiol. 2003;69:4495. PubMed PMC

Chen F, Huang KH. Prevalence and molecular characterization of Cryptosporidium spp. in dairy cattle from farms in China. J Vet Sci. 2012;13:15–22. doi: 10.4142/jvs.2012.13.1.15. PubMed DOI PMC

Zhang W, Wang R, Yang F, Zhang L, Cao J, Zhang X, et al. Distribution and genetic characterizations of Cryptosporidium spp. in pre-weaned dairy calves in northeastern China’s Heilongjiang Province. PLoS One. 2013;8:e54857. PubMed PMC

Liu G, Su Y, Zhou M, Zhao J, Zhang T, Ahmad W, et al. Prevalence and molecular characterization of Giardia duodenalis isolates from dairy cattle in northeast China. Exp Parasitology. 2015:15420–4. PubMed

Liu A, Zhang X, Zhang L, Wang R, Li X, Shu J, et al. Occurrence of bovine giardiasis and endemic genetic characterization of Giardia duodenalis isolates in Heilongjiang Province, in the northeast of China. Parasitol Res. 2012;111:655–61. PubMed

Zhang X, Wang Z, Su Y, Liang X, Sun X, Peng S, et al. Identification and genotyping of Enterocytozoon bieneusi in China. J Clin Microbiol. 2011;49:2006–2008. doi: 10.1128/JCM.00372-11. PubMed DOI PMC

Huetink RE, van der Giessen JW, Noordhuizen JP, Ploeger HW. Epidemiology of Cryptosporidium spp. and Giardia duodenalis on a dairy farm. Vet Parasitol. 2001;102:53–67. doi: 10.1016/S0304-4017(01)00514-3. PubMed DOI

Alum A, Absar IM, Asaad H, Rubino JR, Ijaz MK. Impact of environmental conditions on the survival of Cryptosporidium and Giardia on environmental surfaces. Interdiscip Perspect Infect Dis. 2014;2014:210385. doi: 10.1155/2014/210385. PubMed DOI PMC

Lee JH. Prevalence and molecular characteristics of Enterocytozoon bieneusi in cattle in Korea. Parasitol Res. 2007;101:391–396. doi: 10.1007/s00436-007-0468-0. PubMed DOI

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. doi: 10.1016/j.vetpar.2008.04.018. PubMed DOI

Cui Z, Wang R, Huang J, Wang H, Zhao J, Luo N, et al. Cryptosporidiosis caused by Cryptosporidium parvum subtype IIdA15G1 at a dairy farm in northwestern China. Parasit Vectors. 2014;7:529. PubMed PMC

Wang L, Zhang HW, Zhao XD, Zhang LX, Zhang GQ, Guo MJ, et al. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J Clin Microbiol. 2013;51:557–63. PubMed PMC

Insulander M, Silverlas 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. doi: 10.1017/S0950268812001665. PubMed DOI PMC

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. doi: 10.1371/journal.pone.0031139. PubMed DOI PMC

Chalmers RM, Smith RP, Hadfield SJ, Elwin K, Giles M. Zoonotic linkage and variation in Cryptosporidium parvum from patients in the United Kingdom. Parasitol Res. 2011;108:1321–1325. doi: 10.1007/s00436-010-2199-x. PubMed DOI

Hijjawi N, Ng J, Yang RC, Atoum MFM, Ryan U. Identification of rare and novel Cryptosporidium gp60 subtypes in human isolates from Jordan. Exp Parasitol. 2010;125:161–164. doi: 10.1016/j.exppara.2010.01.011. PubMed DOI

Zintl A, Proctor AF, Read C, Dewaal T, Shanaghy N, Fanning S, et al. The prevalence of Cryptosporidium species and subtypes in human faecal samples in Ireland. Epidemiol Infect. 2009;137:270–277. doi: 10.1017/S0950268808000769. PubMed DOI

Waldron LS, Ferrari BC, Power ML. Glycoprotein 60 diversity in C. hominis and C. parvum causing human cryptosporidiosis in NSW, Australia. Exp Parasitol. 2009;122:124–127. doi: 10.1016/j.exppara.2009.02.006. PubMed DOI

Wielinga PR, de Vries A, van der Goot TH, Mank T, Mars MH, Kortbeek LM, et al. Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. Int J Parasitol. 2008;38:809–817. doi: 10.1016/j.ijpara.2007.10.014. PubMed DOI

Alves M, Xiao LH, Antunes F, Matos O. Distribution of Cryptosporidium subtypes in humans and domestic and wild ruminants in Portugal. Parasitol Res. 2006;99:287–292. doi: 10.1007/s00436-006-0164-5. PubMed DOI

Abe N, Matsubayashi M, Kimata I, Iseki M. Subgenotype analysis of Cryptosporidium parvum isolates from humans and animals in Japan using the 60-kDa glycoprotein gene sequences. Parasitol Res. 2006;99:303–305. doi: 10.1007/s00436-006-0140-0. PubMed DOI

Sulaiman IM, Hira PR, Zhou L, Al-Ali FM, Al-Shelahi FA, Shweiki HM, et al. Unique endemicity of cryptosporidiosis in children in Kuwait. J Clin Microbiol. 2005;43:2805–2809. doi: 10.1128/JCM.43.6.2805-2809.2005. PubMed DOI PMC

Asher AJ, Hose G, Power ML. 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. 2016;44:157–161. doi: 10.1016/j.meegid.2016.06.051. PubMed DOI

Inpankaew T, Jiyipong T, Thadtapong N, Kengradomkij C, Pinyopanuwat N, Chimnoi W, et al. Prevalence and genotype of Giardia duodenalis in dairy cattle from northern and northeastern part of Thailand. Acta Parasitol. 2015;60:459–461. PubMed

Aguiar JM, Silva SO, Santos VA, Taniwaki SA, Oliveira TM, Ferreira HL, et al. Evidence of heterozygosity and recombinant alleles in single cysts of Giardia duodenalis. Rev Bras Parasitol Vet. 2016;25:187–195. doi: 10.1590/S1984-29612016031. PubMed DOI

Santin M, Fayer R. A longitudinal study of Enterocytozoon bieneusi in dairy cattle. Parasitol Res. 2009;105:141–144. doi: 10.1007/s00436-009-1374-4. PubMed DOI

Wang L, Xiao LH, Duan LP, Ye JB, Guo YQ, Guo MJ, et al. Concurrent infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in children during a cryptosporidiosis outbreak in a pediatric hospital in China. PLoS Negl Trop Dis. 2013;7:e2437. doi: 10.1371/journal.pntd.0002437. PubMed DOI PMC

Wang T, Fan YY, Koehler AV, Ma GX, Li T, Hu M, et al. First survey of Cryptosporidium, Giardia and Enterocytozoon in diarrhoeic children from Wuhan, China. Infect Genet Evol. 2017;51:127–131. doi: 10.1016/j.meegid.2017.03.006. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...