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Prevalence and Molecular Characterization of Intestinal Trichomonads in Pet Dogs in East China

  • Li, Wen-Chao (College of Animal Science, Anhui Science and Technology University) ;
  • Wang, Kai (College of Animal Science, Anhui Science and Technology University) ;
  • Zhang, Wei (College of Animal Science, Anhui Science and Technology University) ;
  • Wu, Jingjing (College of Animal Science, Anhui Science and Technology University) ;
  • Gu, You-Fang (College of Animal Science, Anhui Science and Technology University) ;
  • Zhang, Xi-Chen (College of Veterinary Medicine, Jilin University)
  • Received : 2016.06.27
  • Accepted : 2016.09.27
  • Published : 2016.12.31

Abstract

The trichomonad species Tritrichomonas foetus and Pentatrichomonas hominis were recently detected in the feces of dogs with diarrhea. However, little information is available on the prevalence and pathogenicity of these parasites in the canine population. Therefore, the aim of this study was to determine the prevalence and molecular characterization of trichomonads infecting pet dogs in Anhui and Zhejiang provinces, east China. In total, 315 pet dogs, with or without diarrhea, from 7 pet hospitals were included in this epidemiological survey. Microscopy and PCR detected P. hominis in 19.7% (62/315) and 31.4% (99/315) of fecal samples, respectively. T. foetus infection was detected in 0% (0/315) of samples with microscopy and in 0.6% (2/315) with PCR. The prevalence of P. hominis was significantly higher in young dogs (${\leq}12months$) than in adult dogs (>12 months), and was significantly higher in diarrheic dogs (50.6%) than in non-diarrheic dogs (24.3%; P<0.05). Infection with T. foetus did not correlate with any risk factors evaluated in this study. A sequence analysis of the P. hominis PCR products showed minor allelic variations between our sequences and those of P. hominis strains from other hosts in different parts of the world. Type CC1 was the most common strain in dogs in east China. The internal transcribed spacer 1 (ITS1)-5.8S rRNA gene sequences from the 2 T. foetus isolates detected in this study displayed 100% identity and were homologous to the sequences of other strains isolated from domestic cats in other countries.

Keywords

References

  1. Tolbert MK, Leutenegger CM, Lobetti R, Birrell J, Gookin JL. Species identification of trichomonads and associated coinfections in dogs with diarrhea and suspected trichomonosis. Vet Parasitol 2012; 187: 319-322. https://doi.org/10.1016/j.vetpar.2011.12.031
  2. Li WC, Gong PT, Ying M, Li JH, Yang J, Li H, Yang ZT, Zhang GC, Zhang XC. Pentatrichomonas hominis: first isolation from the feces of a dog with diarrhea in China. Parasitol Res 2014; 113: 1795-1801. https://doi.org/10.1007/s00436-014-3825-9
  3. Gookin JL, Birkenheuer AJ, St John V, Spector M, Levy MG. Molecular characterization of trichomonads from feces of dogs with diarrhea. J Parasitol 2005; 91: 939-943. https://doi.org/10.1645/GE-474R.1
  4. Felleisen RS. Host-parasite interaction in bovine infection with Tritrichomonas foetus. Microbes Infect 1999; 1:807-816. https://doi.org/10.1016/S1286-4579(99)80083-5
  5. Ibanez-Escribano A, Nogal-Ruiz JJ, Delclaux M, Martinez-Nevado E, Ponce-Gordo F. Morphological and molecular identification of Tetratrichomonas flagellates from the giant anteater (Myrmecophaga tridactyla). Res Vet Sci 2013; 95: 176-181. https://doi.org/10.1016/j.rvsc.2013.01.022
  6. Gookin JL, Stauffer SH, Levy MG. Identification of Pentatrichomonas hominis in feline fecal samples by polymerase chain reaction assay. Vet Parasitol 2007; 145: 11-15. https://doi.org/10.1016/j.vetpar.2006.10.020
  7. Kim YA, Kim HY, Cho SH, Cheun HI, Yu JR, Lee SE. PCR detection and molecular characterization of Pentatrichomonas hominis from feces of dogs with diarrhea in the Republic of Korea. Korean J Parasitol 2010; 48: 9-13. https://doi.org/10.3347/kjp.2010.48.1.9
  8. Dimasuay KG, Rivera WL. Molecular characterization of trichomonads isolated from animal hosts in the Philippines. Vet Parasitol 2013; 196: 289-295. https://doi.org/10.1016/j.vetpar.2013.03.019
  9. Grellet A, Brunopolack, Feugier A, Boucraut-Baralon C, Grandjean D, Vandewynckel L, Cian A, Meloni D, Viscogliosi E. Prevalence, risk factors of infection and molecular characterization of trichomonads in puppies from French breeding kennels.Vet Parasitol 2013; 197: 418-426. https://doi.org/10.1016/j.vetpar.2013.07.030
  10. Li WC, Ying M, Gong PT, Li JH, Yang J, Li H, Zhang XC. Pentatrichomonas hominis: prevalence and molecular characterization in humans, dogs, and monkeys in Northern China. Parasitol Res 2016; 115: 569-574. https://doi.org/10.1007/s00436-015-4773-8
  11. Parsonson IM, Clark BL, Dufty JH. Early pathogenesis and pathology of Tritrichomonas foetus infection in virgin heifers. J Comp Pathol 1976; 86: 59-66. https://doi.org/10.1016/0021-9975(76)90028-1
  12. Frey CF, Schild M, Hemphill A, Stunzi P, Muller N, Gottstein B, Burgener IA. Intestinal Tritrichomonas foetus infection in cats in Switzerland detected by in vitro cultivation and PCR. Parasitol Res 2009; 104: 783-788. https://doi.org/10.1007/s00436-008-1255-2
  13. Yao C, Koster LS. Tritrichomonas foetus infection, a cause of chronic diarrhea in the domestic cat. Vet Res 2015; 46: 35. https://doi.org/10.1186/s13567-015-0169-0
  14. Lun ZR, Chen XG, Zhu XQ, Li XR, Xie MQ. Are Tritrichomonas foetus and Tritrichomonas suis synonyms? Trends Parasitol 2005; 21: 122-125. https://doi.org/10.1016/j.pt.2004.12.001
  15. Mostegl MM, Richter B, Nedorost N, Maderner A, Dinhopl N, Weissenbock H . Investigations on the prevalence and potential pathogenicity of intestinal trichomonads in pigs using in situ hybridization. Vet Parasitol 2011; 178: 58-63. https://doi.org/10.1016/j.vetpar.2010.12.022
  16. Yang CR, Meng ZD, Wang X, Li YL, Zhang YX, Zhao QP. Diarrhoea surveillance in children aged under 5 years in a rural area of Hebei Province, China. J Diarrhoeal Dis Res 1990; 8: 155-159.
  17. Meloni D, Mantini C, Goustille J, Desoubeaux G, Maakaroun-Vermesse Z, Chandenier J, Gantois N, Duboucher C, Fiori PL, Dei-Cas E, Duong TH, Viscogliosi E . Molecular identification of Pentatrichomonas hominis in two patients with gastrointestinal symptoms. J Clin Pathol 2011; 64: 933-935. https://doi.org/10.1136/jcp.2011.089326
  18. Jakobsen EB, Friis-Moller A, Friis J. Trichomonas species in a subhepatic abscess. Eur J Microbiol 1987; 6: 296-297. https://doi.org/10.1007/BF02017616
  19. Jongwutiwes SU, Silachamroon U, Putaporntip C. Pentatrichomonas hominis in empyema thoracis. Trans R Soc Trop Med Hyg 2000; 94: 185-186. https://doi.org/10.1016/S0035-9203(00)90270-0
  20. Slapeta J, Craig S, McDonell D, Emery D. Tritrichomonas foetus from domestic cats and cattle are genetically distinct. Exp Parasitol 2010; 126: 209-213. https://doi.org/10.1016/j.exppara.2010.04.024
  21. Reinmann K, Muller N, Kuhnert P, Campero CM, Leitsch D, Hess M, Henning K, Fort M, Muller J, Gottstein B, Frey CF . Tritrichomonas foetus isolates from cats and cattle show minor genetic differences in unrelated loci ITS-2 and EF-$1{\alpha}$. Vet Parasitol 2012; 185: 138-144. https://doi.org/10.1016/j.vetpar.2011.09.032
  22. Chen J, Xu MJ, Zhou DH, Song HQ, Wang CR, Zhu XQ. Canine and feline parasitic zoonoses in China. Parasit Vectors 2012; 5: 152. https://doi.org/10.1186/1756-3305-5-152
  23. Gookin JL, Birkenheuer AJ, Breitschwerdt EB, Levy MG. Single-tube nested PCR for detection of Tritrichomonas foetus in feline feces. J Clin Microbiol 2002; 40: 4126-4130. https://doi.org/10.1128/JCM.40.11.4126-4130.2002
  24. Duboucher C, Caby S, Dufernez F, Chabe M, Gantois N, Delgado-Viscogliosi P, Billy C, Barre E, Torabi E, Capron M, Pierce RJ, Dei-Cas E, Viscogliosi E. Molecular identification of Tritrichomonas foetus-like organisms as coinfecting agents of human Pneumocystis pneumonia. J Clin Microbiol 2006; 44: 1165-1168. https://doi.org/10.1128/JCM.44.3.1165-1168.2006
  25. Cobo ER, Campero CM, Mariante RM, Benchimol M. Ultrastructural study of a tetratrichomonad species isolated from prepucial smegma of virgin bulls. Vet Parasitol 2003; 117: 195-211. https://doi.org/10.1016/j.vetpar.2003.07.026
  26. Walker RL, Hayes DC, Sawyer SJ, Nordhausen RW, Van Hoosear KA, Bon-Durant RH. Comparison of the 5.8 S rRNA gene and internal transcribed spacer regions of trichomonadid protozoa recovered from the bovine preputial cavity. J Vet Diagn Invest 2003; 15: 14-20. https://doi.org/10.1177/104063870301500104
  27. Kleina P, Bettim-Bandinelli J, Bonatto SL, Benchimol M, Bogo MR. Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8S rRNA and ITS-2 sequences. Int J Parasitol 2004; 34: 963-970. https://doi.org/10.1016/j.ijpara.2004.04.004
  28. Grabensteiner E, Bilic I, Kolbe T, Hess M. Molecular analysis of clonal trichomonad isolates indicate the existence of heterogenic species present in different birds and within the same host. Vet Parasitol 2010; 172: 53-64. https://doi.org/10.1016/j.vetpar.2010.04.015
  29. Malik SB, Brochu CD, Bilic I, Yuan J, Hess M, Logsdon JM Jr, Carlton JM. Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers vs. Rpb1, a single-copy gene. PLoS ONE 2011; 6, e20774. https://doi.org/10.1371/journal.pone.0020774
  30. Gookin JL, Copple CN, Papich MG, Poore MF, Stauffer SH, Birkenheuer AJ, Twedt DC, Levy MG. Efficacy of ronidazole for treatment of feline Tritrichomonas foetus infection. J Vet Intern Med 2006; 20: 536-543. https://doi.org/10.1111/j.1939-1676.2006.tb02893.x
  31. Profizi C, Cian A, Meloni D, Hugonnard M, Lambert V, Groud K, Gagnon AC, Viscogliosi E, Zenner L. Prevalence of Tritrichomonas foetus infections in French catteries. Vet Parasitol 2013; 196: 50-55. https://doi.org/10.1016/j.vetpar.2013.01.021

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