Tritrichomonas foetus infection, a cause of chronic diarrhea in the domestic cat

Springer Science and Business Media LLC - Tập 46 - Trang 1-16 - 2015
Chaoqun Yao1,2, Liza S Köster3,2
1Department of Biomedical Sciences, Ross University School of Veterinary Medicine, Basseterre, Saint Kitts and Nevis
2One Health Center for Zoonoses and Tropical Veterinary Medicine, Ross University School of Veterinary Medicine, Basseterre, Saint Kitts and Nevis
3Department of Clinical Sciences, Ross University School of Veterinary Medicine, Basseterre, Saint Kitts And Nevis

Tóm tắt

Tritrichomonas foetus is a very intriguing trichomonad protozoan with respect to its varied choice of residence in the different host species. It is an obligate parasite of the reproductive and the gastrointestinal tract of bovine and feline host respectively, leading to trichomonosis. Bovine trichomonosis is a sexually transmitted disease whereas feline trichomonosis is a disease with a purported fecal-oral route of spread. Further, the trichomonad is a commensal in the nasal passages, stomach, cecum and colon of swine host. Advances have been exponential in understanding the trichomonad biology and specifically feline trichomonosis since late 1990s and early 2000s when T. foetus was soundly determined to be a causative agent of chronic diarrhea in the domestic cat. It is a challenging task, even for a skilled investigator not to mention the busy clinical veterinarian, to keep up with the vast volume of information. Here we comprehensively reviewed the trichomonad biology, clinical manifestations, pathogenesis, host immunity, world map of distribution, risk factors, diagnosis and treatment. Risk factors associated with T. foetus-positive status in the domestic cat include young age, purebred, history of diarrhea, co-infections with other enteral pathogens. In addition, molecular similarity of bovine and feline isolates of T. foetus in DNA sequence was concisely discussed. The data presented serve as an information source for veterinarians, and investigators who are interested in biology of T. foetus and feline trichomonosis.

Tài liệu tham khảo

Yao C (2012) Opportunistic human infections caused by Tritrichomonas species: a mini-review. Clin Microbiol Newsl 34:127–131 Yao C (2013) Diagnosis of Tritrichomonas foetus-infected bulls, an ultimate approach to eradicate bovine trichomoniasis in US cattle? J Med Microbiol 62:1–9 Gookin JL, Breitschwerdt EB, Levy MG, Gager RB, Benrud JG (1999) Diarrhea associated with trichomonosis in cats. J Am Vet Med Assoc 215:1450–1454 Levy MG, Gookin JL, Poore M, Birkenheuer AJ, Dykstra MJ, Litaker RW (2003) Tritrichomonas foetus and not Pentatrichomonas hominis is the etiologic agent of feline trichomonal diarrhea. J Parasitol 89:99–104 Kessel JF (1928) Trichomoniasis in kittens. Trans R Soc Trop Med Hyg 22:61–80 Benchimol M (2004) Trichomonads under Microscopy. Microsc Microanal 10:528–550 Lipman NS, Lampen N, Nguyen HT (1999) Identification of pseudocysts of Tritrichomonas muris in Armenian hamsters and their transmission to mice. Lab Anim Sci 49:313–315 Mariante RM, Lopes LC, Benchimol M (2004) Tritrichomonas foetus pseudocysts adhere to vaginal epithelial cells in a contact-dependent manner. Parasitol Res 92:303–312 Pereira-Neves A, Ribeiro KC, Benchimol M (2003) Pseudocysts in trichomonads–new insights. Protist 154:313–329 Gruffydd-Jones T, Addie D, Belak S, Boucraut-Baralon C, Egberink H, Frymus T, Hartmann K, Hosie MJ, Lloret A, Lutz H, Marsilio F, Möstl K, Pennisi MG, Radford AD, Thiry E, Truyen U, Horzinek MC (2013) Tritrichomoniasis in cats: ABCD guidelines on prevention and management. J Feline Med Surg 15:647–649 Lappin MR (2005) Enteric protozoal diseases. Vet Clin North Am Small Anim Pract 35:81–88 Levy MG, Gookin JL, Poore MF, Litaker RW, Dykstra M (2001) Information on parasitic gastrointestinal tract infections in cats. J Am Vet Med Assoc 218:194–195 Manning K (2010) Update on the diagnosis and management of Tritrichomonas foetus infections in cats. Top Companion Anim Med 25:145–148 Payne PA, Artzer M (2009) The biology and control of Giardia spp and Tritrichomonas foetus. Vet Clin North Am Small Anim Pract 39:993–1007 Tolbert MK, Gookin J (2009) Tritrichomonas foetus: a new agent of feline diarrhea. Compend Contin Educ Vet 31:374–381 Reinmann K, Muller N, Kuhnert P, Campero CM, Leitsch D, Hess M, Henning K, Fort M, Muller J, Gottstein B, Frey CF (2012) Tritrichomonas foetus isolates from cats and cattle show minor genetic differences in unrelated loci ITS-2 and EF-1alpha. Vet Parasitol 185:138–144 Slapeta J, Craig S, McDonell D, Emery D (2010) Tritrichomonas foetus from domestic cats and cattle are genetically distinct. Exp Parasitol 126:209–213 Slapeta J, Muller N, Stack CM, Walker G, Lew-Tabor A, Tachezy J, Frey CF (2012) Comparative analysis of Tritrichomonas foetus (Riedmuller, 1928) cat genotype, T. foetus (Riedmuller, 1928) cattle genotype and Tritrichomonas suis (Davaine, 1875) at 10 DNA loci. Int J Parasitol 42:1143–1149 Sun Z, Stack C, Slapeta J (2012) Sequence differences in the diagnostic region of the cysteine protease 8 gene of Tritrichomonas foetus parasites of cats and cattle. Vet Parasitol 186:445–449 Morin-Adeline V, Lomas R, O’Meally D, Stack C, Conesa A, Sapeta J (2014) Comparative transcriptomics reveals striking similarities between the bovine and feline isolates of Tritrichomonas foetus: consequences for in silico drug-target identification. BMC Genomics 15:955 Walden HS, Dykstra C, Dillon A, Rodning S, Givens D, Bird R, Newton J, Lindsay D (2013) A new species of Tritrichomonas (Sarcomastigophora: Trichomonida) from the domestic cat (Felis catus). Parasitol Res 112:2227–2235 Felleisen RS (1998) Comparative genetic analysis of tritrichomonadid protozoa by the random amplified polymorphic DNA technique. Parasitol Res 84:153–156 Hampl V, Pavlicek A, Flegr J (2001) Construction and bootstrap analysis of DNA fingerprinting-based phylogenetic trees with the freeware program FreeTree: application to trichomonad parasites. Int J Syst Evol Microbiol 51:731–735 Tachezy J, Tachezy R, Hampl V, Sedinova M, Vanacova S, Vrlik M, Van Ranst M, Flegr J, Kuldaa J (2002) Cattle pathogen Tritrichomonas foetus (Riedmuller, 1928) and pig commensal Tritrichomonas suis (Gruby & Delafond, 1843) belong to the same species. J Eukaryot Microbiol 49:154–163 Kleina P, Bettim-Bandinelli J, Bonatto SL, Benchimol M, Bogo MR (2004) Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8S rRNA and ITS-2 sequences. Int J Parasitol 34:963–970 Walker RL, Hayes DC, Sawyer SJ, Nordhausen RW, Van Hoosear KA, BonDurant RH (2003) Comparison of the 5.8S rRNA gene and internal transcribed spacer regions of trichomonadid protozoa recovered from the bovine preputial cavity. J Vet Diagn Invest 15:14–20 Lun ZR, Chen XG, Zhu XQ, Li XR, Xie MQ (2005) Are Tritrichomonas foetus and Tritrichomonas suis synonyms? Trends Parasitol 21:122–125 Gookin JL, Levy MG, Law JM, Papich MG, Poore MF, Breitschwerdt EB (2001) Experimental infection of cats with Tritrichomonas foetus. Am J Vet Res 62:1690–1697 Hale S, Norris JM, Slapeta J (2009) Prolonged resilience of Tritrichomonas foetus in cat faeces at ambient temperature. Vet Parasitol 166:60–65 Van der Saag M, McDonell D, Slapeta J (2011) Cat genotype Tritrichomonas foetus survives passage through the alimentary tract of two common slug species. Vet Parasitol 177:262–266 Rosypal AC, Ripley A, Stockdale Walden HD, Blagburn BL, Grant DC, Lindsay DS (2012) Survival of a feline isolate of Tritrichomonas foetus in water, cat urine, cat food and cat litter. Vet Parasitol 185:279–281 Stockdale HD, Dillon AR, Newton JC, Bird RC, Bondurant RH, Deinnocentes P, Barney S, Bulter J, Land T, Spencer JA, Lindsay DS, Blagburn BL (2008) Experimental infection of cats (Felis catus) with Tritrichomonas foetus isolated from cattle. Vet Parasitol 154:156–161 Foster DM, Gookin JL, Poore MF, Stebbins ME, Levy MG (2004) Outcome of cats with diarrhea and Tritrichomonas foetus infection. J Am Vet Med Assoc 225:888–892 Xenoulis PG, Lopinski DJ, Read SA, Suchodolski JS, Steiner JM (2013) Intestinal Tritrichomonas foetus infection in cats: a retrospective study of 104 cases. J Feline Med Surg 15:1098–1103 Kuehner KA, Marks SL, Kass PH, Sauter-Louis C, Grahn RA, Barutzki D, Hartmann K (2011) Tritrichomonas foetus infection in purebred cats in Germany: prevalence of clinical signs and the role of co-infection with other enteroparasites. J Feline Med Surg 13:251–258 Mardell EJ, Sparkes AH (2006) Chronic diarrhoea associated with Tritrichomonas foetus infection in a British cat. Vet Rec 158:765–766 Stockdale H, Rodning S, Givens M, Carpenter D, Lenz S, Spencer J, Dykstra C, Lindsay D, Blagburn B (2007) Experimental infection of cattle with a feline isolate of Tritrichomonas foetus. J Parasitol 93:1429–1434 Holliday M, Deni D, Gunn-Moore DA (2009) Tritrichomonas foetus infection in cats with diarrhoea in a rescue colony in Italy. J Feline Med Surg 11:131–134 Stockdale HD, Givens MD, Dykstra CC, Blagburn BL (2009) Tritrichomonas foetus infections in surveyed pet cats. Vet Parasitol 160:13–17 Dahlgren SS, Gjerde B, Pettersen HY (2007) First record of natural Tritrichomonas foetus infection of the feline uterus. J Small Anim Pract 48:654–657 Gray SG, Hunter SA, Stone MR, Gookin JL (2010) Assessment of reproductive tract disease in cats at risk for Tritrichomonas foetus infection. Am J Vet Res 71:76–81 Yaeger MJ, Gookin JL (2005) Histologic features associated with tritrichomonas foetus-induced colitis in domestic cats. Vet Pathol 42:797–804 Burgess DE, Knoblock KF, Daugherty T, Robertson NP (1990) Cytotoxic and hemolytic effects of Tritrichomonas foetus on mammalian cells. Infect Immun 58:3627–3632 Corbeil LB, Hodgson JL, Jones DW, Corbeil RR, Widders PR, Stephens LR (1989) Adherence of Tritrichomonas foetus to bovine vaginal epithelial cells. Infect Immun 57:2158–2165 Singh BN, Lucas JJ, Beach DH, Shin ST, Gilbert RO (1999) Adhesion of Tritrichomonas foetus to bovine vaginal epithelial cells. Infect Immun 67:3847–3854 Singh BN, Lucas JJ, Hayes GR, Kumar I, Beach DH, Frajblat M, Gilbert RO, Sommer U, Costello CE (2004) Tritrichomonas foetus induces apoptotic cell death in bovine vaginal epithelial cells. Infect Immun 72:4151–4158 Tolbert MK, Stauffer SH, Gookin JL (2013) Feline Tritrichomonas foetus adhere to intestinal epithelium by receptor-ligand-dependent mechanisms. Vet Parasitol 192:75–82 Tolbert MK, Stauffer SH, Brand MD, Gookin JL (2014) Cysteine protease activity of feline Tritrichomonas foetus promotes adhesion-dependent cytotoxicity to intestinal epithelial cells. Infect Immun 82:2851–2859 Da Rocha-Azevedo B, De Melo-Braga MB, Silva-Filho FC E (2005) Intra-strain clonal phenotypic variation of Tritrichomonas foetus is related to the cytotoxicity exerted by the parasite to cultured cells. Parasitol Res 95:106–112 Kania SA, Reed SL, Thomford JW, BonDurant RH, Hirata K, Corbeil RR, North MJ, Corbeil LB (2001) Degradation of bovine complement C3 by trichomonad extracellular proteinase. Vet Immunol Immunopathol 78:83–96 Allenspach K (2011) Clinical immunology and immunopathology of the canine and feline intestine. Vet Clin North Am Small Anim Pract 41:345–360 Stokes C, Waly N (2006) Mucosal defence along the gastrointestinal tract of cats and dogs. Vet Res 37:281–293 Aydintug MK, Leid RW, Widders PR (1990) Antibody enhances killing of Tritrichomonas foetus by the alternative bovine complement pathway. Infect Immun 58:944–948 Queen EV, Marks SL, Farver TB (2012) Prevalence of selected bacterial and parasitic agents in feces from diarrheic and healthy control cats from Northern California. J Vet Intern Med 26:54–60 Polak KC, Levy JK, Crawford PC, Leutenegger CM, Moriello KA (2014) Infectious diseases in large-scale cat hoarding investigations. Vet J 201:189–195 Szumilas M (2010) Explaining Odds Ratios. J Can Acad Child Adolesc Psychiatry 19:227–229 Gunn-Moore DA, McCann TM, Reed N, Simpson KE, Tennant B (2007) Prevalence of Tritrichomonas foetus infection in cats with diarrhoea in the UK. J Feline Med Surg 9:214–218 Profizi C, Cian A, Meloni D, Hugonnard M, Lambert V, Groud K, Gagnon AC, Viscogliosi E, Zenner L (2013) Prevalence of Tritrichomonas foetus infections in French catteries. Vet Parasitol 196:50–55 Galián M, Heusinger A, Gentil M, Müller E (2011) Tritrichomonas fetus in cats. Argos - Informativo Veterinario 134:44-45. Gookin JL, Stebbins ME, Hunt E, Burlone K, Fulton M, Hochel R, Talaat M, Poore M, Levy MG (2004) Prevalence of and risk factors for feline Tritrichomonas foetus and giardia infection. J Clin Microbiol 42:2707–2710 Hosein A, Kruth SA, Pearl DL, Richardson D, Maggs JC, Peach HA, Peregrine AS (2013) Isolation of Tritrichomonas foetus from cats sampled at a cat clinic, cat shows and a humane society in southern Ontario. J Feline Med Surg 15:706–711 Tysnes K, Gjerde B, Nodtvedt A, Skancke E (2011) A cross-sectional study of Tritrichomonas foetus infection among healthy cats at shows in Norway. Acta Vet Scand 53:39 Bissett SA, Gowan RA, O’Brien CR, Stone MR, Gookin JL (2008) Feline diarrhoea associated with Tritrichomonas cf. foetus and Giardia co-infection in an Australian cattery. Aust Vet J 86:440–443 Kingsbury DD, Marks SL, Cave NJ, Grahn RA (2010) Identification of Tritrichomonas foetus and Giardia spp. infection in pedigree show cats in New Zealand. N Z Vet J 58:6–10 Mancianti F, Nardoni S, Mugnaini L, Zambernardi L, Guerrini A, Gazzola V, Papini RA (2015) A retrospective molecular study of select intestinal protozoa in healthy pet cats from Italy. J Feline Med Surg 17:163–167 Paris J, Wills S, Balzer H-J, Shaw D, Gunn-Moore D (2014) Enteropathogen co-infection in UK cats with diarrhoea. BMC Vet Res 10:13 Colon Flush Technique [http://www.youtube.com/watch?v=JMfZ9M80V8E] Accessed 15 Jan 2015 T. foetus vs. Giardia [http://www.youtube.com/watch?v=aF06jlbcF8E] Accessed 15 Jan 2015 NC State University CVM, Submission of Samples for T. foetus PCR Testing [http://www.JodyGookin.com]. Accessed 15 Jan 2015 Gookin JL, Stone MR, Yaeger MJ, Meyerholz DK, Moisan P (2010) Fluorescence in situ hybridization for identification of Tritrichomonas foetus in formalin-fixed and paraffin-embedded histological specimens of intestinal trichomoniasis. Vet Parasitol 172:139–143 Mostegl MM, Wetscher A, Richter B, Nedorost N, Dinhopl N, Weissenbock H (2012) Detection of Tritrichomonas foetus and Pentatrichomonas hominis in intestinal tissue specimens of cats by chromogenic in situ hybridization. Vet Parasitol 183:209–214 Kulda J (1999) Trichomonads, hydrogenosomes and drug resistance. Int J Parasitol 29:199–212 Gookin JL, Riviere JE, Gilger BC, Papich MG (1999) Acute renal failure in four cats treated with paromomycin. J Am Vet Med Assoc 215:1821–1823. 1806 Kather EJ, Marks SL, Kass PH (2007) Determination of the in vitro susceptibility of feline Tritrichomonas foetus to 5 antimicrobial agents. J Vet Intern Med 21:966–970 Gookin JL, Copple CN, Papich MG, Poore MF, Stauffer SH, Birkenheuer AJ, Twedt DC, Levy MG (2006) Efficacy of ronidazole for treatment of feline Tritrichomonas foetus infection. J Vet Intern Med 20:536–543 Gookin JL, Stauffer SH, Coccaro MR, Poore MF, Levy MG, Papich MG (2007) Efficacy of tinidazole for treatment of cats experimentally infected with Tritrichomonas foetus. Am J Vet Res 68:1085–1088 Gookin JL, Stauffer SH, Dybas D, Cannon DH (2010) Documentation of in vivo and in vitro aerobic resistance of feline Tritrichomonas foetus isolates to ronidazole. J Vet Intern Med 24:1003–1007 Rosado TW, Specht A, Marks SL (2007) Neurotoxicosis in 4 cats receiving ronidazole. J Vet Intern Med 21:328–331 Lalor SL, Gunn-Moore DA (2012) Effects of concurrent ronidazole and probiotic therapy in cats with Tritrichomonas foetus-associated diarrhoea. J Feline Med Surg 14:650–658 Doi J, Hirota J, Morita A, Fukushima K, Kamijyo H, Ohta H, Yamasaki M, Takahashi T, Katakura K, Oku Y (2012) Intestinal Tritrichomonas suis (=T. foetus) infection in Japanese cats. J Vet Med Sci 74:413–417 Midlej V, Pereira-Neves A, Kist LW, Bogo MR, Benchimol M (2011) Ultrastructural features of Tritrichomonas mobilensis and comparison with Tritrichomonas foetus. Vet Parasitol 182:171–180 Bell ET, Gowan RA, Lingard AE, McCoy RJ, Slapeta J, Malik R (2010) Naturally occurring Tritrichomonas foetus infections in Australian cats: 38 cases. J Feline Med Surg 12:889–898 Bissett SA, Stone ML, Malik R, Norris JM, O’Brien C, Mansfield CS, Nicholls JM, Griffin A, Gookin JL (2009) Observed occurrence of Tritrichomonas foetus and other enteric parasites in Australian cattery and shelter cats. J Feline Med Surg 11:803–807 Steiner JM, Xenoulis PG, Read SA, Suchodolski JS, Globokar M, Huisinga E, Thuere S (2007) Identification of Tritrichomonas foetus DNA in feces from cats with diarrhea from Germany and Austria. J Vet Intern Med 21:649 Pham D (2009) Chronic intermittent diarrhea in a 14-month-old Abyssinian cat. Can Vet J 50:85–87 Galián M, Gentil M, Heusinger A, Müller E (2011) Tritrichomonas foetus as a cause of diarrhoea in cats. Tierärztliche Umschau Parasiten-Spezial 1:5-8 Castrén L, Vainio-Siukola K, Laaksonen I, Saari S (2011) Tritrichomonas foetus as a cause of feline chronic large bowel diarrhoea. Suomen Eläinlääkärilehti 117:371–378 Schrey C, Mundhenk L, Grubers A, Henning K, Frey C (2009) Tritrichomonas foetus as a cause of diarrhoea in three cats. Kleintierpraxis 54:93–96 Xenoulis PG, Saridomichelakis MN, Read SA, Suchodolski JS, Steiner JM (2010) Detection of Tritrichomonas foetus in cats in Greece. J Feline Med Surg 12:831–833 Mugnaini L, Papini R, Gorini G, Passantino A, Merildi V, Mancianti F (2012) Pattern and predictive factors of endoparasitism in cats in Central Italy. Rev Med Vet 163:89–94 van Doorn DC, de Bruin MJ, Jorritsma RA, Ploeger HW, Schoormans A (2009) Prevalence of Tritrichomonas foetus among Dutch cats. Tijdschr Diergeneeskd 134:698–700 (in Dutch) Hensinger T (2009) Trichomonas foetus. A pathogen responsible for diarrhoea in cats. Weterynaria w Praktyce 6:80–81 Lim S, Park SI, Ahn KS, Oh DS, Ryu JS, Shin SS (2010) First report of feline intestinal trichomoniasis caused by Tritrichomonas foetus in Korea. Korean J Parasitol 48:247–251 Miro G, Hernandez L, Montoya A, Arranz-Solis D, Dado D, Rojo-Montejo S, Mendoza-Ibarra JA, Ortega-Mora LM, Pedraza-Diaz S (2011) First description of naturally acquired Tritrichomonas foetus infection in a Persian cattery in Spain. Parasitol Res 109:1151–1154 Forshell U, Osterman-Lind E (2010) Chronic diarrhoea caused by Tritrichomonas foetus in the cat. Svensk Veterinärtidning 62:19–21 Frey CF, Schild M, Hemphill A, Stunzi P, Muller N, Gottstein B, Burgener IA (2009) Intestinal Tritrichomonas foetus infection in cats in Switzerland detected by in vitro cultivation and PCR. Parasitol Res 104:783–788 Burgener IA, Frey CF, Kook PH, Gottstein B (2010) Tritrichomonas foetus: a new intestinal parasite in Swiss cats. Schweiz Arch Tierheilkd 151:383–389 (in German) Gunn-Moore D, Tennant B (2007) Tritrichomonas foetus diarrhoea in cats. Vet Rec 160:850–851