What is the importance of zoonotic trichomonads for human health?
2014; Elsevier BV; Volume: 30; Issue: 7 Linguagem: Inglês
10.1016/j.pt.2014.05.005
ISSN1471-5007
AutoresJulia M. Maritz, Kirkwood M. Land, Jane M. Carlton, Robert P. Hirt,
Tópico(s)Viral gastroenteritis research and epidemiology
Resumo•Trichomonads represent emerging species of medical and veterinary importance.•Clinical and molecular evidence suggest a zoonotic potential for trichomonads.•Close relationship between avian and human trichomonads revealed in outbreaks. Trichomonads are common parasites of many vertebrate and invertebrate species, with four species classically recognized as human parasites: Dientamoeba fragilis, Pentatrichomonas hominis, Trichomonas vaginalis, and Trichomonas tenax. The latter two species are considered human-specific; by contrast, D. fragilis and P. hominis have been isolated from domestic and farm mammals, demonstrating a wide host range and potential zoonotic origin. Several new studies have highlighted the zoonotic dimension of trichomonads. First, species typically known to infect birds and domestic mammals have been identified in human clinical samples. Second, several phylogenetic analyses have identified animal-derived trichomonads as close sister taxa of the two human-specific species. It is our opinion, therefore, that these observations prompt further investigation into the importance of zoonotic trichomonads for human health. Trichomonads are common parasites of many vertebrate and invertebrate species, with four species classically recognized as human parasites: Dientamoeba fragilis, Pentatrichomonas hominis, Trichomonas vaginalis, and Trichomonas tenax. The latter two species are considered human-specific; by contrast, D. fragilis and P. hominis have been isolated from domestic and farm mammals, demonstrating a wide host range and potential zoonotic origin. Several new studies have highlighted the zoonotic dimension of trichomonads. First, species typically known to infect birds and domestic mammals have been identified in human clinical samples. Second, several phylogenetic analyses have identified animal-derived trichomonads as close sister taxa of the two human-specific species. It is our opinion, therefore, that these observations prompt further investigation into the importance of zoonotic trichomonads for human health. Trichomonads are anaerobic, flagellated protists belonging to the large and diverse groups Trichomonadea and Tritrichomonadea of phylum Parabasalia [1Adl S.M. et al.The revised classification of eukaryotes.J. Eukaryot. Microbiol. 2012; 59: 429-493Crossref PubMed Scopus (1255) Google Scholar]. They are characterized by the presence of three to five anterior flagella, hydrogenosomes – hydrogen-producing organelles corresponding to anaerobic versions of mitochondria [2Muller M. et al.Biochemistry and evolution of anaerobic energy metabolism in eukaryotes.Microbiol. Mol. Biol. Rev. 2012; 76: 444-495Crossref PubMed Scopus (566) Google Scholar], a parabasal body (a large Golgi), and a complex cytoskeleton. A few species have been isolated from environmental samples and may represent free-living species; however, the majority of species form symbiotic interactions (see Glossary) with various animal hosts. Among the parasitic trichomonads, several species inhabit the oral, digestive, and urogenital tracts of invertebrate and vertebrate hosts, including livestock, pets, and humans. Historically, phylum Parabasalia was divided into two groups based on morphological characteristics; however, the recent inclusion of molecular data recovered six groups: Trichomonadea, Tritrichomonadea, Hypotrichomonadea, Cristamonadea, Spirotrichonymphea, and Trichonymphea [3Cepicka I. et al.Critical taxonomic revision of parabasalids with description of one new genus and three new species.Protist. 2010; 161: 400-433Crossref PubMed Scopus (117) Google Scholar]. The Trichomonadea, Tritrichomonadea, and Hypotrichomonadea are of primary concern to parasitologists; however, the evolutionary relationships within and between these groups are unclear [4Noda S. et al.Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α.PLoS ONE. 2012; 7: e29938Crossref PubMed Scopus (41) Google Scholar]. Several molecular phylogenies have attempted to resolve these evolutionary relationships using phylogenetic markers such as ribosomal RNA (rRNA) and protein coding genes (Figure 1), which give inconsistent phylogenies [4Noda S. et al.Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α.PLoS ONE. 2012; 7: e29938Crossref PubMed Scopus (41) Google Scholar, 5Malik S.B. et al.Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers vs Rpb1, a single-copy gene.PLoS ONE. 2011; 6: e20774Crossref PubMed Scopus (37) Google Scholar]. Four species of trichomonad are considered human parasites: Trichomonas vaginalis (found in the urogenital tract) [6Kissinger P. Adamski A. Trichomoniasis and HIV interactions: a review.Sex. Transm. Infect. 2013; 89: 426-433Crossref PubMed Scopus (161) Google Scholar], Trichomonas tenax (localized to the oral cavity) [7Duboucher C. et al.Salivary trichomoniasis. A case report of infestation of a submaxillary gland by Trichomonas tenax.Arch. Pathol. Lab. Med. 1995; 119: 277-279PubMed Google Scholar], and Pentatrichomonas hominis and Dientamoeba fragilis (located in the digestive tract) [8Meloni D. et al.Molecular identification of Pentatrichomonas hominis in two patients with gastrointestinal symptoms.J. Clin. Pathol. 2011; 64: 933-935Crossref PubMed Scopus (41) Google Scholar, 9Johnson E.H. et al.Emerging from obscurity: biological, clinical, and diagnostic aspects of Dientamoeba fragilis.Clin. Microbiol. Rev. 2004; 17: 553-570Crossref PubMed Scopus (139) Google Scholar]. Only one species has well-established pathogenic potential: T. vaginalis, the cause of the most prevalent non-viral sexually transmitted infection in humans, trichomoniasis [10Hobbs M.M. et al.Trichomonas vaginalis and trichomoniasis.in: Holmes K. Sexually Transmitted Diseases. 4th edn. McGraw-Hill, 2008: 771-793Google Scholar]. Only T. vaginalis and T. tenax are considered human-specific, with the former characterized by the richest, although still limited, epidemiology data [11Poole D.N. McClelland R.S. Global epidemiology of Trichomonas vaginalis.Sex. Transm. Infect. 2013; 89: 418-422Crossref PubMed Scopus (123) Google Scholar], but very little is known about the latter. P. hominis and D. fragilis can cause gastrointestinal symptoms in some patients, such as abdominal pain and diarrhea [8Meloni D. et al.Molecular identification of Pentatrichomonas hominis in two patients with gastrointestinal symptoms.J. Clin. Pathol. 2011; 64: 933-935Crossref PubMed Scopus (41) Google Scholar, 12Barratt J.L. et al.A review of Dientamoeba fragilis carriage in humans: several reasons why this organism should be considered in the diagnosis of gastrointestinal illness.Gut Microbes. 2011; 2: 3-12Crossref PubMed Scopus (106) Google Scholar], D. fragilis has also been proffered as a potential causative agent of irritable bowel syndrome (IBS) [13Hussein E.M. et al.Genetic diversity of Dientamoeba fragilis isolates of irritable bowel syndrome patients by high-resolution melting-curve (HRM) analysis.Parasitol. Res. 2009; 105: 1053-1060Crossref PubMed Scopus (26) Google Scholar, 14Stark D. et al.A review of the clinical presentation of dientamoebiasis.Am. J. Trop. Med. Hyg. 2010; 82: 614-619Crossref PubMed Scopus (99) Google Scholar], but debate surrounds its pathogenicity, infection route, and epidemiology [15Clark C.G. et al.Transmission of Dientamoeba fragilis: pinworm or cysts?.Trends Parasitol. 2014; 30: 136-140Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]. In addition, several trichomonad species are of veterinary importance, such as the avian pathogens Trichomonas gallinae, Tetratrichomonas gallinarum, and Histomonas meleagridis [16Robinson R.A. et al.Emerging infectious disease leads to rapid population declines of common British birds.PLoS ONE. 2010; 5: e12215Crossref PubMed Scopus (196) Google Scholar, 17Amin A. et al.Trichomonads in birds – a review.Parasitology. 2014; 141: 733-747Crossref PubMed Scopus (95) Google Scholar, 18Lawson B. et al.A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease.Infect. Genet. Evol. 2011; 11: 1638-1645Crossref PubMed Scopus (69) Google Scholar, 19Bilic I. et al.Multi-locus typing of Histomonas meleagridis isolates demonstrates the existence of two different genotypes.PLoS ONE. 2014; 9: e92438Crossref PubMed Scopus (35) Google Scholar], and Tritrichomonas foetus, the causative agent of a venereal disease in cattle [20Frey C.F. Muller N. Tritrichomonas–systematics of an enigmatic genus.Mol. Cell. Probes. 2012; 26: 132-136Crossref PubMed Scopus (18) Google Scholar]. This extensive host range, along with the isolation of D. fragilis [21Caccio S.M. et al.Pigs as natural hosts of Dientamoeba fragilis genotypes found in humans.Emerg. Infect. Dis. 2012; 18: 838-841Crossref PubMed Scopus (39) Google Scholar] and P. hominis [22Mostegl M.M. et al.Detection of Tritrichomonas foetus and Pentatrichomonas hominis in intestinal tissue specimens of cats by chromogenic in situ hybridization.Vet. Parasitol. 2012; 183: 209-214Crossref PubMed Scopus (19) Google Scholar] from various animal hosts, suggests that certain species of trichomonads may exhibit the characteristics of zoonoses. Although the question of zoonotic trichomonads has been considered for some years (e.g., [23Duboucher C. et al.Frequency of trichomonads as coinfecting agents in Pneumocystis pneumonia.Acta Cytol. 2005; 49: 273-277Crossref PubMed Scopus (20) Google Scholar, 24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar]), recent results from several different sources have highlighted this potential. Here we summarize the clinical and phylogenetic studies that suggest a zoonotic potential for trichomonads, discuss their implications for human health, and the next steps required for investigation into their epidemiology, pathobiology and evolution. The four trichomonad species recognized as human parasites were initially thought to be site-specific [25Duboucher C. et al.Recent advances in pulmonary trichomonosis.Trends Parasitol. 2008; 24: 201-202Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar] (Table 1). However, various clinical studies have shown that they can also be found in atypical locations. For example, T. tenax, a commensal of the human mouth found in patients with poor oral hygiene [7Duboucher C. et al.Salivary trichomoniasis. A case report of infestation of a submaxillary gland by Trichomonas tenax.Arch. Pathol. Lab. Med. 1995; 119: 277-279PubMed Google Scholar], has been identified by microscopic and molecular methods in the upper and lower respiratory tracts [26Mallat H. et al.Molecular characterization of Trichomonas tenax causing pulmonary infection.J. Clin. Microbiol. 2004; 42: 3886-3887Crossref PubMed Scopus (48) Google Scholar, 27Leterrier M. et al.Trichomonads in pleural effusion: case report, literature review and utility of PCR for species identification.New Microbiol. 2012; 35: 83-87PubMed Google Scholar]. One possibility that could account from this 'aberrant' location is inhalation of the parasite from the oral cavity into the respiratory tract. However, in some cases where T. tenax was identified in the respiratory tract, no parasites were found in the mouth [26Mallat H. et al.Molecular characterization of Trichomonas tenax causing pulmonary infection.J. Clin. Microbiol. 2004; 42: 3886-3887Crossref PubMed Scopus (48) Google Scholar]. Other human trichomonad species have also been identified in the respiratory tract including the sexually transmitted species T. vaginalis [28Duboucher C. et al.Pulmonary coinfection by Trichomonas vaginalis and Pneumocystis sp. as a novel manifestation of AIDS.Hum. Pathol. 2003; 34: 508-511Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar, 29Carter J.E. Whithaus K.C. Neonatal respiratory tract involvement by Trichomonas vaginalis: a case report and review of the literature.Am. J. Trop. Med. Hyg. 2008; 78: 17-19PubMed Google Scholar] and the gut parasite P. hominis [30Jongwutiwes S. et al.Pentatrichomonas hominis in empyema thoracis.Trans. R. Soc. Trop. Med. Hyg. 2000; 94: 185-186Abstract Full Text PDF PubMed Scopus (56) Google Scholar], which suggests that these species too can proliferate outside their usual body sites.Table 1Trichomonad species identified in clinical studiesaAbbreviations: DT, digestive tract; UGT, urogenital tract; RT, respiratory tract; ITS, internal transcribed spacer; IBS, irritable bowel syndrome; PcP, Pneumocystis pneumonia; ARDS, acute respiratory distress syndrome.SpeciesPrimary hostbThe primary host may not represent the true natural history of the species, which may have a broader host range.; infection siteHost range; infection siteDiagnostic method used to detect in other hosts or sitesClinical conditionscPulmonary infections include PcP, ARDS-associated infections, pneumonia, and can lead to empyema.RefsTrichomonas vaginalisHuman; UGTHumans; RTPCR and sequencing of the ITS1–5.8S–ITS2 rRNA regionTrichomoniasis, pulmonary infections, AIDS10Hobbs M.M. et al.Trichomonas vaginalis and trichomoniasis.in: Holmes K. Sexually Transmitted Diseases. 4th edn. McGraw-Hill, 2008: 771-793Google Scholar, 27Leterrier M. et al.Trichomonads in pleural effusion: case report, literature review and utility of PCR for species identification.New Microbiol. 2012; 35: 83-87PubMed Google Scholar, 28Duboucher C. et al.Pulmonary coinfection by Trichomonas vaginalis and Pneumocystis sp. as a novel manifestation of AIDS.Hum. Pathol. 2003; 34: 508-511Abstract Full Text Full Text PDF PubMed Scopus (38) Google ScholarTrichomonas tenaxHuman; DT and buccal cavityHumans; RTPCR and sequencing of the ITS1–5.8S–ITS2 rRNA regionSalivary trichomonosis, pulmonary infections7Duboucher C. et al.Salivary trichomoniasis. A case report of infestation of a submaxillary gland by Trichomonas tenax.Arch. Pathol. Lab. Med. 1995; 119: 277-279PubMed Google Scholar, 25Duboucher C. et al.Recent advances in pulmonary trichomonosis.Trends Parasitol. 2008; 24: 201-202Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, 26Mallat H. et al.Molecular characterization of Trichomonas tenax causing pulmonary infection.J. Clin. Microbiol. 2004; 42: 3886-3887Crossref PubMed Scopus (48) Google ScholarDientamoeba fragilisHumans; DTHumans and other mammals; DTFecal smears, PCR, and sequencing of the ITS1–5.8S–ITS2 rRNA region, 18S rRNAChronic diarrhea, IBS13Hussein E.M. et al.Genetic diversity of Dientamoeba fragilis isolates of irritable bowel syndrome patients by high-resolution melting-curve (HRM) analysis.Parasitol. Res. 2009; 105: 1053-1060Crossref PubMed Scopus (26) Google Scholar, 14Stark D. et al.A review of the clinical presentation of dientamoebiasis.Am. J. Trop. Med. Hyg. 2010; 82: 614-619Crossref PubMed Scopus (99) Google Scholar, 21Caccio S.M. et al.Pigs as natural hosts of Dientamoeba fragilis genotypes found in humans.Emerg. Infect. Dis. 2012; 18: 838-841Crossref PubMed Scopus (39) Google ScholarPentatrichomonas hominisNot known; DTHumans and other mammals; DTFecal smears, PCR, and sequencing of the ITS1–5.8S–ITS2 rRNA regionDiarrhea, pulmonary infections, rheumatoid arthritis8Meloni D. et al.Molecular identification of Pentatrichomonas hominis in two patients with gastrointestinal symptoms.J. Clin. Pathol. 2011; 64: 933-935Crossref PubMed Scopus (41) Google Scholar, 30Jongwutiwes S. et al.Pentatrichomonas hominis in empyema thoracis.Trans. R. Soc. Trop. Med. Hyg. 2000; 94: 185-186Abstract Full Text PDF PubMed Scopus (56) Google Scholar, 33Compaore C. et al.Pentatrichomonas hominis infection in rheumatoid arthritis treated with adalimumab.Rheumatology. 2013; 52: 1534-1535Crossref PubMed Scopus (17) Google ScholarTritrichomonas foetusBovine; UGT, DTHumans and other mammals; RTPCR and sequencing of the ITS1–5.8S–ITS2 rRNA region, EF-1α gene, and TR7/TR8 variable length regionPulmonary infections, AIDS20Frey C.F. Muller N. Tritrichomonas–systematics of an enigmatic genus.Mol. Cell. Probes. 2012; 26: 132-136Crossref PubMed Scopus (18) Google Scholar, 38Reinmann K. et al.Tritrichomonas foetus isolates from cats and cattle show minor genetic differences in unrelated loci ITS-2 and EF-1α.Vet. Parasitol. 2012; 185: 138-144Crossref PubMed Scopus (53) Google Scholar, 41Duboucher C. et al.Molecular identification of Tritrichomonas foetus-like organisms as coinfecting agents of human Pneumocystis pneumonia.J. Clin. Microbiol. 2006; 44: 1165-1168Crossref PubMed Scopus (52) Google ScholarTetratrichomonas gallinarumBirds; DTBirds, humans; RTPCR and sequencing of the ITS1–5.8S–ITS2 rRNA regionPulmonary infections24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar, 44Mantini C. et al.Molecular characterization of a new Tetratrichomonas species in a patient with empyema.J. Clin. Microbiol. 2009; 47: 2336-2339Crossref PubMed Scopus (31) Google ScholarTetratrichomonas sp.Not knownHumans; RTPCR and sequencing of the ITS1–5.8S–ITS2 rRNA regionPulmonary infections24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar, 43Cepicka I. et al.Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism.Vet. Parasitol. 2005; 128: 11-21Crossref PubMed Scopus (80) Google Scholara Abbreviations: DT, digestive tract; UGT, urogenital tract; RT, respiratory tract; ITS, internal transcribed spacer; IBS, irritable bowel syndrome; PcP, Pneumocystis pneumonia; ARDS, acute respiratory distress syndrome.b The primary host may not represent the true natural history of the species, which may have a broader host range.c Pulmonary infections include PcP, ARDS-associated infections, pneumonia, and can lead to empyema. Open table in a new tab At least five species of trichomonad, including P. hominis, T. tenax, T. vaginalis, T. foetus, and T. gallinarum, have been identified in the human respiratory tract and as causative agents of pulmonary trichomoniasis (Table 1). They have been found in up to 60% of patients with Pneumocystis pneumonia (PcP) and in up to 30% of patients with acute respiratory distress syndrome (ARDS) [31Duboucher C. et al.Trichomonads as superinfecting agents in Pneumocystis pneumonia and acute respiratory distress syndrome.J. Eukaryot. Microbiol. 2006; 53: S95-S97Crossref PubMed Scopus (12) Google Scholar]. Because trichomonads are microaerophilic it is unlikely that they initiate and cause these diseases themselves, but may represent secondary and opportunistic infections that could exacerbate symptoms and prolong illness [23Duboucher C. et al.Frequency of trichomonads as coinfecting agents in Pneumocystis pneumonia.Acta Cytol. 2005; 49: 273-277Crossref PubMed Scopus (20) Google Scholar]. These trichomonad respiratory infections seem to depend upon: (i) the presence of bacteria on which to feed and (ii) local anaerobic conditions caused by PcP or ARDS-associated infections [32Duboucher C. et al.Pulmonary superinfection by trichomonads in the course of acute respiratory distress syndrome.Lung. 2007; 185: 295-301Crossref PubMed Scopus (22) Google Scholar] but not necessarily upon immunosuppression, because drugs against PcP consistently cure patients of pulmonary trichomonosis and, in one study, treated ARDS patients were not found to be immunocompromised [25Duboucher C. et al.Recent advances in pulmonary trichomonosis.Trends Parasitol. 2008; 24: 201-202Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar]. Thus, the presence of an increasing number of distinct trichomonads in a broader range of clinical samples from patients with diverse diseases, such as AIDS, rheumatoid arthritis, prostate cancer, pulmonary infections (empyema and pneumonia in addition to PcP and ARDS), and digestive conditions such as diarrhea and IBS [33Compaore C. et al.Pentatrichomonas hominis infection in rheumatoid arthritis treated with adalimumab.Rheumatology. 2013; 52: 1534-1535Crossref PubMed Scopus (17) Google Scholar, 34Sutcliffe S. Sexually transmitted infections and risk of prostate cancer: review of historical and emerging hypotheses.Future Oncol. 2010; 6: 1289-1311Crossref PubMed Scopus (61) Google Scholar, 35Engsbro A.L. et al.Prevalence, incidence, and risk factors of intestinal parasites in Danish primary care patients with irritable bowel syndrome.Scand. J. Infect. Dis. 2014; 46: 204-209Crossref PubMed Scopus (28) Google Scholar], is becoming increasingly apparent. Indeed, the frequency of pulmonary trichomonosis infections may be higher than reported because transformation of parasites from the motile, pear-shaped stage to the amoeboid stage renders microscopic identification in clinical samples difficult [31Duboucher C. et al.Trichomonads as superinfecting agents in Pneumocystis pneumonia and acute respiratory distress syndrome.J. Eukaryot. Microbiol. 2006; 53: S95-S97Crossref PubMed Scopus (12) Google Scholar], highlighting the importance of molecular data to identify such infections [25Duboucher C. et al.Recent advances in pulmonary trichomonosis.Trends Parasitol. 2008; 24: 201-202Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar]. Trichomonads were thought to have strict host specificity [25Duboucher C. et al.Recent advances in pulmonary trichomonosis.Trends Parasitol. 2008; 24: 201-202Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar]; however, trichomonad parasites not previously reported as infecting humans have recently been found in human clinical samples (Table 1). For example, parasites belonging to the genus Tritrichomonas can be isolated from the reproductive tract of cattle (Tritrichomonas foetus), the nasal mucosa and intestine of pigs (Tritrichomonas suis), and the intestine of non-human primates (Tritrichomonas mobilensis) [20Frey C.F. Muller N. Tritrichomonas–systematics of an enigmatic genus.Mol. Cell. Probes. 2012; 26: 132-136Crossref PubMed Scopus (18) Google Scholar]. Another example is T. foetus, historically considered specific to cattle [25Duboucher C. et al.Recent advances in pulmonary trichomonosis.Trends Parasitol. 2008; 24: 201-202Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, 36Dufernez F. et al.Morphological and molecular identification of non-Tritrichomonas foetus trichomonad protozoa from the bovine preputial cavity.J. Eukaryot. Microbiol. 2007; 54: 161-168Crossref PubMed Scopus (34) Google Scholar]. Nonetheless, experimental cross-infections of the parasites between pigs and cattle in addition to analysis of molecular data suggest that these three species should be considered strains of the same species [20Frey C.F. Muller N. Tritrichomonas–systematics of an enigmatic genus.Mol. Cell. Probes. 2012; 26: 132-136Crossref PubMed Scopus (18) Google Scholar, 37Smejkalova P. et al.Extensive diversity of intestinal trichomonads of non-human primates.Parasitology. 2012; 139: 92-102Crossref PubMed Scopus (18) Google Scholar]. In addition, several different genotypes of T. foetus have been identified as causing diarrhea in cats in ∼12 countries [38Reinmann K. et al.Tritrichomonas foetus isolates from cats and cattle show minor genetic differences in unrelated loci ITS-2 and EF-1α.Vet. Parasitol. 2012; 185: 138-144Crossref PubMed Scopus (53) Google Scholar, 39Slapeta J. et al.Tritrichomonas foetus from domestic cats and cattle are genetically distinct.Exp. Parasitol. 2010; 126: 209-213Crossref PubMed Scopus (60) Google Scholar] and have also been isolated from dogs with diarrhea [40Gookin J.L. et al.Molecular characterization of trichomonads from feces of dogs with diarrhea.J. Parasitol. 2005; 91: 939-943Crossref PubMed Scopus (59) Google Scholar]. Moreover, in several new clinical cases, T. foetus or T. foetus-like organisms have unexpectedly been identified in the lungs of human patients [41Duboucher C. et al.Molecular identification of Tritrichomonas foetus-like organisms as coinfecting agents of human Pneumocystis pneumonia.J. Clin. Microbiol. 2006; 44: 1165-1168Crossref PubMed Scopus (52) Google Scholar]. Such findings suggest that T. foetus is a zoonotic parasite capable of colonizing an extensive range of hosts and body sites. Other examples of species of non-human trichomonads recently found to infect humans are members of the genus Tetratrichomonas, currently the largest genus in phylum Parabasalia. Tetratrichomonas species are found in the small intestine of a wide spectrum of invertebrate and vertebrate hosts, such as leeches, birds, and rodents [42Cepicka I. et al.New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas.Mol. Phylogenet. Evol. 2006; 39: 542-551Crossref PubMed Scopus (53) Google Scholar]. Indeed, some species of tetratrichomonad are known to infect a wide range of unrelated hosts, such as Tetratrichomonas prowazeki, which has been found in species of amphibians and reptiles [42Cepicka I. et al.New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas.Mol. Phylogenet. Evol. 2006; 39: 542-551Crossref PubMed Scopus (53) Google Scholar]. Another example, Tetratrichomonas gallinarum, is primarily thought of as an avian parasite of the digestive tract in domestic and wild birds [43Cepicka I. et al.Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism.Vet. Parasitol. 2005; 128: 11-21Crossref PubMed Scopus (80) Google Scholar], although its pathogenicity is not well established [17Amin A. et al.Trichomonads in birds – a review.Parasitology. 2014; 141: 733-747Crossref PubMed Scopus (95) Google Scholar]. However, several recent studies have identified Tetratrichomonas strains isolated from human lungs or the human oral cavity as T. gallinarum or T. gallinarum-like organisms [24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar, 44Mantini C. et al.Molecular characterization of a new Tetratrichomonas species in a patient with empyema.J. Clin. Microbiol. 2009; 47: 2336-2339Crossref PubMed Scopus (31) Google Scholar, 45Lopez-Escamilla E. et al.New Tetratrichomonas species in two patients with pleural empyema.J. Clin. Microbiol. 2013; 51: 3143-3146Crossref PubMed Scopus (24) Google Scholar]. Studies have also shown that genus Tetratrichomonas is much more diverse than previously thought and that T. gallinarum comprises at least three cryptic species with variable host specificity, some that represent human isolates [24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar, 43Cepicka I. et al.Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism.Vet. Parasitol. 2005; 128: 11-21Crossref PubMed Scopus (80) Google Scholar]. Notably, experiments failed to transmit two Tetratrichomonas of human origin to birds, although the authors suggest this result could be explained by either adaptation of the T. gallinarum-like trichomonads to the human host or extensive in vitro culturing, so that infection of birds was no longer biologically achievable [24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar]. Recent molecular phylogenetic analysis of trichomonads using rRNA and protein coding genes (e.g., Rpb1) has begun to answer important questions regarding trichomonad phylogeny. Rpb1 is a ubiquitous eukaryotic gene coding for the largest subunit of RNA polymerase II and is present as a single copy in many eukaryotes. A recent analysis of Rpb1 generated a fully resolved phylogeny of Trichomonadea, Tritrichomonadea, and Hypotrichomonadea, and species and isolates within these groups (Figure 2) [5Malik S.B. et al.Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers vs Rpb1, a single-copy gene.PLoS ONE. 2011; 6: e20774Crossref PubMed Scopus (37) Google Scholar]. Interestingly, the phylogeny recovered some avian isolates of Trichomonas spp. as sister taxa to T. vaginalis, and T. tenax as closely related to T. gallinae; these findings are consistent with previous phylogenies based upon rRNA and other protein coding genes [24Kutisova K. et al.Tetratrichomonads from the oral cavity and respiratory tract of humans.Parasitology. 2005; 131: 309-319Crossref PubMed Scopus (54) Google Scholar, 46Grabensteiner E. et al.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: 53-64Crossref PubMed Scopus (71) Google Scholar, 47Kleina P. et al.Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8S rRNA and ITS-2 sequences.Int. J. Parasitol. 2004; 34: 963-970Crossref PubMed Scopus (69) Google Scholar, 48Gerhold R.W. et al.Molecular characterization of the Trichomonas gallinae morphologic complex in the United States.J. Parasitol. 2008; 94: 1335-1341Crossref PubMed Scopus (92) Google Scholar]. The common ancestor to this complex is also related to the avian T. gallinarum (e.g., [42Cepicka I. et al.New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas.Mol. Phylogenet. Evol. 2006; 39: 54
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