Torque Teno Sus Virus: History
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Subjects: Virology | Veterinary Sciences
Contributor:
Sara Arnaboldi

Torque teno sus virus (TTSuV) belongs to the Anelloviridae family. TTSuV is a non-enveloped circular ssDNA virus which frequently infects swine and has been associated with hepatic, respiratory, and autoimmune disorders. TTSuV pathogenic role is still uncertain, and clear data in the literature on virus reservoirs are lacking.

  • swine-related virus
  • wild ungulates
  • reservoir
Torque teno viruses (TTVs) belong to the Anelloviridae family and are widespread worldwide in humans and animals [1][2]. TTVs were isolated for the first time in humans in 1997 in a patient with post-transfusional hepatitis of unknown etiology [3]. Human infection has been associated with respiratory diseases, acute enteritis, viral hepatitis, and autoimmune rheumatic diseases [4][5][6][7]. Their pathological mechanisms are still unclear, but recent studies suggested an interaction with the host immune system. Moreover, in the case of co-infection with other viruses an increased disease severity was reported [8].
TTVs are ubiquitous viruses and have been often detected in mammalian species, including dogs, cats, swine, cattle, sheep, wild boars, hares, and non-human primates [9][10][11][12][13][14]. TTVs are genetically distinct and are classified in a species-specific manner, although the genomes of TTVs detected from several animal species, including humans, show a similar organization [15].
In swine, Torque teno sus virus (TTSuV) has a genome organization similar to human TTV (huTTV) and comprises two genera: Iotatorquevirus, which includes TTSuV1a, and Kappatorquevirus, which includes two species (TTSuVk2a and TTSuVk2b [2][16][17][18][19]. TTSuV1a and TTSuVk2a are the most studied and well-characterized genogroups and appear to act as primary pathogens in swine, causing mild to moderate respiratory, hepatic, and nephritic lesions [15][20][21]. Recently, TTSuV co-infection with other swine-related viruses was studied, and it was demonstrated that the association of TTSuV with Porcine circovirus type 2 can enhance disease severity [22].
TTSuVs are mainly transmitted by the fecal–route, and they are frequently detected in fecal excretions as well as nasal excretions, sera, and several organs including the liver of infected pigs [23]. The virus transmission may also occur by a vertical route, as fetuses infected with TTSuV have been found at different stages of pregnancy [24][25].
TTSuV is widespread in Europe in both swine and wild boars, as reported by different studies: TTSuV was found in Romania and in Germany, while a high sero-prevalence (84%) was found among wild boars in Spain [12][26][27]. In Italy, previous studies reported a prevalence of 83.2% in sera of pigs at different ages, as well as a prevalence of 58.3% in fresh pork liver sausages [28][29][30]. Moreover, a recent study investigated the role of wild animals as TTSuV reservoirs in Northern Italy. TTSuV prevalence in wild boars was as high as 4.5%, while in wild ruminants a prevalence of 9.4% was reported [31], highlighting the need for monitoring studies in wild populations to improve the knowledge of emerging viruses and to better evaluate their likely zoonotic potential. In fact, wild animals could be putative reservoirs that may contribute, to varying degrees, to the spread and amplification of viruses, possibly including those initially originated on farms, to other farms with eventual transmission to humans. The public health significance of TTSuVs as potentially zoonotic swine viruses must be evaluated, considering that modern human lifestyle, which is characterized by growing populations, high density rates, and global movements, leads to the increase in new risks for human and animal health.

This entry is adapted from the peer-reviewed paper 10.3390/microorganisms10020242

References

  1. Gallian, P.; Biagini, P.; Zhong, S.; Touinssi, M.; Yeo, W.; Cantaloube, J.F.; Attoui, H.; de Micco, P.; Johnson, P.J.; de Lamballerie, X. TT Virus: A Study of Molecular Epidemiology and Transmission of Genotypes 1, 2 and 3. J. Clin. Virol. 2000, 17, 43–49.
  2. International Committee on Taxonomy of Viruses. Available online: https://talk.ictvonline.org/ictv-reports/ictv_9th_report/ssdna-viruses-2011/w/ssdna_viruses/139/anelloviridae (accessed on 4 December 2021).
  3. Nishizawa, T.; Okamoto, H.; Konishi, K.; Yoshizawa, H.; Miyakawa, Y.; Mayumi, M. A Novel DNA Virus (TTV) Associated with Elevated Transaminase Levels in Posttransfusion Hepatitis of Unknown Etiology. Biochem. Biophys. Res. Commun. 1997, 241, 92–97.
  4. Prasetyo, A.A.; Desyardi, M.N.; Tanamas, J.; Suradi; Reviono; Harsini; Kageyama, S.; Chikumi, H.; Shimizu, E. Respiratory Viruses and Torque Teno Virus in Adults with Acute Respiratory Infections. Intervirology 2015, 58, 57–68.
  5. Brassard, J.; Gagné, M.-J.; Leblanc, D.; Poitras, É.; Houde, A.; Boras, V.F.; Inglis, G.D. Association of Age and Gender with Torque Teno Virus Detection in Stools from Diarrheic and Non-Diarrheic People. J. Clin. Virol. 2015, 72, 55–59.
  6. Kasirga, E.; Sanlidag, T.; Akcali, S.; Keskin, S.; Aktas, E.; Karakoç, Z.; Helvaci, M.; Sözen, G.; Kuzu, M. Clinical Significance of TT Virus Infection in Children with Chronic Hepatitis B. Pediatrics Int. Off. J. Jpn. Pediatric Society 2005, 47, 300–304.
  7. Gergely, P.; Perl, A.; Poór, G. Possible Pathogenic Nature of the Recently Discovered TT Virus: Does It Play a Role in Autoimmune Rheumatic Diseases? Autoimmun. Rev. 2006, 6, 5–9.
  8. Spandole, S.; Cimponeriu, D.; Berca, L.M.; Mihăescu, G. Human Anelloviruses: An Update of Molecular, Epidemiological and Clinical Aspects. Arch. Virol. 2015, 160, 893–908.
  9. Leary, T.P.; Erker, J.C.; Chalmers, M.L.; Desai, S.M.; Mushahwar, I.K. Improved Detection Systems for TT Virus Reveal High Prevalence in Humans, Non-Human Primates and Farm Animals. J. Gen. Virol. 1999, 80(Pt. 8), 2115–2120.
  10. Cong, M.; Nichols, B.; Dou, X.; Spelbring, J.E.; Krawczynski, K.; Fields, H.A.; Khudyakov, Y.E. Related TT Viruses in Chimpanzees. Virology 2000, 274, 343–355.
  11. Okamoto, H.; Takahashi, M.; Nishizawa, T.; Tawara, A.; Fukai, K.; Muramatsu, U.; Naito, Y.; Yoshikawa, A. Genomic Characterization of TT Viruses (TTVs) in Pigs, Cats and Dogs and Their Relatedness with Species-Specific TTVs in Primates and Tupaias. J. Gen. Virol. 2002, 83(Pt. 6), 1291–1297.
  12. Martínez, L.; Kekarainen, T.; Sibila, M.; Ruiz-Fons, F.; Vidal, D.; Gortázar, C.; Segalés, J. Torque Teno Virus (TTV) Is Highly Prevalent in the European Wild Boar (Sus Scrofa). Vet. Microbiol. 2006, 118, 223–229.
  13. Brassard, J.; Gagné, M.-J.; Lamoureux, L.; Inglis, G.D.; Leblanc, D.; Houde, A. Molecular Detection of Bovine and Porcine Torque Teno Virus in Plasma and Feces. Vet. Microbiol. 2008, 126, 271–276.
  14. Águeda-Pinto, A.; Kraberger, S.; Lund, M.C.; Gortázar, C.; McFadden, G.; Varsani, A.; Esteves, P.J. Coinfections of Novel Polyomavirus, Anelloviruses and a Recombinant Strain of Myxoma Virus-MYXV-Tol Identified in Iberian Hares. Viruses 2020, 12, 340.
  15. Ssemadaali, M.A.; Effertz, K.; Singh, P.; Kolyvushko, O.; Ramamoorthy, S. Identification of Heterologous Torque Teno Viruses in Humans and Swine. Sci. Rep. 2016, 6, 26655.
  16. Varsani, A.; Opriessnig, T.; Celer, V.; Maggi, F.; Okamoto, H.; Blomström, A.L.; Cadar, D.; Harrach, B.; Biagini, P.; Kraberger, S. Taxonomic update for mammalian anelloviruses (family Anelloviridae). Arch. Virol. 2021, 166, 2943–2953.
  17. Manzin, A.; Mallus, F.; Macera, L.; Maggi, F.; Blois, S. Global Impact of Torque Teno Virus Infection in Wild and Domesticated Animals. J. Infect. Dev. Ctries. 2015, 9, 562–570.
  18. Liu, J.; Guo, L.; Zhang, L.; Wei, Y.; Huang, L.; Wu, H.; Liu, C. Three New Emerging Subgroups of Torque Teno Sus Viruses (TTSuVs) and Co-Infection of TTSuVs with Porcine Circovirus Type 2 in China. Virol. J. 2013, 10, 189.
  19. Cortey, M.; Pileri, E.; Segalés, J.; Kekarainen, T. Globalisation and Global Trade Influence Molecular Viral Population Genetics of Torque Teno Sus Viruses 1 and 2 in Pigs. Vet. Microbiol. 2012, 156, 81–87.
  20. Krakowka, S.; Ellis, J.A. Evaluation of the Effects of Porcine Genogroup 1 Torque Teno Virus in Gnotobiotic Swine. Am. J. Vet. Res. 2008, 69, 1623–1629.
  21. Krakowka, S.; Hartunian, C.; Hamberg, A.; Shoup, D.; Rings, M.; Zhang, Y.; Allan, G.; Ellis, J.A. Evaluation of Induction of Porcine Dermatitis and Nephropathy Syndrome in Gnotobiotic Pigs with Negative Results for Porcine Circovirus Type 2. Am. J. Vet. Res. 2008, 69, 1615–1622.
  22. Ellis, J.A.; Allan, G.; Krakowka, S. Effect of Coinfection with Genogroup 1 Porcine Torque Teno Virus on Porcine Circovirus Type 2-Associated Postweaning Multisystemic Wasting Syndrome in Gnotobiotic Pigs. Am. J. Vet. Res. 2008, 69, 1608–1614.
  23. Li, G.; Wang, R.; Cai, Y.; Zhang, J.; Zhao, W.; Gao, Q.; Franzo, G.; Su, S. Epidemiology and Evolutionary Analysis of Torque Teno Sus Virus. Vet. Microbiol. 2020, 244, 108668.
  24. Sibila, M.; Martínez-Guinó, L.; Huerta, E.; Llorens, A.; Mora, M.; Grau-Roma, L.; Kekarainen, T.; Segalés, J. Swine Torque Teno Virus (TTV) Infection and Excretion Dynamics in Conventional Pig Farms. Vet. Microbiol. 2009, 139, 213–218.
  25. Aramouni, M.; Segalés, J.; Cortey, M.; Kekarainen, T. Age-Related Tissue Distribution of Swine Torque Teno Sus Virus 1 and 2. Vet. Microbiol. 2010, 146, 350–353.
  26. Gallei, A.; Pesch, S.; Esking, W.S.; Keller, C.; Ohlinger, V.F. Porcine Torque Teno Virus: Determination of Viral Genomic Loads by Genogroup-Specific Multiplex Rt-PCR, Detection of Frequent Multiple Infections with Genogroups 1 or 2, and Establishment of Viral Full-Length Sequences. Vet. Microbiol. 2010, 143, 202–212.
  27. Cadar, D.; Kiss, T.; Ádám, D.; Cságola, A.; Novosel, D.; Tuboly, T. Phylogeny, Spatio-Temporal Phylodynamics and Evolutionary Scenario of Torque Teno Sus Virus 1 (TTSuV1) and 2 (TTSuV2) in Wild Boars: Fast Dispersal and High Genetic Diversity. Vet. Microbiol. 2013, 166, 200–213.
  28. Blois, S.; Mallus, F.; Liciardi, M.; Pilo, C.; Camboni, T.; Macera, L.; Maggi, F.; Manzin, A. High Prevalence of Co-Infection with Multiple Torque Teno Sus Virus Species in Italian Pig Herds. PLoS ONE 2014, 9, e113720.
  29. Martelli, F.; Caprioli, A.; Di Bartolo, I.; Cibin, V.; Pezzotti, G.; Ruggeri, F.M.; Ostanello, F. Detection of Swine Torque Teno Virus in Italian Pig Herds. J. Vet. Med. B Infect. Dis. Vet. Public Health 2006, 53, 234–238.
  30. Monini, M.; Vignolo, E.; Ianiro, G.; Ostanello, F.; Ruggeri, F.M.; Di Bartolo, I. Detection of Torque Teno Sus Virus in Pork Bile and Liver Sausages. Food Environ. Virol. 2016, 8, 283–288.
  31. Francesco Righi; Sara Arnaboldi; Virginia Filipello; Giovanni Ianiro; Ilaria Di Bartolo; Stefania Calò; Silvia Bellini; Tiziana Trogu; Davide Lelli; Alessandro Bianchi; et al. Torque Teno Sus Virus (TTSuV) Prevalence in Wild Fauna of Northern Italy. Microorganisms 2022, 10, 242, 10.3390/microorganisms10020242.
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