Torque Teno Virus in Pigs - a Review

Torque Teno Virus (TTV) was first mentioned in the scientific literature in 1997 and for several years, it was thought not to cause any disease. Early work focussed on its occurrence and prevalence, writes Jackie Linden in a review for ThePigSite. However, new research offers strong evidence of a link between TTV and those most problematical of pig diseases caused by porcine circoviruses (PCVs), including PMWS.

27 October 2008

8 minute read

TTV is a member of the family, Circoviridae - the same group as chicken anaemia virus and the porcine circoviruses (PCVs) that cause immense problems to the pig industry around the world.

Kekarainen and Segalés (2008) describe TTVs as belonging to the genus, Anellovirus. They are single stranded circular DNA viruses that infect many vertebrate species. They have not been consistently linked to specific diseases.

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"Although porcine TTV is not known to be associated with any swine disease, co-infection of pigs with TTV and other known swine pathogens may result in enhanced disease."

N. E. McKeown and co-workers

Occurrence and Distribution of TTV

TTV was first isolated in 1997 from a human patient with hepatitis following a transfusion. At that time, the virus was thought to be ubiquitous but non-pathogenic.

Subsequently, viruses related to human TTV were found in a number of other other species, including pigs. The genomic characterisation of torque teno viruses was studied by Okamamoto and colleagues in Japan in 2002. Their work suggested that domestic pigs, cats and dogs were naturally infected with species-specific TTVs, each with a small genome.

Brazilian researchers identified what appeared to be different TTV genomes from humans and pigs, and two different nucleotide sequences from the pig (Niel et al., 2005). This confirmed that TTVs are species-specific and indicated that two different TTVs occur in pigs. They were subsequently distinguished as genogroups 1 and 2 by Kekarainen et al., 2007.

In 2004, McKeown and colleagues from Virginia Polytechnic Institute and State University carried out molecular characterisation of the virus in pigs. They used serum samples from 154 pigs in six different countries and found porcine TTV DNA in 66% of the samples. The number of TTV-positive samples varied between and within countries with the lowest positive percentage in Iowa, USA (33%) and the highest at 100% in Quebec and Saskatchewan in Canada. Comparing isolates, they found no relationship between the genetic make-up of the virus and its geographical source.

Researchers from Barcelona found a very high prevalence of TTV in wild boars - 84% overall, 58% for genotype 1 and 66% for genotype 2 (Martinéz et al., 2006).

Scientists at Italy's University of Bologna tested serum from 179 pigs in ten Italian herds, and found TTV in 24% of the pigs from eight of the farms (Martelli et al., 2006). Prevalence was higher in finishing herds than farrow-to-finish herds (40% versus 11%). Among the finishing herds, TTV was more prevalent in weaners (57%) than fatteners (23%). There were no links between TTV prevalence and herd size, general hygiene practices or biosecurity levels.

A paper published this year from Quebec, Canada (Brassard et al., 2008) reports the TTV virus in 91% of plasma samples and 60% of faecal samples from a single pig herd in Quebec.

It now appears that TTV may not be quite such a new entity as was first thought. This year, researchers at the University in Barcelona published the results of a retrospective study on TTV infections in pigs in Spain (Segalés et al., 2008). They found evidence of infection way back in 1985 - 14 years before it was reported in any species.

Possible Routes of Virus Transmission

In 2002, a group from Poland (Liwén et al.,) detected TTV DNA in blood serum and in several organs in human patients, including in saliva and faeces. They suggested TTV could be transmitted by sexual and faecal-oral routes.

In 2007, researchers in Barcelona were the first to identify TTV in pig semen - in 72% of samples. They found genotype 1 in 55% of samples and genotype 2 in 32% of samples. They found some associations between TTV infection and semen characteristics but no clear evidence of the virus affecting fertility. The work did provide evidence of a possible route for the transmission of the virus between pigs.

New work from Canada (Brassard et al., 2008) confirms the possibility of TTV transmission in the faeces.

Possible Crucial Role of TTV in Major Diseases in Pigs

The early reports of TTVs made no mention of related disease, describing the virus as non-pathogenic.

However, McKeown et al. (2004) concluded, "Although porcine TTV is not known to be associated with any swine disease, co-infection of pigs with TTV and other known swine pathogens may result in enhanced disease." This now appears to have been a most prophetic statement.

A possible link between TTV and other diseases was reported two years later by the group from Barcelona. Kekarainen et al. (2006) observed a higher prevalence of TTV in the serum of sows from herds affected by Post-Weaning Multisystemic Wasting Syndrome (PMWS) than non-PMWS animals (97% versus 78%). They only found this link with the TTV genotype 2, not genotype 1. The work also confirmed the high prevalence of TTV in Spanish pig herds.

The link between TTV and other diseases was confirmed in a paper by Gagnon et al. (2007) from Quebec, Canada. Their research focussed on the emergence of PCV-2b in pigs in Canada, which had caused a significant increase in the mortality rate from PMWS over the previous 2 to 3 years. They examined samples from 13 cases of PMWS that had been submitted to the provincial diagnostic lab to determine whether the rise in mortality was caused by a second pathogen exacerbating the PCV-2 infection or a new and more virulent strain of PCV2.

They found PCV-2b in all of the samples - the first time that this type had been found in North America - and swine TTV in 69% of them, leading to the possibility that both of their hypotheses were correct.

Two papers presented at the International Pig Veterinary Society (IPVS) just four months ago shed more light on TTV infection and its potential connection to PCV2 and its related diseases.

Krakowka et al. (2008) reported on disease models where sterile pigs were infected with PCV2 or TTV or both. They found that TTV could modify PCV2 and PRRSV infections in pigs.

In another IPVS report, Martin-Valls et al. reached a similar conclusion. His team found DNA from TTV extensively in the tissues of animals suffering from PMWS but not in tissues from healthy animals. This led them to suggest that a concurrent infection of TTV and PCV2 may result in PMWS.

These latest reports raise the possibility of a role of TTV in the presentation of PMWS. Although a clear link between TTV, PCV2 and PCVAD has yet to be defined, it is clear that this merits further research.

Is it possible that TTV is the missing piece of the jigsaw, and that it might hold the key to the control over one of the the most devastating diseases in the pig industry today?

References

Brassard J. et al., 2008. Molecular detection of bovine and porcine Torque teno virus in plasma and faeces. Veterinary Microbiology, 126: 271-276
Gagnon C.A. et al., 2007. The emergence of porcine circovirus 2b genotype (PCV-2b) in swine in Canada. Canadian Veterinary Journal, 48: 811-819
Kekarainen T. and J. Segalés, 2008. Torque teno virus infection in the pig and its potential role as a model if human infection. Vet. J. [in press]
Kekarainen T. et al., 2006. Prevalence of swine torque teno virus in post-weaning multisystemic wasting syndrome (PMWS)-affected and non-PMWS-affected pigs in Spain. J. Gen. Virol., 87: 833-837
Kekarainen T. et al., 2007. Detection of swine torque teno virus genogroups 1 and 2 in boar sera and semen. Theriogenology, 68: 966-971
Krakowka S. et al., 2008. Porcine genogroup 1 torque teno virus (G1-TTV) potentiates both PCV2 and PRRSV infections in gnotobiotic swine. Proceedings of the 20th IPVS Congress 2008, 99.
Liwén I. et al., 2002. (TT virus - characteristics, occurrence and routes of transmission.) Przegl Epidemiol. 56:91-99
Martelli F. et al., 2006. Detection if swine torque teno virus in Italian pig hers. J. Vet. Med. B Infect. Dis. Vet. Public Health, 53: 234-238
Martin-Valls G. et al., 2008. Torque teno virus tissue distribution in healthy, postweaning multisystemic wasting syndrome and porcine dermatitis and nephropathy syndrome affected pigs by is situ hybridization. Proceedings of the 20th IPVS Congress 2008, 96
Martínez L. et al., 2006. Torque teno virus (TTV) is a highly prevalent in the European wild boar (Sus scrofa). Veterinary Microbiology, 118: 223-229
McKeown N.E. et al., 2004. Molecular characterisation of porcine TT virus, an orphan virus, in pigs form six different countries. Vet. Microbiol., 104: 113-117
Niel C. et al., 2005. Rolling-circle amplification of torque teno virus (TTV) complete genomes from human and swine sera and identification of a novel swine TTV genotype. J. Gen. Virol., 86: 1343-1347
Okamoto H. et al., 2002. Genomic characterization of TT viruses (TTVs) in pigs, cats, dogs and their relatedness with species-specific TTVs in primates and tupaias. J. Gen. Virol., 83: 1291-1297
Segalés, J. et al., 2008. Retrospective study on swine torque teno virus genogroups 1 and 2 infection from 1985 to 2005 in Spain. Vet. Microbiol., [in press]