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Anti-influenza A virus antibodies in Tayassuidae from commercial rearing farms in Brazil

Detecção de anticorpos contra vírus influenza A em Tayassuidae de criações comerciais no Brasil

ABSTRACT:

Family Tayassuidae in the suborder Suina include two species of peccaries in Brazil: the white-lipped peccary (Tayassu pecari) and the collared peccary (Pecari tajacu). These animals share common pathogens with domestic swine (Sus scrofa); however, their role as potential carrier remains unclear. This study focused on detecting the prevalence of influenza A antibodies in Tayassu pecari and Pecari tajacu from commercial rearing farms from two states in Brazil. A set of 50 blood samples from Pecari tajacu and 55 from Tayassu pecari were analyzed using a commercial indirect ELISA in order to investigate anti influenza A antibodies. Pecari tajacu samples presented 22% (11/50) of seropositivity for the virus. Serological surveillance is an important tool to identify the presence and the spread of the influenza virus in feral pigs.

Key words:
influenza; antibodies; peccaries

RESUMO:

A família Tayassuidae pertencente a subordem Suina e compreende duas espécies presentes no Brasil: Queixada (Tayassu pecari) e o Caititu (Pecari tajacu). Ambas as espécies compartilham patógenos com o suíno doméstico (Sus scrofa), entretanto o papel destes animais como carreadores destas infecções permanece indefinido. O presente estudo teve como objetivo detectar a ocorrência de anticorpos contra vírus influenza A em amostras de soro de rebanhos comerciais de queixada e caititu, provenientes de dois estados do Brasil. Um total de 50 amostras de soro de Pecari tajacu e 55 amostras de Tayassu pecari foram testadas por meio de ELISA, sendo que 22% (11/50) das amostras de Pecari tajacu foram soropositivas para o agente. Estudos de vigilância sorológica são importantes para identificar a presença e a disseminação do vírus influenza em suínos selvagens.

Palavras-chave:
influenza; anticorpos; peccaries

White-lipped peccary and collared peccary are species of feral pigs found in ecosystems from southern North America throughout South America (SICURO & OLIVEIRA 2002SICURO F. L., OLIVEIRA L.F.B. Coexistence of peccaries and feral hogs in the Brazilian Pantanal westland: an ecomorphological view. Journal of Mammalogy, v.83, p.207-217. 2002. Available from: <Available from: https://doi.org/10.1644/1545-1542(2002)083<0207:COPAFH>2.0.CO;2 >. Accessed: Apr. 10, 2018.
https://doi.org/10.1644/1545-1542(2002)0...
). Peccaries and pigs are able to be infected by several common pathogens, once they diverged one million years ago from a common ancestor (COUTINHO et al., 2012COUTINHO T.A. et al. Characterization of Erysipelothrix rhusiopathiae isolated from Brazilian Tayassu pecari, Journal of Wildlife Diseases, v.44, p.689-692. 2012. Available from: <Available from: https://doi.org/10.1007/s11250-011-9980-4 >. Accessed: May, 25, 2018.
https://doi.org/10.1007/s11250-011-9980-...
) and previous studies detected peccaries as potential reservoirs of infectious diseases for domestic pigs and wild swine (Sus scrofa) (HERRERA et al. 2008HERRERA, H. M. et al. The role played by sympatric collared peccary (Tayassu tajacu), white-lipped peccary (Tayassu pecari), and feral pig (Sus scrofa) as maintenance hosts for Trypanosoma evansi and Trypanosoma cruzi in a sylvatic area of Brazil. Parasitology Research, v.103, n.3, p.619-624, 2008. Available from: <Available from: https://link.springer.com/article/10.1007/s00436-008-1021-5 >. Accessed: Feb. 20, 2018. doi: 10.1007/s00436-008-1021-5.
https://link.springer.com/article/10.100...
; COUTINHO et al. 2012COUTINHO T.A. et al. Characterization of Erysipelothrix rhusiopathiae isolated from Brazilian Tayassu pecari, Journal of Wildlife Diseases, v.44, p.689-692. 2012. Available from: <Available from: https://doi.org/10.1007/s11250-011-9980-4 >. Accessed: May, 25, 2018.
https://doi.org/10.1007/s11250-011-9980-...
).

Previous studies reported the presence of Porcine Circovirus, Herpesvirus, Mycoplasma hyopneumoniae and Pasteurella multocida in Pecari tajacu and Tayassu pecari populations (CASTRO et al., 2014CASTRO, A. M. M. G., et al. Swine infectious agents in Tayassu pecari and Pecari tajacu tissue samples from Brazil. Journal of Wildlife Diseases, 2014; 50: 205-209. Available from: <Available from: https://doi.org/10.7589/2013-01-021 >. Accessed: Nov. 15, 2017.
https://doi.org/10.7589/2013-01-021...
).

Influenza is a major cause of acute respiratory disease outbreaks in domestic pigs, highly contagious, affecting pigs and other species, including humans. When first introduced in the farm, the disease was described as a sudden onset, involving a large number of pigs (up to 100%) of various age groups (VANALSTINE, 2012VANALSTINE, W. G. Respiratory System. In: ZIMMERMAN, J. J. et al. Diseases of Swine, Ames, The Iowa State University Press, 2012. Cap.21, p.348-362.). Once established in the farm (endemic form), the disease usually appears in the nursery phase in unvaccinated herds, because maternal antibodies persist until the sixth week of life (JANKE, 2000JANKE, B. H. Diagnosis of swine influenza. Journal of Swine Health and Production, v.8, n.2, p.79-84, 2000.).

The enzootic circulation of virus lineages of H1N1, H1N2, and H3N2 subtypes in swine varies by continent and since 2009, includes reassortments with the pandemic H1N1 (H1N1pdm09) (VINCENT et al., 2014VINCENT, A. L. et al. Review of influenza A virus in swine worldwide: a call for increased surveillance and research. Zoonoses and Public Health, v.61, n.1, p.4-17, 2014. Available from: <Available from: https://doi.org/10.1111/zph.12049 >. Accessed: Oct. 17, 2018. doi: 10.1111/zph.120.
https://doi.org/10.1111/zph.12049...
). Besides, recently influenza virus surveillance in pigs has revealed that influenza virus transmission from humans to swine is far more frequent than swine-to-human zoonosis, and these events are the main source of new viral diversity (NELSON & VINCENT, 2015NELSON, M. I.; VINCENT, A. L. Reverse zoonosis of influenza to swine: new perspectives on the human-animal interface. Trends in Microbiology, v.23, n.3, p.142-153, 2015. Available from: <Available from: https://doi.org/10.1016/j.tim.2014.12.002 >. Accessed: Oct. 17, 2018. doi: 10.1016/j.tim.2014.12.002.
https://doi.org/10.1016/j.tim.2014.12.00...
).

Serological data from other countries in wild boars (Sus scrofa) and feral pigs identified antibodies to H3N2 and H1N1 (VICENTE et al., 2002VICENTE, J. et al. Antibodies to selected viral and bacterial pathogens in European wild boars from southcentral Spain. Journal of Wildlife Diseases, v.38, n.3, p.649-652, 2002. Available from: <Available from: https://doi.org/10.7589/0090-3558-38.3.649 >. Accessed: Apr. 20, 2018. doi: 10.7589/0090-3558-38.3.649.
https://doi.org/10.7589/0090-3558-38.3.6...
). In Brazil, wild boars samples revealed a human-like H1N2 influenza virus, with genes derived from the H1N1 pdm09 (BIONDO et al., 2014BIONDO N. et al. Genomic analysis of influenza A virus from captive wild boars in Brazil reveals a human-like H1N2 influenza virus. Veterinary Microbiology, v.168, p.34-40. 2014. Available from: <Available from: https://doi.org/10.1016/j.vetmic.2013.10.010 >. Accessed: Aug. 23, 2018. doi: 10.1016/j.vetmic.2013.10.010.
https://doi.org/10.1016/j.vetmic.2013.10...
).

The commercial swine herds are constantly investigated for influenza virus infection through passive monitoring, the same does not occur in wild boars and peccaries herds. In this scenario, the present study investigated evidence of antibodies against this virus in peccaries from commercial farms in Brazil.

In the present study blood samples were collected from adult slaughtered peccaries of semi-intensive system farms from two Brazilian States, which produced only one of studied species; i.e., there was no farm with extensive mixing between the two species. A total of 105 animals were sampled, 55 samples of Tayassu pecari were obtained on the same day on November of 2014 and 50 samples of Pecari tajacu on the same day on February of 2015. Further information about the specific locations of the herds, number of herds, ages and weight of slaughtered peccaries and herd management were not provided by the farmers.

The presence of antibodies against SIV was tested using CIVTEST SUIS INFLUENZA®, Hipra (Amer - Girona, Spain) subtype H1N1, and cross-reaction to H1N2 and H3N2 (100 % specificity, H1N1: 100%, H3N2: 87%, H1N2: 73% sensitivity).

The herd seroprevalence of influenza A virus was 10.47% (CI; 95%; 4.61-16.36). The seroprevalence regarding to the studied species, Pecari tajacu samples presented 22% (11/50) of seropositivity (CI: 95%; 10.5-33.48), while Tayassu pecari herd did not presented antibodies.

The epidemiology of influenza in pigs is a complex relationship between human, avian and swine viruses with putative genetic viral reassortments, which can create novel subtypes with pandemic potential for people and swine (VANALSTINE, 2012VANALSTINE, W. G. Respiratory System. In: ZIMMERMAN, J. J. et al. Diseases of Swine, Ames, The Iowa State University Press, 2012. Cap.21, p.348-362.).

In Brazil, influenza virus infection of pigs has been suspected since the late 1930s, but the first isolation from pigs occurred in 1974 (CUNHA et al., 1978CUNHA, R. G.; et al. Isolation of a strain of Myxovirus influenzae-A suis from swine slaughtered in Rio de Janeiro. Revista brasileira de biologia, v.38, n.1, p.13-17, 1978. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/635243 >. Accessed: Oct. 10, 2018. pmid:635243.
https://www.ncbi.nlm.nih.gov/pubmed/6352...
). The situation changed quickly after the emergence of H1N1 pdm09 in pigs in 2009 (SCHAEFER et al., 2011SCHAEFER, R., et al. Isolation and characterization of a pandemic H1N1 influenza virus in pigs in Brazil. Pesquisa Veterinária Brasileira, 31, 761-767. 2011. Available from: <Available from: https://doi.org/10.1590/S0100-736X2011000900007 >. Accessed: Jul. 11, 2018.
https://doi.org/10.1590/S0100-736X201100...
).

Since then, serological surveillance in commercial pigs became routine and Brazilian commercial herds have shown the wide circulation of this agent, presenting more than 70% of seroprevalence in almost 65% of tested herds (CIACCI-ZANELLA et al., 2015CIACCI-ZANELLA, J. R., et al. Influenza A virus infection in Brazilian swine herds following the introduction of pandemic 2009 H1N1. Veterinary Microbiology, 180, 118-122, 2015. Available from: <Available from: https://doi.org/10.1016/j.vetmic.2015.08.021 >. Accessed: Mar. 7, 2018. doi: 10.1016/j.vetmic.2015.08.021.
https://doi.org/10.1016/j.vetmic.2015.08...
) and more than 40% of seropositive sows (RAJAO et al., 2013RAJAO, D. S., et al. Serological evidence of swine influenza in Brazil. Influenza and Other Respiratory Viruses, 7, 109-112, 2013. Available from: <Available from: https://doi.org/10.1111/j.1750-2659.2012.00366.x >. Accessed: Jan. 25, 2018. doi: 10.1111/j.1750-2659.2012.00366.x.
https://doi.org/10.1111/j.1750-2659.2012...
).

Brazilian studies detected the presence of H1N1, H3N2 (BRENTANO et al., 2002BRENTANO L, et al. Levantamento soroepidemiológico para Coronavírus respiratório e da gastroenterite transmissível e dos vírus de influenza H3N2 e H1N1 em rebanhos suínos no Brasil, 2002, 6p (Comunicado Técnico 306).; RAJAO et al., 2013RAJAO, D. S., et al. Serological evidence of swine influenza in Brazil. Influenza and Other Respiratory Viruses, 7, 109-112, 2013. Available from: <Available from: https://doi.org/10.1111/j.1750-2659.2012.00366.x >. Accessed: Jan. 25, 2018. doi: 10.1111/j.1750-2659.2012.00366.x.
https://doi.org/10.1111/j.1750-2659.2012...
), H1N1 pdm09 in commercial swine herds (SCHAEFER et al., 2011SCHAEFER, R., et al. Isolation and characterization of a pandemic H1N1 influenza virus in pigs in Brazil. Pesquisa Veterinária Brasileira, 31, 761-767. 2011. Available from: <Available from: https://doi.org/10.1590/S0100-736X2011000900007 >. Accessed: Jul. 11, 2018.
https://doi.org/10.1590/S0100-736X201100...
) and recently, H1N2 in commercial herds (SCHAEFER et al, 2015SCHAEFER R, et al. A human-like H1N2 influenza virus detected during an outbreak of acute respiratory disease in swine in Brazil. Archives of Virology, v.160, p.29-38. 2015. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/25209152 >. Accessed: Jun. 1, 2018. doi: 10.1007/s00705-014-2223-z.
https://www.ncbi.nlm.nih.gov/pubmed/2520...
). In U.S., H1N1 and H1N2 viruses in swine herds, derived from human seasonal influenza A viruses and have emerged and spread across pig herds since 2005 (VINCENT et al., 2009VINCENT, A. L. et al. Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States. Virus Genes, v.39, n.2, p.176, 2009. Available from: <Available from: https://link.springer.com/article/10.1007/s11262-009-0386-6 >. Accessed: Oct. 17, 2018. doi: 10.1007/s11262-009-0386-6.
https://link.springer.com/article/10.100...
).

Regarding to peccaries surveillances, serological results revealed a naïve population before the introduction of H1N1 pdm09 (ALBUQUERQUE et al., 2010ALBUQUERQUE N.I. et al. Intensive production system of Collared peccary (Pecari tajacu) in Brazilian Amazon. Advances in Animal Biosciences, v.1, p.480-481, 2010. Available from: <Available from: https://doi.org/10.1017/S2040470010001007 >. Accessed: Nov. 10, 2017. doi: 10.1017/S2040470010001007.
https://doi.org/10.1017/S204047001000100...
; MAYOR et al., 2006MAYOR P et al. A health evaluation in a colony of captive collared peccaries (Tayassu tajacu) in the eastern Amazon. Research in Veterinary Science, v.81, p.246-253. 2006. Available from: <Available from: http://europepmc.org/abstract/MED/16487552 >. Accessed: Jan. 10, 2018. doi: 10.1016/j.rvsc.2005.12.003.
http://europepmc.org/abstract/MED/164875...
), while wild boars and feral pigs were confirmed susceptible (ROIC et al., 2012ROIC B et al. Prevalence of antibodies to selected viral pathogens in wild boars (Sus scrofa) in Croatia in 2005-2006 and 2009-2010. Journal of Wildlife Diseases, v.48, p.131-137. 2012. Available from: <Available from: https://doi.org/10.7589/0090-3558-48.1.131 >. Accessed: Mar. 1, 2018. doi: 10.7589/0090-3558-48.1.131.
https://doi.org/10.7589/0090-3558-48.1.1...
).

The semi-intensive system allows the circulation of peccaries to an open area, favoring the contact between wild boars and other animal species as avian and feral pigs beside the contact with humans, this situation brings a concern regarding the favorable conditions for virus infection or spreading and possibly an interspecies transmission as observed in previous studies between humans-wild boars (BIONDO et al., 2014BIONDO N. et al. Genomic analysis of influenza A virus from captive wild boars in Brazil reveals a human-like H1N2 influenza virus. Veterinary Microbiology, v.168, p.34-40. 2014. Available from: <Available from: https://doi.org/10.1016/j.vetmic.2013.10.010 >. Accessed: Aug. 23, 2018. doi: 10.1016/j.vetmic.2013.10.010.
https://doi.org/10.1016/j.vetmic.2013.10...
) and humans-pigs (FORGIE et al., 2011FORGIE, S. E. et al. Swine outbreak of pandemic influenza A virus on a Canadian research farm supports human-to-swine transmission. Clinical Infectious Diseases, v.52, n.1, p.10-18, 2011. Available from: <Available from: https://doi.org/10.1093/cid/ciq030 >. Accessed: Feb. 20, 2018. doi: 10.1093/cid/ciq030.
https://doi.org/10.1093/cid/ciq030...
).

In conclusion, the first detection of influenza antibodies in Pecari tajacu confirmed the virus circulation in this population, thus, from now on, the serological surveillance is required to monitor the circulation and further studies are required to understand the role of peccaries on the pathogen dissemination and on risks of reassortment events with pigs.

ACKNOWLEDGMENTS

We would like to acknowledge the financial support provided by grant 2014/13590-3, São Paulo Research Foundation (FAPESP) , and was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil - Finance code 1409232.

REFERENCES

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    » https://doi.org/10.1017/S2040470010001007
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    » https://doi.org/10.1007/s11250-011-9980-4
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  • RAJAO, D. S., et al. Serological evidence of swine influenza in Brazil. Influenza and Other Respiratory Viruses, 7, 109-112, 2013. Available from: <Available from: https://doi.org/10.1111/j.1750-2659.2012.00366.x >. Accessed: Jan. 25, 2018. doi: 10.1111/j.1750-2659.2012.00366.x.
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    » https://doi.org/10.1590/S0100-736X2011000900007
  • SCHAEFER R, et al. A human-like H1N2 influenza virus detected during an outbreak of acute respiratory disease in swine in Brazil. Archives of Virology, v.160, p.29-38. 2015. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pubmed/25209152 >. Accessed: Jun. 1, 2018. doi: 10.1007/s00705-014-2223-z.
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    » https://doi.org/10.1644/1545-1542(2002)083<0207:COPAFH>2.0.CO;2
  • VANALSTINE, W. G. Respiratory System. In: ZIMMERMAN, J. J. et al. Diseases of Swine, Ames, The Iowa State University Press, 2012. Cap.21, p.348-362.
  • VICENTE, J. et al. Antibodies to selected viral and bacterial pathogens in European wild boars from southcentral Spain. Journal of Wildlife Diseases, v.38, n.3, p.649-652, 2002. Available from: <Available from: https://doi.org/10.7589/0090-3558-38.3.649 >. Accessed: Apr. 20, 2018. doi: 10.7589/0090-3558-38.3.649.
    » https://doi.org/10.7589/0090-3558-38.3.649.» https://doi.org/10.7589/0090-3558-38.3.649
  • VINCENT, A. L. et al. Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States. Virus Genes, v.39, n.2, p.176, 2009. Available from: <Available from: https://link.springer.com/article/10.1007/s11262-009-0386-6 >. Accessed: Oct. 17, 2018. doi: 10.1007/s11262-009-0386-6.
    » https://doi.org/10.1007/s11262-009-0386-6.» https://link.springer.com/article/10.1007/s11262-009-0386-6
  • VINCENT, A. L. et al. Review of influenza A virus in swine worldwide: a call for increased surveillance and research. Zoonoses and Public Health, v.61, n.1, p.4-17, 2014. Available from: <Available from: https://doi.org/10.1111/zph.12049 >. Accessed: Oct. 17, 2018. doi: 10.1111/zph.120.
    » https://doi.org/10.1111/zph.120.» https://doi.org/10.1111/zph.12049
  • 0
    CR-2018-0694.R2
  • BIOETHICS AND BIOSSECURITY COMMITTEE APPROVAL

    The institution`s ethics committee approved this research and the certificate registered under the protocol nº 101/2015 on 4th of September of 2015.

Publication Dates

  • Publication in this collection
    2019

History

  • Received
    28 Aug 2018
  • Accepted
    11 Feb 2019
  • Reviewed
    08 Mar 2019
Universidade Federal de Santa Maria Universidade Federal de Santa Maria, Centro de Ciências Rurais , 97105-900 Santa Maria RS Brazil , Tel.: +55 55 3220-8698 , Fax: +55 55 3220-8695 - Santa Maria - RS - Brazil
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