Evaluation of population immunity against classical swine fever under endemic disease conditions in Cuba
Main Article Content
Abstract
Classical swine fever (CSF), or hog cholera, is a highly contagious multisystemic viral disease that is notifiable to the World Organization for Animal Health (WOAH) because of the threat of its transboundary spread. It exclusively affects domestic and wild swine, with heterogeneous clinical and lesional signs, depending on host, virus and environmental factors, which complicate its epidemiological behavior. The prolonged endemism of the disease in Cuba and the systematic application of a live vaccine, modified from the Chinese Strain (produced by LABIOFAM), have led to positive selection processes on the circulating strains, which explain their classification in a new genotype 1.4 and the appearance of moderate to low virulence strains, which have aggravated the clinical suspicion of the cases. In addition, there is the presence of persistently infected pigs (pre- and postnatally), which do not respond to vaccination and constantly shed virus into the environment. In this scenario, the serological profile of pig populations from technified and semi-technified farms, with different productive system (closed and open cycle, and both combined), systematically subjected to vaccination was characterized in one province. Antibody detection against CSFV was carried out by ELISA (Enzyme-Linked Immunoabsorbent Assay) (ELISA CSFV Ab Test IDEXX 99-43220). There was a low level of population immunity in the territory with only 52.4 % of positive animals out of 7502 pigs tested. Pigs for reproductive replacement in genetic farms showed the highest percentage (79.27 %), even with respect to their progenitors. Fattener groups showed a lower frequency of positive animals compared to breeders, and in general, it was higher in technified farms (57.97 %) compared to semi-technified farms (45.1 %). Closed cycle farms showed a lower frequency of positive animals (48.2 %) compared to open and combined cycle farms. Pigs under semi-technified production conditions showed only 42.66 % of positive animals and there were differences depending on the farms of origin. These results may be associated both to the presence of unprotected animals due to vaccine failure at vaccination (33 ±3 days of age) in the presence of high maternal antibody titers, and to a high percentage of pre- or postnatally infected pigs that are immunotolerant and do not respond to the vaccine. These conditions favor CSF endemism in that territory and require the review of the strategies used to control the disease. An analysis of these results 10 years after this research was carried out is highlighted.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
National Center for Animal and Plant Health (CENSA)References
Moennig V, Floegel-Niesmann G, Greiser-Wilke I. Clinical signs and epidemiology of classical swine fever: a review of new knowledge. Vet J. 2003; 165:11-20. DOI:10.1016/S1090-0233(02)00112-0
Tarradas J, de la Torre ME, Rosell R, Perez LJ, Pujols J, Muñoz M, Muñoz I, Muñoz S, Abad X, Domingo M, Fraile L, Ganges L. The impact of CSFV on the immune response to control infection. Virus Res. 2014;185, 82-91.
Blome S, Staubach C, Henke H, Carlson J, Beer M. Classical Swine Fever-An Updated Review. Viruses. 2017; 9, 86. doi:10.3390/v9040086
van Oirschot JT. Vaccinology of classical swine fever: from lab to field. Veterinary Microbiology. 2003;96(4,7):367-384
Greiser-Wilke I, Moennig V. Vaccination against classical swine fever virus: limitations and new strategies. Anim. Hlth. Res. Rev. 2004;5:223-226.
Graham SP, Haines FJ, Johns HL, Sosan O, La Rocca SA, Lamp B, Rümenapf T, et al. Characterisation of vaccine-induced, broadly cross-reactive IFN- secreting T cell responses that correlate with rapid protection against classical swine fever virus. Vaccine. 2012;30:2742-2748.
Frías Lepoureau MT. Reemergence of Classical Swine Fever in Cuba 1993-1997. Rev Salud Anim. 2003;25(1):1-4.
Pinto Cortés J. Plan Continental para la Erradicación de la Peste Porcina Clásica de las Américas. Oficina Regional de la FAO para América Latina y el Caribe. Boletín Nº4. 2013; Octubre - Diciembre.
IMV-CENSA. Estrategia de erradicación por zonas de la peste porcina clásica en Cuba. Instituto de Medicina Veterinaria-Centro Nacional de Sanidad Agropecuaria. Informe de trabajo. 2002.
ONEI. Anuario estadístico de Cuba. Capítulo 1: Territorio. Oficina Nacional de Estadística e Información. República de Cuba. 2012. Disponible en: http://www.one.cu (Consultado: 10/12/2015).
(FAO, 2010): http://www.fao.org/docs/eims/upload/214190/ProductionSystemsCharacteristics.pdf
ArcGIS, E. 2011. Release 10.2. Redlands (CA): ESRI.
Corp, I. 2012. IBM SPSS Statistics for Windows, Version 21.0.0.0, IBM Corp Armonk, NY.
Van Bekkum JG. Experience in the Netherlands with the lapinized so-called Chinese (C) strain of vaccine. In Hog cholera/classical swine fever and african swine fever. Commission of the European Communities, Brussels. 1977:379-391.
Percedo MI, Alfonso P, Frías MT, Díaz de Arce H, Barrera M, Fonseca O, et al. Humoral response to different vaccination schemes against classical swine fever (CSF) successively applied during an outbreak of the disease. Rev Salud Anim. 2009;31:158-163.
Fonseca O, Domínguez P, Ferrer E, Fernández O, Castell S, Frías MT, et al. Respuesta humoral a dos inmunógenos contra la peste porcina clásica en condiciones de campo. Rev. Salud Anim. 2013;35(1).
Instituto de Medicina Veterinaria (IMV). Programa Nacional para la Prevención y control de la peste porcina clásica en Cuba. 2005. Documento de trabajo.
Rivera H, Angeles R, Sandoval N, Manchego A. Persistencia del virus del cólera porcino de baja virulencia en el sistema nervioso central de lechones de granjas tecnificadas. Revista de Investigaciones Veterinarias del Perú. 1999;10(1).
Coronado L, Ríos L, Frías MT, Amarán L, Naranjo P, Percedo MI, et al. Positive selection pressure on E2 protein of classical swine fever virus drives variations in virulence, pathogenesis and antigenicity: Implication for epidemiological surveillance in endemic areas. Transbound Emerg Dis. 2019;00:1-21. DOI:10.1111/tbed.13293
Elbers ARW, Stegeman A, Moser H, Ekker HM, Smak JA, Pluimers FH. The classical swine fever epidemic 1997-1998 in the Netherlands: descriptive epidemiology. Prev. Vet Med. 1999;42(3-4):157-184. DOI:10.1016/S0167-5877(99)00074-4
Elbers ARW, Bouma A, Stegeman JA. Quantitative assessment of clinical signs for the detection of classical swine fever outbreaks during an epidemic. Vet Microbiol. 2002;85:323-332.
SongJ-Y, Lim SI, Jeoung HY, Choi E-J, Hyun B-H, Kim B, et al. Prevalence of classical swine fever virus in domestic pigs in South Korea: 1999-2011. Transbound Emerg Dis. 2013; 60:546-551. DOI:10.1111/j.1865-1682.2012.01371.x
Suradhat S, Damrongwatanapokin S, Thanawongnuwech R. Factors critical for successful vaccination against classical swine fever in endemic areas. Veterinary Microbiology. 2007;(119):1-9.
Terpstra C, Wensvoort G. Influence of the vaccination regime on the herd immune response for swine fever. Vet. Microbiol. 1987;13:143-151.
Suradhat S, Damrongwatanapokin S. Factors that influenced an effectiveness of classical swine fever vaccine: a case study. Thai. J. Vet. Med. 2002;32(Suppl):163-172 (English abstract).
Suradhat S, Damrongwatanapokin S. The influence of maternal immunity on the efficacy of a classical swine fever vaccine against classical swine fever virus, genogroup 2.2, infection. Veterinary Microbiology. 2003;92(1-2):187-194. DOI:10.1016/S0378-1135(02)00357-7
Morilla González A, Carvajal Velásquez MA. La Fiebre Porcina Clásica endémica en México. Ciencia Veterinaria. 2003:165-190.
Instituto de Medicina Veterinaria (IMV). Informe anual de las actividades veterinarias y los programas de control y prevención. Informe de trabajo.
Qiu H, Shen R, Tong G. The Lapinized Chinese Strain Vaccine Against Classical Swine Fever Virus: A Retrospective Review Spanning Half A Century. Agricultural Sciences in China. 2006;5(1)1-14DOI:10.1016/s1671-2927(06)60013-
Suradhat S, Damrongwatanapokin S, Thanawongnuwech R. Factors critical for successful vaccination against classical swine fever in endemic areas. Veterinary Microbiology. 2007;(119):1-9. DOI:10.1016/j.vetmic.2006.10.003
Fonseca O, Percedo MI, Rutili D, Alfonso P, Conte A, Ferrer E, et al. Simulation model for assessing the risk of Classical Swine Fever spreading in Pinar del Río province, Cuba. 2nd Int. Conf. on Animal Health Surveillance (ICAHS2), Havana (Cuba),2014,7-9 May.
Fonseca O, Grisi-Filho JHH, Santoro KR, Alfonso P, Abeledo MA, Fernández O, et al. Network analysis of pig industry in a proposed zone for Classical Swine Fever eradication in Cuba. OIE Global Conf. on Biol. Threat Reduction. Paris, 2015a,30 June-2 July.
Fonseca O, Percedo MI, Grisi-Filho JH, Alfonso P, Abeledo MA, Fernández O, et al. Network analysis applied to classical swine fever epidemiology in Cuba. Int. Cong Eur. Soc. of Vet. Virol. (ESVV). Montpellier (France), 2015b, 31Aug-03 Sept.
Fonseca O, Santoro K, Alfonso P, Abeledo M, Fernández O, Blanco M, et al. Spatial analysis of Classical Swine Fever outbreaks in Pinar del Río province, Cuba. 14th Int Symp on Vet Epidemiol Econ (ISVEE14), Merida, Yucatan (Mexico), 2015c, 3-7 Nov.
Fonseca O, Santoro KR, Abeledo MA, Capdevila Y, Fernández O, Alfonso P, et al. Spatiotemporal distribution of classical swine fever in Cuba, 2007-2013. Rev Salud Anim. 2016;38(1):30-38.
Fonseca O, Coronado L, Amarán L, Perera CL, Centelles Y, Montano DN, et al. Descriptive epidemiology of endemic Classical Swine Fever in Cuba. Spanish Journal of Agricultural Research. 2018;16(2). DOI:10.5424/sjar/2018162-12487
Fonseca O. Caracterización espaciotemporal y factores de riesgo del comportamiento endémico de la peste porcina clásica en Cuba. (Doctoral Thesis(, Agricultural University of Havana, 2016, Cuba.
Coronado L, Bohórquez JA, Muñoz-González S, Perez LJ, Rosell R, Fonseca O, et al. Investigation of chronic and persistent classical swine fever infections under field conditions and their impact on vaccine efficacy. BMC Veterinary Research. 2019;15:247. DOI:10.1186/s12917-019-1982-x
Díaz de Arce H, Ganges L, Barrera M, Naranjo D, Sobrino F, Frias M, et al. Origin and evolution of viruses causing classical swine fever in Cuba. Virus Res. 2005;112(1-2):123-131. DOI:10.1016/j. virusres. 2005.03.018
Pérez LJ, Diaz de Arce H, Perera CL, Rosell R, Frias MT, Percedo MI, et al. Positive selection pressure on the B/C domains of the E2-gene of classical swine fever virus in endemic areas under C-strain vaccination. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases.2012;12:1405-1412.
Postel A, Schmeiser S, Perera CL, Rodríguez LJP, Frias- Lepoureau MT, Becher P. Classical swine fever virus isolates from Cuba form a new subgenotype 1.4. Vet Microbiol. 2013;161(3-4):334-338. DOI:10.1016/j.vetmic.2012.07.045
Postel A, Pérez LJ, Perera CL, Schmeiser S, Meyer D, Meindl‐Boehmer A, et al. Development of a new LAMP assay for the detection of CSFV strains from Cuba: A proof‐of‐concept study. Archives of Virology. 2015;160:1435-1448.
Liess B. Persistent infections of hog cholera: a review. Prey. Vet. Med. 1984;2:109-113.
van Oirschot JT. Experimental production of congenital persistent swine fever infections. I Clinical, pathological and virological observations. Vet Microbiol. 1979;4:117-132.
Muñoz-González S, Perez-Simo M, Muñoz M, Bohorquez JA, Rosell R, Summerfield A, et al. Efficacy of a live attenuated vaccine in classical swine fever virus postnatally persistently infected pigs. Vet. Res. 2015; 46:78.
Cabezón O, Colom-Cadena A, Muñoz-Gonzalez S, Perez-Simo M, Bohorquez JA, Rosell R, et al. Post-natal persistent infection with classical swine fever virus in wild boar: A strategy for viral maintenance? Transbound. Emerg. Dis. 2017;64:651-655.
Weesendorp E, Backer J, Stegeman A, Loeffen W. Transmission of classical swine fever virus depends on the clinical course of infection which is associated with high and low levels of virus excretion. Vet. Microbiol. 2010.DOI:10.1016/j.vetmic.2010.06.032
Luo Y, Ji S, Liu Y, Le JL, Xia SL, Wang Y, et al. Isolation and characterization of a moderately virulent classical swine fever virus emerging in China. Transbound Emerg Dis. 2017;64:1848-1857.
Huang Y-L, Fei Pang V, Lin C-M, Tsai Y-C, Chia M-Y, Deng M-C, et al. Porcine circovirus type 2 (PCV2) infection decreases the efficacy of an attenuated classical swine fever virus (CSFV) vaccine. Veterinary Research. 2011;42:115. DOI:10.1186/1297-9716-42-115
Pérez LJ, Díaz de Arce H, Percedo MI, Domínguez P, Frías MT. First report of porcine circovirus type 2 infections in Cuba. Res. Vet. Sci. 2009;DOI:10.1016/j.rvsc.2009.11.014
Percedo MI, Domínguez P, Pérez LJ, Díaz de Arce H, Fonseca O, Castell S, et al. Efective humoral response to Classical Swine Fever E2-subunit marker vaccine candidate in Porcine Circovirus Type 2 naturally infected animals. Congreso de Enfermedades Emergentes y Reemergentes, CRESA, Barcelona, España, junio 2011
Pérez LJ, de AHD, Frias MT, Perera CL, Ganges L, Núñez JI. Molecular detection of torque Teno sus virus in lymphoid tissues in concomitant infections with other porcine viral pathogens. Res Vet Sci. 2011;91:e154-7. DOI:10.1016/J.RVSC.2011.02.01
Graham SP, Everett HE, Haines FJ, Johns HL, Sosan OA, Salguero FJ, et al. Challenge of pigs with classical swine fever viruses after C-strain vaccination reveals remarkably rapid protection and insights into early immunity. PLoS One. 2012;7, e29310. DOI:10.1371/journal.pone.0029310
Rios L, Coronado L, Naranjo‐Feliciano D, Martinez‐Pere O, Perera CL, Hernandez‐Alvarez L, et al. Deciphering the emergence, genetic diversity and evolution of classical swine fever virus. Scientific Reports.2017;7:17887.
Wei Ji, Dan-Dan Niu, Hong-Li Si, Nai-Zheng Ding, Cheng-Qiang He. Vaccination influences the evolution of classical swine fever virus. Infection, Genetics and Evolution. 2014;25:69-77. DOI:10.1016/j.meegid.2014.04.008
Yoo SJ, Kwon T, Kang K, Kim H, Kang SC, Richt JA, et al. Genetic evolution of classical swine fever virus under immune environments conditioned by genotype 1-based modified live virus. Transbound Emerg Dis. 2018;1-11.DOI: 10.1111/tbed.12798
Suárez M, Sordo Y, Prieto Y, Rodríguez MP, Méndez L, Rodríguez EM, et al. A single dose of the novel chimeric subunit vaccine E2‐CD154 confers early full protection against Classical Swine Fever virus. Vaccine. 2017;35:4437-4443, DOI:10.1016/j.vaccine.2017.05.028
Muñoz-González S, Sordo Y, Pérez-Simó M, Suarez M, Canturri A, Rodríguez MP, et al. Efficacy of E2 glycoprotein fused to porcine CD154 as a novel chimeric subunit vaccine to prevent classical swine fever virus vertical transmission in pregnant sows. Vet. Microbiol. 2012.DOI:10.1016/j.vetmic.2017.05.003
Sordo‐Puga Y, SuM, Vald PN, Pérez‐Pérez D, Santana‐Rodriguez E, Sardinas‐Gonzalez T, et al. Porvac® Subunit Vaccine E2‐CD154 Induces Remarkable Rapid Protection Against Classical Swine Fever Virus. Vaccines. 2021;9:167. DOI:10.3390/vaccines9020167
LozadaA, Estrada E, Diosdado F, Socci G, Carrera E, Arellano J, et al. Epidemiology of Classical Swine Fever outbreaks in the Central Partof Mexico. Resúmenes de International Pig Veterinary Soc. 2002;17:22.
Estrada Salmerón E, Diosdado Vargas F, Arriaga Ruiz E, Ávila Segura E, Hernández Carrillo A, Morilla González A. Evaluación de algunos factores que pudieron influir en el incremento de la fiebre porcina clásica en el Estado de México, México, durante 1997. Vet. Méx. 2001;32(1).