Caprine Paratuberculosis Seroprevalence and Immune Response to Anti-Mycobacterium avium Subspecies paratuberculosis Vaccination on the Canary Islands, Spain
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design and Sampling
2.1.1. Animals and Farms
2.1.2. “TB-Free” Status Confirmation
2.1.3. PTB Confirmation on Herd Level
2.2. Serum Sampling
2.3. Anti-MAP Vaccine
2.4. Serological Assay
2.5. Farm Characterization
2.6. Prevalence Groups
2.7. Statistical Analysis
3. Results
3.1. First Sampling Session
3.1.1. Seroprevalence
3.1.2. Age Analysis
3.1.3. Farm Characterization
3.2. Second Sampling Session
Age Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Uzal, F.A.; Plattner, B.L.; Hostetter, J.M. Chapter 1—Alimentary System. In Jubb, Kennedy & Palmer’s Pathology of Domestic Animals: Volume 2, 6th ed.; Maxie, M.G., Ed.; W.B. Saunders: Philadelphia, PA, USA, 2016; pp. 1–257.e2. ISBN 978-0-7020-5318-4. [Google Scholar]
- Benavides, J.; González, L.; Dagleish, M.; Pérez, V. Diagnostic Pathology in Microbial Diseases of Sheep or Goats. Vet. Microbiol. 2015, 181, 15–26. [Google Scholar] [CrossRef] [PubMed]
- Windsor, P.A. Paratuberculosis in Sheep and Goats. Vet. Microbiol. 2015, 181, 161–169. [Google Scholar] [CrossRef] [PubMed]
- Jiménez-Martín, D.; García-Bocanegra, I.; Risalde, M.A.; Fernández-Molera, V.; Jiménez-Ruiz, S.; Isla, J.; Cano-Terriza, D. Epidemiology of Paratuberculosis in Sheep and Goats in Southern Spain. Prev. Vet Med. 2022, 202, 105637. [Google Scholar] [CrossRef] [PubMed]
- Idris, S.M.; Eltom, K.H.; Okuni, J.B.; Ojok, L.; Elmagzoub, W.A.; El Wahed, A.A.; Eltayeb, E.; Gameel, A.A. Paratuberculosis: The Hidden Killer of Small Ruminants. Animals 2022, 12, 12. [Google Scholar] [CrossRef]
- Barrero-Domínguez, B.; Luque, I.; Huerta, B.; Gomez-Laguna, J.; Galán-Relaño, Á.; Gómez-Gascón, L.; Sánchez, M.; Astorga, R.J. Paratuberculosis in Dairy Goat Flocks from Southern Spain: Risk Factors Associated with Seroprevalence. Vet Rec. 2019, 185, 600. [Google Scholar] [CrossRef]
- Matthews, J. Herd Health and Biosecurity. In Diseases of the Goat; John Wiley & Sons: Hoboken, NJ, USA, 2016; pp. 339–345. ISBN 9781119073543. [Google Scholar]
- Smith, M.C.; Sherman, D.M. Goat Medicine; John Wiley & Sons: Hoboken, NJ, USA, 2009; ISBN 0781796431. [Google Scholar]
- Terrestrial Animal Health Code. WOAH. Available online: https://www.woah.org/en/what-we-do/standards/codes-and-manuals/terrestrial-code-online-access/ (accessed on 21 June 2024).
- González, J.; Geijo, M.V.; García-Pariente, C.; Verna, A.; Corpa, J.M.; Reyes, L.E.; Ferreras, M.C.; Juste, R.A.; García Marín, J.F.; Pérez, V. Histopathological Classification of Lesions Associated with Natural Paratuberculosis Infection in Cattle. J. Comp. Pathol. 2005, 133, 184–196. [Google Scholar] [CrossRef]
- Bastida, F.; Juste, R.A. Paratuberculosis Control: A Review with a Focus on Vaccination. J. Immune Based Ther. Vaccines 2011, 9, 8. [Google Scholar] [CrossRef]
- Whittington, R.; Donat, K.; Weber, M.F.; Kelton, D.; Nielsen, S.S.; Eisenberg, S.; Arrigoni, N.; Juste, R.; Sáez, J.L.; Dhand, N.; et al. Control of Paratuberculosis: Who, Why and How. A Review of 48 Countries. BMC Vet Res. 2019, 15, 198. [Google Scholar] [CrossRef]
- Gilardoni, L.R.; Paolicchi, F.A.; Mundo, S.L. Diagnosis of Bovine Paratuberculosis: A Review of the Advantages and Disadvantages of Different Diagnostic Tests. Rev. Argent Microbiol. 2012, 44, 201–215. [Google Scholar]
- Corpa, J.M.; Pérez, V.; García Marín, J.F.; Sánchez, M.A. Control of Paratuberculosis (Johne’s Disease) in Goats by Vaccination of Adult Animals. Vet. Rec. 2000, 146, 195–196. [Google Scholar] [CrossRef]
- Fernández, M.; Royo, M.; Fuertes, M.; Arteche-Villasol, N.; Ferreras, M.C.; Benavides, J.; Pérez, V. Effects of Paratuberculosis Vaccination at Different Ages in a Dairy Goat Herd: A 2-Year Follow-Up. Animals 2022, 12, 3135. [Google Scholar] [CrossRef] [PubMed]
- Espinosa, J.; Fernández, M.; Royo, M.; Grau, A.; Ángel Collazos, J.; Benavides, J.; del Carmen Ferreras, M.; Mínguez, O.; Pérez, V. Influence of Vaccination against Paratuberculosis on the Diagnosis of Caprine Tuberculosis during Official Eradication Programmes in Castilla y León (Spain). Transbound. Emerg. Dis. 2020, 68, 692–703. [Google Scholar] [CrossRef] [PubMed]
- Koets, A.; Ravesloot, L.; Ruuls, R.; Dinkla, A.; Eisenberg, S.; Lievaart-Peterson, K. Effects of Age and Environment on Adaptive Immune Responses to Mycobacterium avium subsp. paratuberculosis (MAP) Vaccination in Dairy Goats in Relation to Paratuberculosis Control Strategies. Vet. Sci. 2019, 6, 62. [Google Scholar] [CrossRef]
- Corpa, J.M.; Pérez, V.; García Marín, J.F. Differences in the Immune Responses in Lambs and Kids Vaccinated Against Paratuberculosis, According to the Age of Vaccination. Vet. Microbiol. 2000, 77, 475–485. [Google Scholar] [CrossRef] [PubMed]
- Schwarz, D.G.G.; Lima, M.C.; Barros, M.; Valente, F.L.; Scatamburlo, T.M.; Rosado, N.; Oliveira, C.T.S.A.M.; Oliveira, L.L.; Moreira, M.A.S. Short Communication: Passive Shedding of Mycobacterium avium Ssp. paratuberculosis in Commercial Dairy Goats in Brazil. J. Dairy Sci. 2017, 100, 8426–8429. [Google Scholar] [CrossRef]
- El Sector de Ovino y Caprino en Cifras, © Ministerio de Agricultura, Pesca y Alimentación, NIPO: 003-22-136-X. Available online: https://www.mapa.gob.es/es/agricultura/estadisticas/indicadoreseconomicosdelsectorovinoycaprinodeleche2023_nuevasactualizaciones_tcm30-109075.pdf (accessed on 21 June 2024).
- Resultados de las Encuestas de Ganado Ovino y Caprino, © Ministerio de Agricultura, Pesca y Alimentación, NIPO: 003-22-136-X. Available online: https://www.mapa.gob.es/es/estadistica/temas/estadisticas-agrarias/ganaderia/encuestas-ganaderas/ (accessed on 21 June 2024).
- de Juan Ferré, L.; Domínguez Rodríguez, L.; Suárez Fernández, G.; Mateos García, A. Paratuberculosis Caprina: Aportaciones a Su Diagnóstico, Epidemilogía Molecular y Control; Universidad Complutense de Madrid: Madrid, Spain, 2005; ISBN 8466928529. [Google Scholar]
- Censo Ganadero, ISTAC 2023. Available online: https://www3.gobiernodecanarias.org/istac/statistical-visualizer/visualizer/data.html?resourceType=indicator&resourceId=GANADO_CAPRINO&measure=ABSOLUTE&geo=ES70#visualization/table (accessed on 21 June 2024).
- Decreto 51/2018 del 23 de Abril. Available online: https://www.gobiernodecanarias.org/boc/2018/084/001.html (accessed on 21 June 2024).
- Stefanova, E.P.; Sierra, E.; Fernández, A.; Quesada-Canales, O.; Paz-Sánchez, Y.; Colom-Rivero, A.; Espinosa de los Monteros, A.; Herráez, P.; Domínguez, L.; Bezos, J.; et al. Detection of Caprine Paratuberculosis (Johne’s Disease) in Pre- and Post-Vaccinated Herds: Morphological Diagnosis, Lesion Grading, and Bacterial Identification. Front. Vet Sci. 2024, 11, 1395928. [Google Scholar] [CrossRef]
- Stefanova, E.P.; Quesada-Canales, Ó.; Paz-Sánchez, Y.; Caballero, M.J.; Quintana-Montesdeoca, M.D.P.; Espinosa de los Monteros, A.; Rivero, M.A.; Castro, A.; Pérez, V.; Andrada, M. Morphological Assessment of Concomitant Lesions Detected in Goat Herds Naturally Infected with Paratuberculosis (Johne’s Disease). Animals 2023, 13, 1693. [Google Scholar] [CrossRef]
- Informe Semestral Para La Notificación de Las Enfermedades, Infecciones e Infestaciones de La Lista de La OIE, Segundo trimestre-2022. Organización mundial de sanidad animal (OIE) © 2023 OIE via Ministerio de Agricultura, Pesca y Alimentación. Available online: https://www.mapa.gob.es/es/ganaderia/temas/sanidad-animal-higiene-ganadera/smr_160123_terrestrial_14042023_espana_tcm30-619669.pdf (accessed on 21 June 2024).
- Falconi, C.; Oleaga, Á.; López-Olvera, J.R.; Casais, R.; Prieto, M.; Gortázar, C. Prevalence of Antibodies against Selected Agents Shared between Cantabrian Chamois (Rupicapra Pyrenaica Parva) and Domestic Goats. Eur. J. Wildl. Res. 2010, 56, 319–325. [Google Scholar] [CrossRef]
- Whittington, R.J.; Begg, D.J.; de Silva, K.; Purdie, A.C.; Dhand, N.K.; Plain, K.M. Case Definition Terminology for Paratuberculosis (Johne’s Disease). BMC Vet. Res. 2017, 13, 328. [Google Scholar] [CrossRef]
- Gaffuri, A.; Barsi, F.; Magni, E.; Bergagna, S.; Dellamaria, D.; Ricchi, M.; De Paolis, L.; Galletti, G.; Arrigoni, N.; Lorenzi, V.; et al. Paratuberculosis, Animal Welfare and Biosecurity: A Survey in 33 Northern Italy Dairy Goat Farms. Animals 2023, 13, 2346. [Google Scholar] [CrossRef]
- Whittington, R.J.; Sergeant, E. Progress towards Understanding the Spread, Detection and Control of Mycobacterium avium subsp paratuberculosis in Animal Populations. Aust. Vet. J. 2001, 79, 267–278. [Google Scholar] [CrossRef]
- Mercier, P.; Brémaud, I.; Gautier, M.P. Vaccination of Kids under One Month of Age with a Killed Vaccine and Reduction in the Frequency of Faecal Shedding of Mycobacterium avium Subspecies paratuberculosis. Small Rumin. Res. 2014, 121, 425–433. [Google Scholar] [CrossRef]
- Chaubey, K.K.; Gangwar, N.; Pawaiya, R.S.; Jatav, G.P.; Sohal, J.S.; Singh, S.V.; Singh, M.; Gupta, S.; Kumaresan, G.; Kumar, N.; et al. Evaluation of Newly Developed ‘Six Recombinant Secretary Proteins Based “Cocktail ELISA” and “Whole Cell Lysate” Based “Indigenous ELISA” and Tissue Microscopy’ with ‘Gold Standard’ Histo-Pathology for the Diagnosis of Johne’s Disease in Slaughtered Goats. Comp. Immunol. Microbiol. Infect. Dis. 2019, 66, 101338. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, S.S.; Toft, N. Ante Mortem Diagnosis of Paratuberculosis: A Review of Accuracies of ELISA, Interferon-γ Assay and Faecal Culture Techniques. Vet. Microbiol. 2008, 129, 217–235. [Google Scholar] [CrossRef]
- Agulló-Ros, I.; Andrada, M.; Pérez-Sancho, M.; Roy, Á.; Bezos, J.; Bonnet, T.; Moreno, I.; Paz-Sánchez, Y.; Domínguez, M.; Gómez-Villamandos, J.C.; et al. Effect of Heat-Inactivated Mycobacterium avium subspecies paratuberculosis (MAP) Vaccine on the Lesions and Immunopathology Developed in Target Tissues of Naturally MAP-Infected Goats. Vet. Microbiol. 2022, 273, 109543. [Google Scholar] [CrossRef] [PubMed]
- Juste, R.A.; Perez, V. Control of Paratuberculosis in Sheep and Goats. Vet. Clin. N. Am. Food Anim. Pract. 2011, 27, 127–138. [Google Scholar] [CrossRef]
- Muskens, J.; van Zijderveld, F.; Eger, A.; Bakker, D. Evaluation of the Long-term Immune Response in Cattle After Vaccination Against Paratuberculosis in Two Dutch Dairy Herds. Vet. Microbiol. 2002, 86, 269–278. [Google Scholar] [CrossRef]
Farm | 1st Sampling | 2nd Sampling | PTB Herd Confirmation | ||
---|---|---|---|---|---|
V | nV | Total | |||
Fuerteventura | 1098 | 165 | 769 | 934 | |
F1 | 36 | 36 | 34 | 70 | + |
F2 | 740 | 117 | 623 | 740 | ++ |
F3 | 80 | 12 | 68 | 80 | ++ |
F4 | 196 | - | - | - | + |
F5 | 46 | 0 | 44 | 44 | + |
Gran Canaria | 402 | 200 | 140 | 340 | |
F6 | 46 | - | - | - | + |
F7 | 43 | 30 | 12 | 42 | + |
F8 | 38 | 79 | 36 | 115 | + |
F9 | 15 | 20 | 10 | 30 | + |
F10 | 91 | 71 | 25 | 96 | + |
F11 | 19 | - | - | - | + |
F12 | 150 | 0 | 57 | 57 | ++ |
Total | 1500 | 365 | 909 | 1274 |
Farm | Apparent Seroprevalence (%) | True Seroprevalence (%) | 1st Sampling Session (Month) | Fencing (Y/N) | Altitude (m) | Mean Annual Temperature (°C) | Distance to a Main Road (km) | Ruminant Farms in the Surrounding Area (Y/N) |
---|---|---|---|---|---|---|---|---|
Group A (0–10%] | ||||||||
F3 | 2.5 | 2.3 | May | Y | <600 | 21.2 | <1 | Y |
F4 | 9.7 | 13.6 | May | Y | <600 | 21.4 | >1 | N |
F6 | 6.5 | 8.6 | October | Y | <600 | 20.4 | <1 | Y |
F8 | 2.6 | 2.6 | October | Y | <600 | 20.6 | <1 | Y |
F11 | 5.3 | 6.7 | October | Y | <600 | 20.7 | 0 | Y |
Group B (10–20%] | ||||||||
F9 | 20 | 29.7 | October | Y | >600 | 15 | 0 | N |
F10 | 12.1 | 17.3 | October | N | <600 | 20.1 | 0 | Y |
F12 | 16.7 | 24.5 | March | Y | <600 | 20.2 | Y | |
Group C > 20% | ||||||||
F1 | 61.1 | 93.9 | October | N * | <600 | 19.4 * | <1 | Y * |
F2 | 22.4 | 33.5 | June | Y * | <600 | 21.1 * | <1 | Y * |
F5 | 21.7 | 32.4 | January | Y * | <600 | 20.2 * | >1 | N * |
Farm | 1st Sampling Session | 2nd Sampling Session | ||||
---|---|---|---|---|---|---|
ELISA + (%) | p-Value 1 | V | nV | |||
ELISA + (%) | p-Value 1 | ELISA + (%) | p-Value 1 | |||
Group A (0–10%] | ||||||
F3 | 2/80; 2.5% | 0.200 | 7/12; 58.3% | 0.007 | 33/68; 48.5% | 0.001 |
F4 | 19/196; 9.7% | - | - | |||
F6 | 3/46; 6.5% | - | - | |||
F8 | 1/38; 2.6% | 70/79; 88.6% | 0/36; 0% | |||
F11 | 1/19; 5.3% | - | - | |||
Group B (10–20%] | ||||||
F9 | 3/15; 20% | 0.549 | 17/20; 85% | 0.019 | 2/10; 20% | 0.001 |
F10 | 11/91; 12.1% | 40/71; 56.3% | 19/25; 76% | |||
F12 | 25/150; 16.7% | - | 5/57; 8.8% | |||
Group C > 20% | ||||||
F1 | 22/36; 61.1% | 0.001 | 25/36; 69.4% | 0.001 | 0/34; 0% | 0.001 |
F2 | 166/740; 22.4% | 48/117; 41% | 149/623; 23.9% | |||
F5 | 10/46; 21.7% | - | 7/44; 15.9% | |||
F7 | 13/43; 30.2% | 26/30; 86.7% | 7/12; 58.3% |
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Stefanova, E.P.; Paz-Sánchez, Y.; Quesada-Canales, Ó.; Quintana-Montesdeoca, M.d.P.; Espinosa de los Monteros, A.; Ramírez, A.S.; Fernández, A.; Andrada, M. Caprine Paratuberculosis Seroprevalence and Immune Response to Anti-Mycobacterium avium Subspecies paratuberculosis Vaccination on the Canary Islands, Spain. Vet. Sci. 2024, 11, 388. https://doi.org/10.3390/vetsci11090388
Stefanova EP, Paz-Sánchez Y, Quesada-Canales Ó, Quintana-Montesdeoca MdP, Espinosa de los Monteros A, Ramírez AS, Fernández A, Andrada M. Caprine Paratuberculosis Seroprevalence and Immune Response to Anti-Mycobacterium avium Subspecies paratuberculosis Vaccination on the Canary Islands, Spain. Veterinary Sciences. 2024; 11(9):388. https://doi.org/10.3390/vetsci11090388
Chicago/Turabian StyleStefanova, Elena Plamenova, Yania Paz-Sánchez, Óscar Quesada-Canales, María del Pino Quintana-Montesdeoca, Antonio Espinosa de los Monteros, Ana Sofía Ramírez, Antonio Fernández, and Marisa Andrada. 2024. "Caprine Paratuberculosis Seroprevalence and Immune Response to Anti-Mycobacterium avium Subspecies paratuberculosis Vaccination on the Canary Islands, Spain" Veterinary Sciences 11, no. 9: 388. https://doi.org/10.3390/vetsci11090388