Evaluation of Antibody Tests for Mycobacterium bovis Infection in Pigs and Deer
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals/Serum Samples
2.1.1. Farmed Deer
2.1.2. Farmed Pigs
2.1.3. Forest of Dean Wild Boar
2.1.4. Park and Wild Deer
2.1.5. TB-Free Farmed Deer
2.1.6. TB-Free Farmed Pigs
2.2. Antibody Tests
2.2.1. IDEXX ELISA
2.2.2. Comparative PPD (∆PPD) ELISA
2.2.3. Enferplex Cervid TB Assay and Enferplex Porcine TB Assay
2.2.4. DPP VetTB Lateral Flow
2.3. Statistical Analyses
3. Results
3.1. Antibody Tests Performance—Sensitivity and Specificity—In Deer and Pigs
3.2. Seroprevalence Estimates among Wild Boar within the Forest of Dean and Park/Wild Deer with No Visible Lesions of TB
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Crawshaw, T.; de la Rua-Domenech, R.; Brown, E. Recognising the gross pathology of tuberculosis in South American camelids, deer, goats, pigs and sheep. Practice 2013, 35, 490–502. [Google Scholar] [CrossRef]
- EFSA. Scientific Opinion of the Panel on Animal Health and Animal Welfare. Tuberculosis testing in deer. EFSA J. 2008, 64, 1–34. Available online: https://www.efsa.europa.eu/en/efsajournal/pub/645 (accessed on 19 February 2023).
- Cousins, D.V.; Florisson, N. A review of tests available for use in the diagnosis of tuberculosis in non-bovine species. Rev. Sci. Tech. Off. Int. Epiz. 2005, 24, 1039–1059. [Google Scholar] [CrossRef]
- Godfray, C.; Donnelley, C.; Hewinson, G.; Winter, M. Wood. 2018. Bovine TB Strategy Review: Report to the Rt. Hon. Michael Gove MP, Secretary of State, Defra. Available online: https://www.gov.uk/government/publications/a-strategy-for-achieving-bovine-tuberculosis-free-status-for-england-2018-review (accessed on 19 February 2023).
- Gowtage-Sequeira, S.; Paterson, A.; Lyashchenko, K.P.; Lesellier, S.; Chambers, M.A. Evaluation of the CervidTB STAT-PAK for the detection of Mycobacterium bovis infection in wild deer in Great Britain. Clin. Vaccine Immunol. 2009, 16, 1449–1452. [Google Scholar] [CrossRef] [Green Version]
- Waters, W.R.; Stevens, G.E.; Schoenbaum, M.A.; Orloski, K.A.; Robbe-Austerman, S.; Harris, N.B.; Hall, S.M.; Thomsen, B.V.; Wilson, A.J.; Brannian, R.E.; et al. Bovine tuberculosis in a Nebraska herd of farmed elk and fallow deer: A failure of the tuberculin skin test and opportunities for serodiagnosis. Vet. Med. Int. 2011, 2011, 953985. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nelson, J.T.; Orloski, K.A.; Lloyd, A.L.; Camacho, M.; Schoenbaum, M.A.; Robbe-Austerman, S.; Thomsen, B.V.; Hall, S.M. Evaluation of serodiagnostic assays for Mycobacterium bovis infection in elk, white-tailed deer, and reindeer in the United States. Vet. Med. Int. 2012, 2012, 563293. [Google Scholar] [CrossRef] [Green Version]
- Buddle, B.M.; Wilson, T.; Denis, M.; Greenwald, R.; Esfandiari, J.; Lyashchenko, K.P.; Liggett, S.; Mackintosh, C.G. Sensitivity, specificity, and confounding factors of novel serological tests used for the rapid diagnosis of bovine tuberculosis in farmed red deer (Cervus elaphus). Clin. Vaccine Immunol. 2010, 17, 626–630. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boadella, M.; Barasona, J.A.; Diaz-Sanchez, S.; Lyashchenko, K.P.; Greenwald, R.; Esfandiari, J.; Gortazar, C. Performance of immunochromatographic and ELISA tests for detecting fallow deer infected with Mycobacterium bovis. Prev. Vet. Med. 2012, 104, 160–164. [Google Scholar] [CrossRef]
- Busch, F.; Bannerman, F.; Liggett, S.; Griffin, F.; Clarke, J.; Lyashchenko, K.P.; Rhodes, S. Control of bovine tuberculosis in a farmed red deer herd in England. Vet. Rec. 2017, 180, 68. [Google Scholar] [CrossRef] [Green Version]
- Collard, K.J. A study of the incidence of bovine tuberculosis in the wild red deer herd of Exmoor. Eur. J. Wild. Res. 2023, 69, 14. [Google Scholar] [CrossRef]
- Amat, A.C.; Gonzalez-Barrio, D.; Ortiz, J.A.; Diez-Delgado, I.; Boadella, M.; Barasona, J.A.; Bezos, J.; Romero, B.; Armenteros, J.A.; Lyashchenko, K.P.; et al. Testing Eurasian wild boar piglets for serum antibodies against Mycobacterium bovis. Prev. Vet. Med. 2015, 121, 93–98. [Google Scholar] [CrossRef] [Green Version]
- Roos, E.O.; Buss, P.; de Klerk-Lorist, L.-M.; Hewlett, J.; Hausler, G.A.; Rossouw, L.; McCall, A.J.; Cooper, D.; van Helden, P.; Parsons, S.D.C.; et al. Test performance of three serological assays for the detection of Mycobacterium bovis in warthogs (Phacochoerus africanus). Vet. Immunol. Immunopathol. 2016, 182, 79–84. [Google Scholar] [CrossRef] [PubMed]
- Ashford, R.T.; Anderson, P.; Waring, L.; Davé, D.; Smith, F.; Delahay, R.J.; Eamonn Gormley, E.; Chambers, M.A.; Sawyer, J.; Lesellier, S. Evaluation of the Dual Path Platform (DPP) VetTB assay for the detection of Mycobacterium bovis infection in badgers. Prev. Vet. Med. 2020, 180, 105005. [Google Scholar] [CrossRef] [PubMed]
- Rhodes, S.; Holder, T.; Clifford, D.; Dexter, I.; Clarke, J.; de la Rua-Domenech, R.; Gillgan, S.; Lyashchenko, K.; Lawrence, J.; Brewer, J.; et al. Evaluation of gamma-interferon and antibody tuberculosis tests in alpacas. Clin. Vaccine Immunol. 2012, 19, 1677. [Google Scholar] [CrossRef]
- New Zealand Annual Report for Bovine Tuberculosis: 2022-Surveillance-Annual-Report-No-49-3 September-Animals-TB-pdf. Available online: https://sciquest.org.nz/browse/publications/article/171695 (accessed on 19 February 2023).
- Whelan, C.; Whelan, A.O.; Shuralev, E.; Kwok HFHewinson, G.; Clarke, J.; Vordermeier, H.M. Performance of the Enferplex TB Assay with cattle in Great Britain and assessment of its suitability as a test to distinguish infected and vaccinated animals. Clin. Vaccine Immunol. 2010, 17, 813–817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Casal, C.; Díez-Guerrier, A.; Lvarez, J.A.; Rodriguez-Campos, S.; Mateos, A.; Linscott, R.; Martel, E.; Lawrence, J.C.; Whelan, C.; Clarke, J.; et al. Strategic use of serology for the diagnosis of bovine tuberculosis after intradermal skin testing. Vet. Microbiol. 2014, 170, 342–351. [Google Scholar] [CrossRef]
- O’Brien, A.; Clarke, J.; Hayton, A.; Adler, A.; Cutler, K.; Shaw, D.J.; Whelan, C.; Watt, N.J.; Harkiss, G.D. Diagnostic accuracy of the Enferplex bovine tuberculosis antibody test in cattle sera. Nat. Sci. Rep. 2023, 13, 1875. [Google Scholar] [CrossRef]
- O’Brien, A.; Whelan Clarke, J.B.; Hayton, A.; Watt, N.J.; Harkiss, G.D. Serological analysis of tuberculosis in goats by use of the Enferplex Caprine TB Multiplex Test. Clin. Vaccine Immunol. 2017, 24, e00518-16. [Google Scholar] [CrossRef] [Green Version]
- Bacigalupo, S.A.; Dixon, L.S.A.; Gubbins, K.; Kucharski, A.J.; Drewe, J.A. Wild boar visits to commercial pig farms in southwest England: Implications for disease transmission. Eur. J. Wildl. Res. 2022, 68, 69. [Google Scholar] [CrossRef]
- Naranjo, V.; Gortazar, C.; Vicente, J.; de la Fuente, J. Evidence of the role of the European wild boar as a reservoir of Mycobacterium tuberculosis complex. Vet. Microbiol. 2008, 127, 1–9. [Google Scholar] [CrossRef]
- Santos, N.; Correia-Neves, M.; Ghebremichael, S.; Kallenius, G.; Svenson, S.B.; Almeida, V. Epidemiology of M. bovis infection in wild boar (Sus scrofa) from Portugal. J. Wildl. Dis. 2009, 45, 1048–1061. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Marco, V.; Mazzone, P.; Capucchio, M.T.; Boniotti, M.B.; Aronica, V.; Russo, M.; Fiasconaro, M.; Cifani, N.; Corneli, S.; Biasibetti, E.; et al. Epidemiological significance of the domestic black pig (Sus scrofa) in maintenance of bovine tuberculosis in Sicilly. J. Clin. Microbiol. 2012, 50, 1209–1218. [Google Scholar] [CrossRef] [Green Version]
- Cardoso-Toset, F.; Luque, I.; Carrasco, L.; Jurado-Martos, F.; Risalde, M.A.; Venteo, A.; Infantes-Lorenzo, J.A.; Bezos, J.; Rueda, P.; Tapia, I.; et al. Evaluation of five serologic assays for bovine tuberculosis surveillance in domestic free-range pigs from southern Spain. Prev. Vet. Med. 2017, 137, 101–104. [Google Scholar] [CrossRef]
- Nugent, G.; Whitford, J.; Young, N. Use of released pigs as sentinels for Mycobacterium bovis. J. Wildl. Dis. 2002, 38, 665–677. [Google Scholar] [CrossRef] [PubMed]
- Bailey, S.S.; Crawshaw, T.R.; Smith, N.S.; Palgrave, C.J. Mycobacterium bovis infection in domestic pigs in Great Britain. Vet. J. 2013, 198, 391–397. [Google Scholar] [CrossRef] [PubMed]
TB-Free | TB-Infected | ||
---|---|---|---|
% Specificity [95%CI] | % Sensitivity [95%CI] | ||
(No Prior Skin Test) | Park/Wild: VL/Mb+ (No Prior Skin Test) | Farmed: Skin Test+/VL/Mb+ (with Prior Skin Test) | |
IDEXX ELISA | 98.8 [97.2–99.6] | 55.2 [45.2–65.0] | 76.6 [65.6–85.5] |
DPP VetTB | 99.0 [98.1–100] | 58.1 [48.7–67.5] | 77.9 [68.6–87.2] |
∆PPD ELISA | 98.8 [97.2–99.6] | 51.4 [41.5–61.3] | 79.2 [68.5–87.6] |
Enferplex High Se | 99.0 [98.1–100] | 56.2 [46.7–66.7] | 85.7 [77.9–93.5] |
Enferplex High Sp | 99.5 [ 98.8–100] | 55.2 [45.7–64.7] | 85.7 [77.9–93.5] |
TB-Positive Deer | Kappa Statistic | McNemar | |||
---|---|---|---|---|---|
k Value | Level of Agreement | SE of k | 95%CI | p Value | |
IDEXX v. DPPD ELISA | 0.83 | almost perfect | 0.043 | 0.75–0.92 | 0.789 |
IDEXX v. DPP VetTB | 0.81 | substantial | 0.046 | 0.72–0.90 | 0.453 |
Enferplex v. ∆PPD ELISA | 0.81 | substantial | 0.046 | 0.70–0.90 | 0.024 |
IDEXX v. Enferplex | 0.78 | substantial | 0.049 | 0.68–0.88 | 0.01 |
DPP VetTB v. Enferplex | 0.72 | substantial | 0.055 | 0.62–0.83 | 0.522 |
DPP VetTB v. ∆PPD ELISA | 0.69 | substantial | 0.056 | 0.58–0.80 | 0.327 |
Pig Tests | TB-Free (No Prior Skin Test) | TB-Infected Skin Test+/VL/Mb+ (with Prior Skin Test) |
---|---|---|
% Specificity [95%CI] | % Sensitivity [95%CI] | |
IDEXX ELISA | 99.0 [97.5–99.6] | 72.4 [54.3–85.3] |
DPP VetTB | 100.0 [99.1–100] | 86.2 [73.6–98.8] |
∆PPD ELISA | 99.0 [97.5–99.6] | 62.1 [44.0–77.3] |
Enferplex High Se | 99.3 [98.5–100] | 86.2 [73.6–98.8] |
Enferplex High Sp | 99.5 [ 98.8–100] | 86.2 [73.6–98.8] |
TB-Positive Pigs | Kappa Statistic | McNemar | |||
---|---|---|---|---|---|
k Value | Level of Agreement | SE of K | 95%CI | p Value | |
IDEXX v. ∆PPD ELISA | 0.77 | substantial | 0.123 | 0.53–1.0 | 0.248 |
IDEXX v. DPP VetTB | 0.71 | substantial | 0.153 | 0.41–1.0 | 0.248 |
IDEXX v. Enferplex | 0.59 | moderate | 0.173 | 0.25–0.93 | 0.134 |
DPP VetTB v. ∆PPD ELISA | 0.51 | moderate | 0.156 | 0.20–0.81 | 0.041 |
Enferplex v. ∆PPD ELISA | 0.42 | moderate | 0.156 | 0.11–0.72 | 0.023 |
DPP VetTB v. Enferplex | 0.34 | fair | 0.231 | −0.11–0.8 | 1.00 |
Pigs (n = 27) | Deer (n = 135) | |||
---|---|---|---|---|
Number of Tests Positive (out of 4) | n | % | n | % |
4 | 18 | 66.7 | 101 | 74.8 |
3 | 3 | 11.1 | 15 | 15 |
2 | 1 | 3.7 | 10 | 10 |
1 | 5 | 18.5 | 9 | 9 |
Mean Test % Sensitivity | Mean Test % Specificity | ||||||
---|---|---|---|---|---|---|---|
Single | Parallel | % Increase Se | Single | Parallel | % Decrease Sp | ||
Deer | with prior skin test | 79.9 | 87.2 | 7.3 | |||
no prior skin test | 55.0 | 58.9 | 3.9 | 99.03 | 98.4 | 0.63 | |
Pig | 76.7 | 83.9 | 7.2 | 99.4 | 98.8 | 0.6 |
Mean Test % Specificity | Mean Test % Sensitivity | ||||||
---|---|---|---|---|---|---|---|
Single | Serial | % Increase Sp | Single | Serial | % Decrease Se | ||
Deer | with prior skin test | 79.9 | 73.4 | 6.5 | |||
no prior skin test | 99.03 | 99.9 | 0.87 | 55.0 | 51.4 | 3.6 | |
Pig | 99.4 | 99.9 | 0.5 | 76.7 | 67.8 | 8.9 |
Wild Boar (n = 233) | Park Deer (n = 197) | |||
---|---|---|---|---|
ELISA Test | % Sp [95%CI] | % Positive | % Sp [95%CI] | % Positive |
IDEXX | 99.0 [97.5–99.6] | 17.2 | 98.8 [97.2–99.6] | 3.6 |
∆PPD | 99.0 [97.5–99.6] | 15.4 | 98.8 [97.2–99.6] | 5.1 |
Enferplex—High Se | 99.3 [98.5–100] | 19.7 | 99.0 [98.1–100] | 2.5 |
Enferplex—High Sp | 99.5 [98.8–100] | 19.3 | 99.5 [98.8–100] | 2.5 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Barton, P.; Robinson, N.; Middleton, S.; O’Brien, A.; Clarke, J.; Dominguez, M.; Gillgan, S.; Selmes, J.; Rhodes, S. Evaluation of Antibody Tests for Mycobacterium bovis Infection in Pigs and Deer. Vet. Sci. 2023, 10, 489. https://doi.org/10.3390/vetsci10080489
Barton P, Robinson N, Middleton S, O’Brien A, Clarke J, Dominguez M, Gillgan S, Selmes J, Rhodes S. Evaluation of Antibody Tests for Mycobacterium bovis Infection in Pigs and Deer. Veterinary Sciences. 2023; 10(8):489. https://doi.org/10.3390/vetsci10080489
Chicago/Turabian StyleBarton, Penny, Nick Robinson, Sonya Middleton, Amanda O’Brien, John Clarke, Maria Dominguez, Steve Gillgan, John Selmes, and Shelley Rhodes. 2023. "Evaluation of Antibody Tests for Mycobacterium bovis Infection in Pigs and Deer" Veterinary Sciences 10, no. 8: 489. https://doi.org/10.3390/vetsci10080489
APA StyleBarton, P., Robinson, N., Middleton, S., O’Brien, A., Clarke, J., Dominguez, M., Gillgan, S., Selmes, J., & Rhodes, S. (2023). Evaluation of Antibody Tests for Mycobacterium bovis Infection in Pigs and Deer. Veterinary Sciences, 10(8), 489. https://doi.org/10.3390/vetsci10080489