Tuberculosis in the wild boar: Frequentist and Bayesian estimations of diagnostic test parameters when Mycobacterium bovis is present in wild boars but at low prevalence


Autoři: Céline Richomme aff001;  Aurélie Courcoul aff002;  Jean-Louis Moyen aff003;  Édouard Reveillaud aff004;  Oscar Maestrini aff005;  Krystel de Cruz aff006;  Antoine Drapeau aff006;  Maria Laura Boschiroli aff006
Působiště autorů: Nancy Laboratory for Rabies and Wildlife, ANSES, Malzéville, France aff001;  University Paris-Est, Laboratory for Animal Health, Epidemiology Unit, ANSES, Maisons-Alfort, France aff002;  Laboratoire Départemental d’Analyse et de Recherche de la Dordogne, Coulounieix-Chamiers, France aff003;  Unit of Coordination and Support to Surveillance, ANSES, Maisons-Alfort, France aff004;  UR 045, INRA, Corte, France aff005;  University Paris-Est, Laboratory for Animal Health, Tuberculosis National Reference Laboratory, ANSES, Maisons-Alfort, France aff006
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222661

Souhrn

The Eurasian wild boar (Sus scrofa) is increasingly considered as a relevant actor in the epidemiology of animal tuberculosis (TB). Therefore, monitoring TB in this species is key when establishing comprehensive control schemes for this disease still present in Europe. No data are available on direct and indirect TB diagnostic methods in wild boars in epidemiological contexts where TB is endemic in cattle and detected in wild boars at low prevalence. We aimed to estimate and compare sensitivity and specificity values for bacterial culture, PCR and three commercial ELISAs, i.e. the TB ELISA-VK (using the bPPD antigen), INgezim TB Porcine and IDEXX M. bovis Ab Test (both using the MPB83 and MPB70 antigens), under field conditions in France. We used frequentist methods, with bacteriology as the gold standard, and a Bayesian formulation of the latent class analysis (LCA), without using a gold standard. Submandibular lymph nodes and sera from 495 wild boars hunter-harvested in three endemic areas (Aquitaine region, Côte d’Or region, and Corsica region) were collected between 2014 and 2016. Only eight individuals were positive for M. bovis by bacteriology (1.61%; CI95% 0.70–3.51%). The LCA method provided high specificities (99.2%; CI95% 98.2–99.8% for INgezim TB Porcine and 99.7%; CI95% 98.8–100% for IDEXX M. bovis Ab Test) and sensitivities (78.5%; CI95% 65.1–88.8% for INgezim TB Porcine and 83.9%; CI95% 58.9–97.2% for IDEXX M. bovis Ab Test) for both ELISAs using the MPB83 and MPB70 antigens. Bacterial culture showed limited sensitivity (42.8%; CI95% 19.0–70.6%), estimated as the probability of a positive result in an animal exposed to M. bovis. PCR and ELISA using the bPPD antigens demonstrated high specificities, and sensitivities intermediates between culture and the ELISAs using the MPB83 and MPB70 antigens. These results suggest that ELISA tests using the MPB83 and MPB70 antigens are useful to detect and monitor TB exposure of wild boar populations in field conditions in France.

Klíčová slova:

Bacteriology – Mycobacterium bovis – Mycobacterium tuberculosis – Polymerase chain reaction – Serology – Tuberculosis – Tuberculosis diagnosis and management – Bovine tuberculosis


Zdroje

1. Schiller I, Waters WR, RayWaters W, Vordermeier HM, Jemmi T, Welsh M, et al. Bovine tuberculosis in Europe from the perspective of an officially tuberculosis free country: trade, surveillance and diagnostics. Vet Microbiol. 2011;151:153–9. doi: 10.1016/j.vetmic.2011.02.039 21439740

2. Aranaz A, De Juan L, Montero N, Sánchez C, Galka M, Delso C, et al. Bovine tuberculosis (Mycobacterium bovis) in wildlife in Spain. J Clin Microbiol. 2004;42:2602–8. doi: 10.1128/JCM.42.6.2602-2608.2004 15184440

3. Dondo A, Zoppi S, Rossi F, Chiavacci L, Barbaro A, Garrone A, et al. Mycobacteriosis in wild boar: results of 2000–2006 activity in north-western Italy. Epidémiol Santé Anim. 2007;35–42.

4. Duarte EL, Domingos M, Amado A, Botelho A. Spoligotype diversity of Mycobacterium bovis and Mycobacterium caprae animal isolates. Vet Microbiol. 2008;130:415–21. doi: 10.1016/j.vetmic.2008.02.012 18417301

5. Zanella G, Duvauchelle A, Hars J, Moutou F, Boschiroli ML, Durand B. Patterns of lesions of bovine tuberculosis in wild red deer and wild boar. Vet Rec. 2008;163:43–7. doi: 10.1136/vr.163.2.43 18621995

6. Rodríguez S, Romero B, Bezos J, de Juan L, Álvarez J, Castellanos E, et al. High spoligotype diversity within a Mycobacterium bovis population: Clues to understanding the demography of the pathogen in Europe. Vet Microbiol. 2010;141:89–95. doi: 10.1016/j.vetmic.2009.08.007 19720476

7. Réveillaud É, Desvaux S, Boschiroli M-L, Hars J, Faure É, Fediaevsky A, et al. Infection of Wildlife by Mycobacterium bovis in France Assessment Through a National Surveillance System, Sylvatub. Front Vet Sci [Internet]. 2018 [cité 8 nov 2018];5. Disponible sur: https://www.frontiersin.org/articles/10.3389/fvets.2018.00262/full

8. Nugent G, Gortazar C, Knowles G. The epidemiology of Mycobacterium bovis in wild deer and feral pigs and their roles in the establishment and spread of bovine tuberculosis in New Zealand wildlife. N Z Vet J. 2015;63 Suppl 1:54–67.

9. Naranjo V, Gortazar C, Vicente J, de la Fuente J. Evidence of the role of European wild boar as a reservoir of Mycobacterium tuberculosis complex. Vet Microbiol. 2008;127:1–9. doi: 10.1016/j.vetmic.2007.10.002 18023299

10. Santos N, Correia-Neves M, Ghebremichael S, Källenius G, Svenson SB, Almeida V. Epidemiology of Mycobacterium bovis infection in wild boar (Sus scrofa) from Portugal. J Wildl Dis. 2009;45:1048–61. doi: 10.7589/0090-3558-45.4.1048 19901381

11. Barasona JA, Torres MJ, Aznar J, Gortázar C, Vicente J. DNA Detection Reveals Mycobacterium tuberculosis Complex Shedding Routes in Its Wildlife Reservoir the Eurasian Wild Boar. Transbound Emerg Dis. 2017;64:906–15. doi: 10.1111/tbed.12458 26663251

12. Santos N, Almeida V, Gortázar C, Correia-Neves M. Patterns of Mycobacterium tuberculosis-complex excretion and characterization of super-shedders in naturally-infected wild boar and red deer. Vet Res. 2015;46:129. doi: 10.1186/s13567-015-0270-4 26518244

13. Gortázar C, Fernández-Calle LM, Collazos-Martínez JA, Mínguez-González O, Acevedo P. Animal tuberculosis maintenance at low abundance of suitable wildlife reservoir hosts: A case study in northern Spain. Prev Vet Med. 2017;146:150–7. doi: 10.1016/j.prevetmed.2017.08.009 28992920

14. Zanella G, Durand B, Hars J, Moutou F, Garin-Bastuji B, Duvauchelle A, et al. Mycobacterium bovis in wildlife in France. J Wildl Dis. 2008;44:99–108. doi: 10.7589/0090-3558-44.1.99 18263825

15. Santos N, Geraldes M, Afonso A, Almeida V, Correia-Neves M. Diagnosis of tuberculosis in the wild boar (Sus scrofa): a comparison of methods applicable to hunter-harvested animals. PloS One. 2010;5.

16. Risco D, Serrano E, Fernández-Llario P, Cuesta JM, Gonçalves P, García-Jiménez WL, et al. Severity of Bovine Tuberculosis Is Associated with Co-Infection with Common Pathogens in Wild Boar. PLoS ONE. 2014;9:e110123. doi: 10.1371/journal.pone.0110123 25350002

17. Krajewska M, Lipiec M, Zabost A, Augustynowicz-Kopeć E, Szulowski K. Bovine tuberculosis in a wild boar (Sus scrofa) in Poland. J Wildl Dis. 2014;50:1001–2. doi: 10.7589/2013-07-187 25075538

18. Boniotti MB, Gaffuri A, Gelmetti D, Tagliabue S, Chiari M, Mangeli A, et al. Detection and Molecular Characterization of Mycobacterium microti Isolates in Wild Boar from Northern Italy. J Clin Microbiol. 2014;52:2834–43. doi: 10.1128/JCM.00440-14 24871212

19. Chiari M, Ferrari N, Giardiello D, Avisani D, Pacciarini ML, Alborali L, et al. Spatiotemporal and Ecological Patterns of Mycobacterium microti Infection in Wild Boar (Sus scrofa). Transbound Emerg Dis. 2016;63:e381–388. doi: 10.1111/tbed.12313 25580561

20. Michelet L, de Cruz K, Zanella G, Aaziz R, Bulach T, Karoui C, et al. Infection with Mycobacterium microti in animals in France. J Clin Microbiol. 2015;53:981–5. doi: 10.1128/JCM.02713-14 25540404

21. Lara GHB, Ribeiro MG, Leite CQF, Paes AC, Guazzelli A, Silva AVD, et al. Occurrence of Mycobacterium spp. and other pathogens in lymph nodes of slaughtered swine and wild boars (Sus scrofa). Res Vet Sci. 2011;90:185–8. doi: 10.1016/j.rvsc.2010.06.009 20621319

22. Gortazar C, Vicente J, Gavier-Widén D. Pathology of bovine tuberculosis in the European wild boar (Sus scrofa). Vet Rec. 2003;152:779–80. doi: 10.1136/vr.152.25.779 12846290

23. de Lisle GW, Bengis RG, Schmitt SM, O’Brien DJ. Tuberculosis in free-ranging wildlife: detection, diagnosis and management. Rev Sci Tech Int Off Epizoot. 2002;21:317–34.

24. Courcoul A, Moyen J-L, Brugère L, Faye S, Hénault S, Gares H, et al. Estimation of sensitivity and specificity of bacteriology, histopathology and PCR for the confirmatory diagnosis of bovine tuberculosis using latent class analysis. PloS One. 2014;9:e90334. doi: 10.1371/journal.pone.0090334 24625670

25. Corner L a. L, Gormley E, Pfeiffer DU. Primary isolation of Mycobacterium bovis from bovine tissues: conditions for maximising the number of positive cultures. Vet Microbiol. 2012;156:162–71. doi: 10.1016/j.vetmic.2011.10.016 22074859

26. Hines N, Payeur JB, Hoffman LJ. Comparison of the recovery of Mycobacterium bovis isolates using the BACTEC MGIT 960 system, BACTEC 460 system, and Middlebrook 7H10 and 7H11 solid media. J Vet Diagn Investig Off Publ Am Assoc Vet Lab Diagn Inc. 2006;18:243–50.

27. Sinha P, Gupta A, Prakash P, Anupurba S, Tripathi R, Srivastava GN. Differentiation of Mycobacterium tuberculosis complex from non-tubercular mycobacteria by nested multiplex PCR targeting IS6110, MTP40 and 32kD alpha antigen encoding gene fragments. BMC Infect Dis. 2016;16:123. doi: 10.1186/s12879-016-1450-1 26968508

28. Thomas J, Infantes-Lorenzo JA, Moreno I, Cano-Terriza D, de Juan L, García-Bocanegra I, et al. Validation of a new serological assay for the identification of Mycobacterium tuberculosis complex-specific antibodies in pigs and wild boar. Prev Vet Med. 2019;162:11–7. doi: 10.1016/j.prevetmed.2018.11.004 30621888

29. Aurtenetxe O, Barral M, Vicente J, de la Fuente J, Gortázar C, Juste RA. Development and validation of an enzyme-linked immunosorbent assay for antibodies against Mycobacterium bovis in European wild boar. BMC Vet Res. 2008;4:43. doi: 10.1186/1746-6148-4-43 18976491

30. Richomme C, Boadella M, Courcoul A, Durand B, Drapeau A, Corde Y, et al. Exposure of Wild Boar to Mycobacterium tuberculosis Complex in France since 2000 Is Consistent with the Distribution of Bovine Tuberculosis Outbreaks in Cattle. PLoS ONE [Internet]. 2013 [cité 19 oct 2015];8. Disponible sur: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3805591/

31. Boadella M, Lyashchenko K, Greenwald R, Esfandiari J, Jaroso R, Carta T, et al. Serologic tests for detecting antibodies against Mycobacterium bovis and Mycobacterium avium subspecies paratuberculosis in Eurasian wild boar (Sus scrofa scrofa). J Vet Diagn Investig Off Publ Am Assoc Vet Lab Diagn Inc. 2011;23:77–83.

32. García-Bocanegra I, Pérez de Val B, Arenas-Montes A, Paniagua J, Boadella M, Gortázar C, et al. Seroprevalence and Risk Factors Associated to Mycobacterium bovis in Wild Artiodactyl Species from Southern Spain, 2006–2010. PLoS ONE. 2012;7:e34908. doi: 10.1371/journal.pone.0034908 22523563

33. Pérez de Val B, Napp S, Velarde R, Lavín S, Cervera Z, Singh M, et al. Serological Follow-up of Tuberculosis in a Wild Boar Population in Contact with Infected Cattle. Transbound Emerg Dis. 2015;

34. Cardoso-Toset F, Luque I, Carrasco L, Jurado-Martos F, Risalde MÁ, Venteo Á, et al. Evaluation of five serologic assays for bovine tuberculosis surveillance in domestic free-range pigs from southern Spain. Prev Vet Med. 2017;137:101–4. doi: 10.1016/j.prevetmed.2016.12.016 28089289

35. Roos EO, Buss P, de Klerk-Lorist L-M, Hewlett J, Hausler GA, Rossouw L, et al. Test performance of three serological assays for the detection of Mycobacterium bovis infection in common warthogs (Phacochoerus africanus). Vet Immunol Immunopathol. 2016;182:79–84. doi: 10.1016/j.vetimm.2016.10.006 27863555

36. Roos EO, Olea-Popelka F, Buss P, Hausler GA, Warren R, van Helden PD, et al. Measuring antigen-specific responses in Mycobacterium bovis-infected warthogs (Phacochoerus africanus) using the intradermal tuberculin test. BMC Vet Res [Internet]. 2018 [cité 30 avr 2019];14. Disponible sur: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6247514/

37. Cano-Terriza D, Risalde MA, Rodríguez-Hernández P, Napp S, Fernández-Morente M, Moreno I, et al. Epidemiological surveillance of Mycobacterium tuberculosis complex in extensively raised pigs in the south of Spain. Prev Vet Med. 2018;159:87–91. doi: 10.1016/j.prevetmed.2018.08.015 30314795

38. Réveillaud É, Desvaux S, Boschiroli M-L, Hars J, Faure É, Fediaevsky A, et al. Infection of Wildlife by Mycobacterium bovis in France Assessment Through a National Surveillance System, Sylvatub. Front Vet Sci. 2018;5:262. doi: 10.3389/fvets.2018.00262 30430112

39. OIE. Bovine tuberculosis. Man Diagn Tests Vaccines Terr Anim Mamm Birds Bees. 7e éd. PAris; 2002. p. 674–89.

40. Michelet L, de Cruz K, Karoui C, Tambosco J, Moyen J-L, Hénault S, et al. Second line molecular diagnosis for bovine tuberculosis to improve diagnostic schemes. PLOS ONE. 2018;13:e0207614. doi: 10.1371/journal.pone.0207614 30475835

41. Zhang J, Abadia E, Refregier G, Tafaj S, Boschiroli ML, Guillard B, et al. Mycobacterium tuberculosis complex CRISPR genotyping: improving efficiency, throughput and discriminative power of « spoligotyping » with new spacers and a microbead-based hybridization assay. J Med Microbiol. 2010;59:285–94. doi: 10.1099/jmm.0.016949-0 19959631

42. Thierry D, Brisson-Noël A, Vincent-Lévy-Frébault V, Nguyen S, Guesdon JL, Gicquel B. Characterization of a Mycobacterium tuberculosis insertion sequence, IS6110, and its application in diagnosis. J Clin Microbiol. 1990;28:2668–73. 2177747

43. Boadella M, Gortázar C. Effect of haemolysis and repeated freeze-thawing cycles on wild boar serum antibody testing by ELISA. BMC Res Notes. 2011;4:498. doi: 10.1186/1756-0500-4-498 22087883

44. Sturtz S, Ligges U, Gelman A. R2WinBUGS: A Package for Running WinBUGS from R. J Stat Softw. 2005;12:1–16.

45. Madeira S, Manteigas A, Ribeiro R, Otte J, Fonseca AP, Caetano P, et al. Factors that Influence Mycobacterium bovis Infection in Red Deer and Wild Boar in an Epidemiological Risk Area for Tuberculosis of Game Species in Portugal. Transbound Emerg Dis. 2015;n/a–n/a.

46. Vicente J, Barasona JA, Acevedo P, Ruiz-Fons JF, Boadella M, Diez-Delgado I, et al. Temporal trend of tuberculosis in wild ungulates from Mediterranean Spain. Transbound Emerg Dis. 2013;60 Suppl 1:92–103.

47. Richomme C, Boschiroli ML, Hars J, Casabianca F, Ducrot C. Bovine tuberculosis in livestock and wild boar on the Mediterranean island, Corsica. J Wildl Dis. 2010;46:627–31. doi: 10.7589/0090-3558-46.2.627 20688663

48. Cavalerie L, Courcoul A, Boschiroli M-L, Réveillaud É, Gay P. Bovine Tuberculosis in France in 2014: a stable situation. Bull Épidémiologique Anim Health Nutr. 2015;71:4–11.

49. Wiker HG. MPB70 and MPB83—major antigens of Mycobacterium bovis. Scand J Immunol. 2009;69:492–9. doi: 10.1111/j.1365-3083.2009.02256.x 19439009

50. Toft N, Jørgensen E, Højsgaard S. Diagnosing diagnostic tests: evaluating the assumptions underlying the estimation of sensitivity and specificity in the absence of a gold standard. Prev Vet Med. 2005;68:19–33. doi: 10.1016/j.prevetmed.2005.01.006 15795013


Článek vyšel v časopise

PLOS One


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Krvácení v důsledku portální hypertenze při jaterní cirhóze – od pohledu záchranné služby až po závěrečný hepato-gastroenterologický pohled
nový kurz
Autoři: PhDr. Petr Jaššo, MBA, MUDr. Hynek Fiala, Ph.D., prof. MUDr. Radan Brůha, CSc., MUDr. Tomáš Fejfar, Ph.D., MUDr. David Astapenko, Ph.D., prof. MUDr. Vladimír Černý, Ph.D.

Rozšíření možností lokální terapie atopické dermatitidy v ordinaci praktického lékaře či alergologa
Autoři: MUDr. Nina Benáková, Ph.D.

Léčba bolesti v ordinaci praktického lékaře
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se