Flock sensitivity and specificity of pooled fecal qPCR and pooled serum ELISA for screening ovine paratuberculosis
Autoři:
Yoann Mathevon aff001; Gilles Foucras aff001; Fabien Corbière aff001
Působiště autorů:
UMR INRA ENVT 1225 IHAP, Ecole Nationale Vétérinaire de Toulouse, Toulouse Cedex, France
aff001
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226246
Souhrn
The aim of our study was to evaluate the flock sensitivity and specificity of fecal qPCR and serum ELISA using pooled samples for screening paratuberculosis in French sheep.
Using individual feces with low or high qPCR Ct values from ewes sampled in 14 infected flocks, a total of 555 pools of size 5, 10 and 20 were created by diluting individual materials in negative feces and analysed using a commercial IS900 qPCR kit. The relative performances of pooled serum ELISA analysis were evaluated based on the analysis of 181 different pools of size 5 and 10, composed of individual serum samples of various individual S/P values. Results showed that for pools of size 5, 10 or 20, individual fecal samples with low Ct values were invariably detected. Conversely fecal samples with high Ct values were associated with a lower detection rate in both pools of size 5 (87.0% to 90.0%), 10 (63.0% to 70.7%) and 20 (46.7% to 60.0%). After lowering the decision threshold to 25% and 15% for serum pools of size 5 and 10 respectively, the pooled serum ELISA relative sensitivity ranged between 62.2% and 100.0% depending on the composition of the pools.
Finally, a simulation study was carried out to evaluate the performances of 16 screening strategies at flock level, with varying pool size (5 to 20) and number (5 to 60). The use of pooled serum ELISA led to very false positive detection rate ranging between 37.6% and 91.8% in paratuberculosis free flocks and prevents its further use in that context. For infection prevalence ≤ 5%, the flock sensitivity based on pooled fecal qPCR ranged between 39.0% (5 pools of size 10) and 99.9% (300 sampled individuals, with pools of size 5,10 or20), and was always above 93% when the infection prevalence was greater or equal to 15%. We conclude that pooled-fecal qPCR but not pooled-serum ELISA could be a useful tool to detect sheep flocks infected with paratuberculosis.
Klíčová slova:
Enzyme-linked immunoassays – Cattle – DNA extraction – Animal performance – Serology – Sheep – Paratuberculosis – Disease surveillance
Zdroje
1. Allworth MB, Kennedy DJ. Progress in national control and assurance programs for ovine Johne’s disease in Australia. Vet Microbiol 2000;77:415–422. https://doi.org/10.1016/S0378-1135(00)00326-6 11118726
2. Benedictus G, Verhoeff J, Schukken YH, Hesselink JW. Dutch paratuberculosis programme history, principles and development. Vet Microbiol 2000;77:399–413. https://doi.org/10.1016/S0378-1135(00)00325-4 11118725
3. Groenendaal H, Nielen M, Hesselink JW. Development of the Dutch Johne’s disease control program supported by a simulation model. Prev Vet Med 2003;60:69–90. https://doi.org/10.1016/S0167-5877(03)00083-7 12900150
4. Kostoulas P, Leontides L, Enoe C, Billinis C, Florou M, Sofia M. Bayesian estimation of sensitivity and specificity of serum ELISA and faecal culture for diagnosis of paratuberculosis in Greek dairy sheep and goats. Prev Vet Med 2006;76:56–73. https://doi.org/10.1016/j.prevetmed.2006.04.006 16806541
5. Nielsen SS, Toft N. Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gamma assay and faecal culture techniques. Vet Microbiol 2008;129:217–35. https://doi.org/10.1016/j.vetmic.2007.12.011 18255239
6. Dorfman R. The Detection of Defective Members of Large Populations. Ann Math Stat 1943;14:436–440. https://doi.org/10.1214/aoms/1177731363
7. Kalis CHJ, Hesselink JW, Barkema HW, Collins MT. Culture of strategically pooled bovine fecal samples as a method to screen herds for paratuberculosis. J Vet Diagn Invest 2000;12:547–551. https://doi.org/10.1177/104063870001200609 11108455
8. Weber MF, Groenendaal H, van Roermund HJ, Nielen M. Simulation of alternatives for the Dutch Johne’s disease certification-and-monitoring program. Prev Vet Med 2004;62:1–17. https://doi.org/10.1016/j.prevetmed.2003.11.006 15154681
9. Whittington RJ, Fell S, Walker D, McAllister S, Marsh I, Sergeant E, et al. Use of Pooled Fecal Culture for Sensitive and Economic Detection of Mycobacterium avium subsp. paratuberculosisInfection in Flocks of Sheep. J Clin Microbiol 2000;38:2550–2556. 10878042
10. Eamens GJ, Walker DM, Porter NS, Fell SA. Pooled faecal culture for the detection of Mycobacterium avium subsp paratuberculosis in goats. Aust Vet J 2007;85:243–51. https://doi.org/10.1111/j.1751-0813.2007.00160.x 17547638
11. Eamens GJ, Whittington RJ, Turner MJ, Austin SL, Fell SA, Marsh IB. Evaluation of radiometric faecal culture and direct PCR on pooled faeces for detection of Mycobacterium avium subsp. paratuberculosis in cattle. Vet Microbiol 2007;125:22–35. https://doi.org/10.1016/j.vetmic.2007.04.043 17560743
12. Aly SS, Mangold BL, Whitlock RH, Sweeney RW, Anderson RJ, Jiang J, et al. Correlation between Herrold egg yolk medium culture and real-time quantitative polymerase chain reaction results for Mycobacterium avium subspecies paratuberculosis in pooled fecal and environmental samples. J Vet Diagn Invest 2010;22:677–683. https://doi.org/10.1177/104063871002200501 20807920
13. Nielsen SS, Thamsborg SM, Houe H, Bitsch V. Bulk-tank milk ELISA antibodies for estimating the prevalence of paratuberculosis in Danish dairy herds. Prev Vet Med 2000;44:1–7. https://doi.org/10.1016/S0167-5877(00)00098-2 10727740
14. Stabel JR. Transitions in immune responses to Mycobacterium paratuberculosis. Vet Microbiol 2000;77:465–473. https://doi.org/10.1016/S0378-1135(00)00331-X 11118731
15. Slana I, Liapi M, Moravkova M, Kralova A, Pavlik I. Mycobacterium avium subsp. paratuberculosis in cow bulk tank milk in Cyprus detected by culture and quantitative IS900 and F57 real-time PCR. Prev Vet Med 2009;89:223–226. https://doi.org/10.1016/j.prevetmed.2009.02.020 19349086
16. Raizman EA, Wells SJ, Godden SM, Bey RF, Oakes MJ, Bentley DC, et al. The distribution of Mycobacterium avium ssp. paratuberculosis in the environment surrounding Minnesota dairy farms. J Dairy Sci 2004;87:2959–66. https://doi.org/10.3168/jds.S0022-0302(04)73427-X 15375057
17. Whittington RJ, Marsh IB, Taylor PJ, Marshall DJ, Taragel C, Reddacliff LA. Isolation of Mycobacterium avium subsp paratuberculosis from environmental samples collected from farms before and after destocking sheep with paratuberculosis. Aust Vet J 2003;81:559–563. https://doi.org/10.1111/j.1751-0813.2003.tb12887.x 15086096
18. van Schaik G, R Rossiter C, Stehman S, J Shin S, Schukken Y. Longitudinal study to investigate variation in results of repeated ELISA and culture of fecal samples for Mycobacterium avium subsp paratuberculosis in commercial dairy herds. Am J Vet Res 2003;64:479–84. https://doi.org/10.2460/ajvr.2003.64.479 12693540
19. Whittington RJ, Whittington AM, Waldron A, Begg DJ, de Silva K, Purdie AC, et al. Development and validation of a liquid medium (M7H9C) for routine culture of Mycobacterium avium subsp paratuberculosis to replace modified Bactec 12B medium. J Clin Microbiol 2013;51:3993–4000. https://doi.org/10.1128/Jcm.01373-13 24048541
20. Mita A, Mori Y, Nakagawa T, Tasaki T, Utiyama K, Mori H. Comparison of fecal pooling methods and DNA extraction kits for the detection of Mycobacterium avium subspecies paratuberculosis. Microbiologyopen 2015;5:134–142. https://doi.org/10.1002/mbo3.318 26666871
21. Timms VJ, Mitchell HM, Neilan BA. Optimisation of DNA extraction and validation of PCR assays to detect Mycobacterium avium subsp. paratuberculosis. J Microbiol Methods 2015;112:99–103. https://doi.org/10.1016/j.mimet.2015.03.016 25797305
22. Fock-Chow-Tho D, Topp E, Ibeagha-Awemu EA, Bissonnette N. Comparison of commercial DNA extraction kits and quantitative PCR systems for better sensitivity in detecting the causative agent of paratuberculosis in dairy cow fecal samples. J Dairy Sci 2017;100:572–81. https://doi.org/10.3168/jds.2016-11384 27889120
23. Pesqueira MN, Yus E, Factor C, Mato I, Sanjuan ML, Eiras C, et al. Short communication: Correlation between within-herd antibody-prevalence and bulk tank milk antibody levels to Mycobacterium avium ssp. paratuberculosis using 2 commercial immunoassays. J Dairy Sci 2017;100:7544–8. https://doi.org/10.3168/jds.2017-12706 28711239
24. Dhand NK, Sergeant E, Toribio J-ALML, Whittington RJ. Estimation of sensitivity and flock-sensitivity of pooled faecal culture for Mycobacterium avium subsp. paratuberculosis in sheep. Prev Vet Med 2010;95:248–257. https://doi.org/10.1016/j.prevetmed.2010.03.013 20430455
25. Brinkhof JMA, Houwers DJ, van Maanen C. Development of a sample pooling strategy for the serodiagnosis of small ruminant lentiviral infections using the ELITEST-MVV ELISA. Small Rumin Res 2007;70:194–9. https://doi.org/10.1016/j.smallrumres.2006.03.003
26. Rovira A, Cano JP, Muñoz-Zanzi C. Feasibility of pooled-sample testing for the detection of porcine reproductive and respiratory syndrome virus antibodies on serum samples by ELISA. Vet Microbiol 2008;130:60–68. https://doi.org/10.1016/j.vetmic.2007.12.016 18243590
27. Mathevon Y, Foucras G, Falguières R, Corbiere F. Estimation of the sensitivity and specificity of two serum ELISAs and one fecal qPCR for diagnosis of paratuberculosis in sub-clinically infected young-adult French sheep using latent class Bayesian modeling. BMC Vet Res 2017;13:230. https://doi.org/10.1186/s12917-017-1145-x 28774299
28. R Foundation for Statistical Computing. R: A language and environment for statistical computing. Vienna, Austria: R Core Team.; n.d.
29. Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 2015;67:1–48. https://doi.org/10.18637/jss.v067.i01
30. Brien J. simulator: An engine for running simulations, R package version 0.2.0. [https://CRAN.R-project.org/package=simulator]. 2016.
31. Christensen J, Gardner IA. Herd-level interpretation of test results for epidemiologic studies of animal diseases. Prev Vet Med 2000;45:83–106. doi: 10.1016/s0167-5877(00)00118-5 10802335
32. Sweeney RW, Whitlock RH, Hamir AN, Rosenberger AE, Herr SA. Isolation of Mycobacterium paratuberculosis after oral inoculation in uninfected cattle. Am J Vet Res 1992;53:1312–1314. 1510305
33. Moloney BJ, Whittington RJ. Cross species transmission of ovine Johne’s disease from sheep to cattle: an estimate of prevalence in exposed susceptible cattle. Aust Vet J 2008;86:117–123. https://doi.org/10.1111/j.1751-0813.2008.00272.x 18363982
34. Wells SJ, Whitlock RH, Lindeman CJ, Fyock T. Evaluation of bacteriologic culture of pooled fecal samples for detection of Mycobacterium paratuberculosis. Am J Vet Res 2002;63:1207–11. doi: 10.2460/ajvr.2002.63.1207 12171178
35. Tavornpanich S, Gardner IA, Anderson RJ, Shin S, Whitlock RH, Fyock T, et al. Evaluation of microbial culture of pooled fecal samples for detection of Mycobacterium avium subsp paratuberculosis in large dairy herds. Am J Vet Res 2004;65:1061–70. https://doi.org/10.2460/ajvr.2004.65.1061 15334839
36. Enhanced sensitivity and fast turnaround time in laboratory diagnosis for bovine paratuberculosis in faecal samples. J Microbiol Methods 2018;152:39–47. https://doi.org/10.1016/j.mimet.2018.07.010 30031012
37. Sting R, Hrubenja M, Mandl J, Seemann G, Salditt A, Waibel S. Detection of Mycobacterium avium subsp. paratuberculosis in faeces using different procedures of pre-treatment for real-time PCR in comparison to culture. Vet J 2014;199:138–42. https://doi.org/10.1016/j.tvjl.2013.08.033 24280588
38. Plain KM, Marsh IB, Waldron AM, Galea F, Whittington AM, Saunders VF, et al. High-throughput direct fecal PCR assay for detection of Mycobacterium avium subsp. paratuberculosis in sheep and cattle. J Clin Microbiol 2014;52:745–57. https://doi.org/10.1128/JCM.03233-13 24352996
39. Christopher-Hennings J, Dammen MA, Weeks SR, Epperson WB, Singh SN, Steinlicht GL, et al. Comparison of Two DNA Extractions and Nested PCR, Real-Time PCR, a New Commercial PCR Assay, and Bacterial Culture for Detection of Mycobacterium Avium Subsp. Paratuberculosis in Bovine Feces. J Vet Diagn Invest 2003;15:87–93. https://doi.org/10.1177/104063870301500201 12661717
40. Eamens GJ, Marsh IM, Plain KM, Whittington RJ. Paratuberculosis (Johne’s Disease). Australian and New Zealand Standard Diagnostic Procedure; 2015.
41. Graesboll K, Andresen LO, Halasa T, Toft N. Opportunities and challenges when pooling milk samples using ELISA. Prev Vet Med 2016. https://doi.org/10.1016/j.prevetmed.2016.08.001
42. de Silva K, Plain K, Purdie A, Begg D, Whittington R. Defining resilience to mycobacterial disease: Characteristics of survivors of ovine paratuberculosis. Vet Immunol Immunopathol 2018;195:56–64. https://doi.org/10.1016/j.vetimm.2017.11.008 29249318
43. McKenna SL, Sockett DC, Keefe GP, McClure J, VanLeeuwen JA, Barkema HW. Comparison of two enzyme-linked immunosorbent assays for diagnosis of Mycobacterium avium subsp. paratuberculosis. J Vet Diagn Invest 2005;17:463–6. doi: 10.1177/104063870501700510 16312239
44. Collins MT, Wells SJ, Petrini KR, Collins JE, Schultz RD, Whitlock RH. Evaluation of five antibody detection tests for diagnosis of bovine paratuberculosis. Clin Diagn Lab Immunol 2005;12:685–92. https://doi.org/10.1128/CDLI.12.6.685-692.2005 15939741
45. Wells SJ, Collins MT, Faaberg KS, Wees C, Tavornpanich S, Petrini KR, et al. Evaluation of a rapid fecal PCR test for detection of Mycobacterium avium subsp. paratuberculosis in dairy cattle. Clin Vaccine Immunol 2006;13:1125–1130. https://doi.org/10.1128/CVI.00236-06 16928884
46. Tavornpanich S, Munoz-Zanzi CA, Wells SJ, Raizman EA, Carpenter TE, Johnson WO, et al. Simulation model for evaluation of testing strategies for detection of paratuberculosis in midwestern US dairy herds. Prev Vet Med 2008;83:65–82. https://doi.org/10.1016/j.prevetmed.2007.06.010 17719108
47. Sergeant ESG, McAloon CG, Tratalos JA, Citer LR, Graham DA, More SJ. Evaluation of national surveillance methods for detection of Irish dairy herds infected with Mycobacterium avium ssp. paratuberculosis. J Dairy Sci 2019;102:2525–38. https://doi.org/10.3168/jds.2018-15696 30692009
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