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Is serological monitoring a fit-for-purpose tool to assess the epidemiological situation of tuberculosis in the sylvatic species of European bison (Bison bonasus) in Poland?

Michał K. Krzysiak
Michał K. Krzysiak
, 
Magdalena Larska
Magdalena Larska
, 
Anna Zabost
Anna Zabost
, 
Anna Didkowska
Anna Didkowska
, 
Monika Krajewska-Wędzina
Monika Krajewska-Wędzina
, 
Krzysztof Anusz
Krzysztof Anusz
 et 
Ewa Augustynowicz-Kopeć
Ewa Augustynowicz-Kopeć
   | 30 juil. 2022
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Publié en ligne: 30 juil. 2022
Pages: 333 - 344
Reçu: 14 mars 2022
Accepté: 12 juil. 2022
DOI: https://doi.org/10.2478/jvetres-2022-0038
Mots clés
© 2022 Michał K. Krzysiak et al. published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Fig. 1

Distribution of European bison populations included in the study. Herd locations are marked with European bison silhouettes. The captive herds are marked with encircled silhouettes
Distribution of European bison populations included in the study. Herd locations are marked with European bison silhouettes. The captive herds are marked with encircled silhouettes

Fig. 2

Distribution of sample-to-positive (S/P) values ((O.D. value (optical density at 450 nm) of the test sample − mean O.D. value for negative controls)/(mean O.D. value for positive controls − mean O.D. value for negative controls)) of individual samples
Distribution of sample-to-positive (S/P) values ((O.D. value (optical density at 450 nm) of the test sample − mean O.D. value for negative controls)/(mean O.D. value for positive controls − mean O.D. value for negative controls)) of individual samples

Fig. 3

Receiver operating characteristic curve of M. bovis antibody ELISA against a combined tuberculin skin test and interferon gamma release assay (TST+IGRA)
Receiver operating characteristic curve of M. bovis antibody ELISA against a combined tuberculin skin test and interferon gamma release assay (TST+IGRA)

Comparison of an antibody ELISA and tuberculin skin test (TST), interferon gamma release assay (IGRA), and TST and IGRA combined in identification of tuberculosis-affected European bison

Antibody ELISA versus TST (na = 25; 4/21b) IGRA (n = 31; 9/22b) TST+IGRA (na = 33; 13/20b)
Positive/negative results
Sensitivity (%) 50.00 22.22 38.46
95% CIc 6.16–93.24 2.81–60.01 13.86–68.42
Specificity (%) 95.24 90.91 100
95% CI 76.18–99.88 70.84–98.88 83.16–100
Positive predictive value (%) 9.59 2.41 100
95% CI 1.22–47.64 0.41–12.10 −
Negative predictive value (%) 99.47 99.14 99.38
95% CI 98.60–99.80 98.76–99.41 99.05–99.60
Accuracy 94.76 90.22 99.38
95% CI 77.86–99.72 74.12–97.91 88.27–100
Kappa 0.503 0.157 0.431
95% CI 0.019–0.987 −0.191–0.506 0.148–0.713
S/P values
Area under ROC curve 0.619 0.848 0.867
Standard errord 0.205 0.077 0.0773
95% CI 0.405–0.804 0.674–0.951 0.704–0.960
Significance level P 0.562 <0.0001 <0.0001
Youden’s J statisticse 0.452 0.641 0.719
Optimum cut-off point >0.002 >−0.02 >−0.016
Sensitivity 50.00 77.78 76.92
Specificity 95.24 86.36 95.00

Descriptive statistics of 436 European bison tested for the presence of Mycobacterium bovis antibodies with respect to the year of sampling, origin, population type, sanitary status, sex and age group. Statistically significant differences were determined using Pearson’s χ2 test. A P value of ≤0.05 was considered significant

Variable
n/Na % 95% CIb χ2 P
Year 9.50 0.22
2013 1/13 7.7 0.2–36.0
2014 0/47 0 0–7.5c
2015 0/63 0 0–5.7
2016 0/43 0 0–8.2
2017 1/81 1.2 0.03–6.7
2018 1/111 0.9 0.02–4.9
2019 2/60 3.33 0.4–11.5
2020 0/18 0 0–18.5
Origin 18.08 0.26
Bałtów 0/7 0 0–41.0
Białowieża Forest 3/173 1.7 0.4–5.0
Bieszczady Mountains 0/38 0 0–9.2
Gołuchów 0/11 0 0–28.5
Kiermusy 0/5 0 0–52.2
Międzyzdroje 0/5 0 0–52.2
Niepołomice 0/22 0 0–15.4
Pszczyna 0/45 0 0–7.9
Borecka Forest 1/42 2.3 0.06–12.6
Knyszyńska Forest 0/62 0 0–5.8
Smardzewice 1/14 7.1 0.2–33.9
Ustroń 0/2 0 0–84.2
Bydgoszcz Zoo 0/1 0 0–97.5
Łódź Zoo 0/3 0 0–70.7
Warsaw Zoo 0/6 0 0–45.9
Population type 0.11 0.736
free-ranging 2/207 0.9 0.1–3.4
captive 3/229 1.3 0.3–3.7
Sanitary status 0.45 0.93
potentially healthy (immobilised) 3/269 1.1 0.1–3.2
eliminated 2/138 1.4 0.2–5.1
fallen 0/20 0 0–16.8
killed in accidents 0/9 0 0–33.6
Sex 0.49 0.48
XX 2/242 0.8 0.1–2.9
XY 3/194 1.5 0.3–4.4
Age group 3.18 0.20
calves (≤1 year) 1/66 1.5 0.03–8.1
juveniles (2–3 years) 0/161 0 0–2.2
adults (≥4 years) 4/199 2.0 0.5–5.1
no data 0/10 0 0–30.8

List of Mycobacterium bovis ELISA-positive samples among 436 serum samples collected from European bison from 15 different Polish populations

No. Year of sampling Date of sampling (dd/mm) Animal Year of birth Age Sex Sanitary status Origin Population type S/P value
1 2019 21/02 B 2018 7 mo XY culled Białowieża Forest free-ranging 2.311
2 2013 21/11 A 2001 12 yrs XY immobilised Białowieża Forest captive 0.477
3 2018 24/10 E 2013 5 yrs XX immobilised Białowieża Forest captive 0.530
4 2019 23/02 C 2012 7 yrs XY immobilised Borecka Forest free-ranging 1.068
5 2018 11/12 D 2008 10 yrs XX culled Smardzewice captive 11.671
6 2016 01/02 D 2008 8 yrs XX immobilised Smardzewice captive 1.240
7 2016 14/11 D 2008 8 yrs XX immobilised Smardzewice captive 3.891
8 2017 18/09 D 2008 9 yrs XX immobilised Smardzewice captive 4.137
9 2018 22/05 D 2008 10 yrs XX immobilised Smardzewice captive 4.365

Detailed sensitivity and specificity for each cut-off value of M. bovis antibody ELISA against a combined tuberculin skin test and interferon -gamma release assay (TST+IGRA)

Cut-off Sensitivity (%) Specificity (%) Correctly classified (%) LR+ LR−
≥0.124 100.00 0.00 39.39 1.0000
≥0.120 100.00 5.00 42.42 1.0526 0.0000
≥0.111 100.00 10.00 45.45 1.1111 0.0000
≥0.103 100.00 15.00 48.48 1.1765 0.0000
≥0.080 92.31 20.00 48.48 1.1538 0.3846
≥0.079 92.31 30.00 54.55 1.3187 0.2564
≥0.075 92.31 40.00 60.61 1.5385 0.1923
≥0.075 84.62 40.00 57.58 1.4103 0.3846
≥0.074 84.62 45.00 60.61 1.5385 0.3419
≥0.068 84.62 50.00 63.64 1.6923 0.3077
≥0.066 84.62 55.00 66.67 1.8803 0.2797
≥0.060 84.62 60.00 69.70 2.1154 0.2564
≥0.050 84.62 65.00 72.73 2.4176 0.2367
≥0.039 84.62 70.00 75.76 2.8205 0.2198
≥0.033 76.92 70.00 72.73 2.5641 0.3297
≥0.030 76.92 75.00 75.76 3.0769 0.3077
≥0.027 76.92 80.00 78.79 3.8462 0.2885
≥0.019 76.92 85.00 81.82 5.1282 0.2715
≥0.016 76.92 90.00 84.85 7.6923 0.2564
≥0.012 76.92 95.00 87.88 15.3846 0.2429
≥0.012 69.23 95.00 84.85 13.8462 0.3239
≥0.002 69.23 100.00 87.88 0.3077
≥0.099 61.54 100.00 84.85 0.3846
≥0.125 53.85 100.00 81.82 0.4615
≥0.165 46.15 100.00 78.79 0.5385
≥1.240 38.46 100.00 75.76 0.6154
≥3.890 30.77 100.00 72.73 0.6923
≥4.137 23.08 100.00 69.70 0.7692
≥4.364 15.38 100.00 66.67 0.8462
≥11.670 >11.670 7.69 0.00 100.00 100.00 63.64 60.61 0.9231 1.0000
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