Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany
Abstract
:1. Introduction
2. Results
2.1. Small Mammal Trapping
2.2. TBEV Seroprevalence in Small Mammals
2.3. Movement Profile of the Recaptured Small Mammals
3. Discussion
4. Materials and Methods
4.1. Study Area
4.2. Small Mammal Trapping and Sampling
4.3. Ethical Statement
4.4. Serological Analysis
4.4.1. Indirect Immunofluorescence Assay (IIFA)
4.4.2. Serum Neutralization Test (SNT)
4.5. Statistical Analysis
4.5.1. Definition
4.5.2. Statistical Analyses of TBEV Seroprevalence in Small Mammals
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Haselmuehl | Heselbach | ||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Clethrionomys glareolus | Apodemus flavicollis | Clethrionomys glareolus | Apodemus flavicollis | ||||||||||||||
Year | Season | NTR | Seropos. (Seropos./ Sampled Rodents | RF (%) | NTR | Seropos. (Seropos./ Sampled Rodents | RF (%) | NTR | Seropos. (Seropos./ Sampled Rodents | RF (%) | NTR | Seropos. (Seropos./ Sampled Rodents | RF (%) | ||||
Y | S | Y | S | Y | S | Y | S | ||||||||||
2019 | Spring | 34 | 7/30 | 21.3 | 23.3 | 11 | 0/10 | 0 | 0 | 28 | 7/26 | 18.0 | 26.9 | 13 | 4/10 | 22.6 | 40.0 |
Summer | 72 | 14/59 | 23.7 | 12 | 0/11 | 0 | 49 | 5/32 | 15.6 | 38 | 8/33 | 24.2 | |||||
Autumn | 52 | 9/52 | 17.3 | 17 | 0/17 | 0 | 42 | 6/42 | 14.3 | 21 | 2/19 | 10.5 | |||||
2020 | Spring | 0 | 0/0 | 10.8 | 0 | 0 | 0/0 | 0 | 0 | 7 | 3/7 | 23.9 | 42.9 | 0 | 0/0 | 20.0 | 0 |
Summer | 19 | 2/19 | 10.5 | 5 | 0/5 | 0 | 49 | 14/44 | 31.8 | 11 | 3/11 | 27.3 | |||||
Autumn | 19 | 2/18 | 11.1 | 3 | 0/2 | 0 | 41 | 5/41 | 12.2 | 4 | 0/4 | 0 | |||||
2021 | Spring | 2 | 0/2 | 17.6 | 0 | 0 | 0/0 | 5.6 | 0 | 11 | 4/11 | 18.8 | 36.4 | 0 | 0/0 | 0 | 0 |
Summer | 2 | 1/2 | 50.0 | 1 | 0/1 | 0 | 22 | 3/22 | 13.6 | 11 | 0/11 | 0 | |||||
Autumn | 13 | 2/13 | 15.4 | 17 | 1/17 | 5.9 | 15 | 2/15 | 13.3 | 16 | 0/16 | 0 | |||||
2022 | Spring | 6 | 0/6 | 33.3 | 0 | 0 | 0/0 | 0 | 0 | 3 | 0/3 | 0 | 0 | 1 | 0/1 | 7.7 | 0 |
Summer | 9 | 5/9 | 55.6 | 1 | 0/1 | 0 | 6 | 0/6 | 0 | 11 | 1/11 | 9.1 | |||||
Autumn | 0 | 0/0 | 0 | 0 | 0/0 | 0 | 11 | 0/11 | 0 | 1 | 0/1 | 0 | |||||
Total | 228 | 42/210 | 20.0 | 67 | 1/64 | 1.6 | 284 | 49/260 | 18.8 | 127 | 18/117 | 15.4 |
Factor | Estimate | Std. Error | z-Value | p-Value |
---|---|---|---|---|
Total | ||||
Intercept | −2.9372 | 0.3989 | −7.363 | 1.8 × 10-13 *** |
A. flavicollis v. Cl. glareolus | 1.0603 | 0.3037 | 3.491 | 0.000481 *** |
Autumn v. spring | 0.6671 | 0.3517 | 1.897 | 0.057849 . |
Autumn v. summer | 0.6463 | 0.2745 | 2.355 | 0.018545 * |
Haselmuehl v. Heselbach | 0.2883 | 0.2356 | 1.224 | 0.221094 |
2019 v. 2020 | −0.1045 | 0.2798 | −0.374 | 0.708743 |
2019 v. 2021 | −0.5708 | 0.3552 | −1.607 | 0.108080 |
2019 v. 2022 | −0.7571 | 0.4762 | −1.590 | 0.111845 |
Adult v. juvenile | −0.6716 | 0.3426 | −1.960 | 0.049969 * |
Female v. male | 0.8102 | 0.2509 | 3.229 | 0.001240 ** |
Haselmuehl | ||||
Intercept | −5.88806 | 1.16148 | −5.069 | 3.99 × 10−7 *** |
Autumn v. spring | 0.04609 | 0.58515 | 0.079 | 0.93722 |
Autumn v. summer | 0.54246 | 0.43445 | 1.249 | 0.21181 |
A. flavicollis v. Cl. glareolus | 3.44187 | 1.05740 | 3.255 | 0.00113 ** |
2019 v. 2020 | −0.65451 | 0.61951 | −1.056 | 0.29074 |
2019 v. 2021 | 0.51385 | 0.66947 | 0.768 | 0.44276 |
2019 v. 2022 | 0.09561 | 0.68152 | 0.140 | 0.88843 |
Adult v. juvenile | 0.41223 | 0.51703 | 0.797 | 0.42528 |
Female v. male | 2.11164 | 0.47819 | 4.416 | 1.01 × 10−5 *** |
Heselbach | ||||
Intercept | −1.73161 | 0.49816 | −3.476 | 0.000509 *** |
Autumn v. spring | 1.30624 | 0.44224 | 2.954 | 0.003140 ** |
Autumn v. summer | 0.81817 | 0.37229 | 2.198 | 0.027974 * |
A. flavicollis v. Cl. glareolus | 0.28740 | 0.34491 | 0.833 | 0.404698 |
2019 v. 2020 | 0.23872 | 0.35038 | 0.681 | 0.495677 |
2019 v. 2021 | −0.78207 | 0.43313 | −1.806 | 0.070976 |
2019 v. 2022 | −2.01711 | 1.04650 | −1.927 | 0.053920 . |
Adult v. juvenile | −1.31092 | 0.44867 | −2.922 | 0.003480 ** |
Female v. male | 0.09002 | 0.31743 | 0.284 | 0.776736 |
Apodemus flavicollis | ||||
Intercept | −3.9593 | 1.1871 | −3.335 | 0.000852 *** |
Autumn v. spring | 1.4047 | 0.9242 | 1.520 | 0.128515 |
Autumn v. summer | 1.0298 | 0.7217 | 1.427 | 0.153607 |
Haselmuehl v. Heselbach | 2.7111 | 1.0687 | 2.537 | 0.011184 * |
2019 v. 2020 | −0.5673 | 0.7925 | −0.716 | 0.474066 |
2019 v. 2021 | −1.8405 | 1.1040 | −1.667 | 0.095504 |
2019 v. 2022 | −1.7362 | 1.1382 | −1.525 | 0.127161 |
Adult v. juvenile | −2.3298 | 1.1194 | −2.081 | 0.037411 * |
Female v. male | −1.2373 | 0.5951 | −2.079 | 0.037597 * |
Clethrionomys glareolus | ||||
Intercept | −1.935855 | 0.330835 | −5.851 | 4.87 × 10−9 *** |
Autumn v. spring | 0.524291 | 0.361727 | 1.449 | 0.1472 |
Autumn v. summer | 0.494920 | 0.288599 | 1.715 | 0.0864 |
Haselmuehl v. Heselbach | −0.084538 | 0.266944 | −0.317 | 0.7515 |
2019 v. 2020 | 0.001682 | 0.310668 | 0.005 | 0.9957 |
2019 v. 2021 | −0.268220 | 0.399430 | −0.672 | 0.5019 |
2019 v. 2022 | −0.796784 | 0.540969 | −1.473 | 0.1408 |
Female v. male | 1.363863 | 0.289338 | 4.714 | 2.43 × 10−6 *** |
TBEV Seropositive/Sampled Rodents | |||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Haselmuehl | Heselbach | ||||||||||||||||||
Clethrionomys glareolus | Apodemus flavicollis | Clethrionomys glareolus | Apodemus flavicollis | ||||||||||||||||
Year | Season | M | F | Juv. | M | F | Juv. | Total | Seropos. (%) | M | F | Juv. | M | F | Juv. | Total | Seropos. (%) | ||
Y | S | Y | S | ||||||||||||||||
2019 | Spring | 3/5 | 2/19 | 2/6 | 0/8 | 0/2 | 0/0 | 7/40 | 16.8 | 17.5 | 2/7 | 5/16 | 0/3 | 1/2 | 3/5 | 0/3 | 11/36 | 19.8 | 30.6 |
Summer | 9/15 | 2/17 | 3/27 | 0/7 | 0/4 | 0/0 | 14/70 | 20.0 | 3/5 | 0/11 | 2/16 | 3/18 | 4/8 | 1/7 | 13/65 | 20.0 | |||
Autumn | 3/13 | 1/14 | 5/25 | 0/8 | 0/8 | 0/1 | 9/69 | 13.0 | 1/6 | 3/12 | 2/24 | 2/10 | 0/6 | 0/3 | 8/61 | 13.1 | |||
2020 | Spring | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 9.1 | 0 | 1/4 | 0/0 | 2/3 | 0/0 | 0/0 | 0/0 | 3/7 | 23.4 | 42.9 |
Summer | 2/3 | 0/15 | 0/1 | 0/1 | 0/4 | 0/0 | 2/24 | 8.3 | 8/13 | 6/19 | 0/12 | 0/3 | 3/7 | 0/1 | 17/55 | 30.9 | |||
Autumn | 1/3 | 0/8 | 1/7 | 0/1 | 0/1 | 0/0 | 2/20 | 10.0 | 3/8 | 1/8 | 1/25 | 0/3 | 0/1 | 0/0 | 5/45 | 11.1 | |||
2021 | Spring | 0/0 | 0/0 | 0/2 | 0/0 | 0/0 | 0/0 | 0/2 | 11.4 | 0 | 0/5 | 4/6 | 0/0 | 0/0 | 0/0 | 0/0 | 4/11 | 12.0 | 36.4 |
Summer | 1/1 | 0/1 | 0/0 | 0/0 | 0/1 | 0/0 | 1/3 | 33.3 | 2/10 | 1/6 | 0/6 | 0/6 | 0/4 | 0/1 | 3/33 | 9.1 | |||
Autumn | 1/1 | 1/4 | 0/8 | 0/5 | 1/3 | 0/9 | 3/30 | 10.0 | 2/3 | 0/3 | 0/9 | 0/8 | 0/4 | 0/4 | 2/31 | 6.5 | |||
2022 | Spring | 0/4 | 0/2 | 0/0 | 0/0 | 0/0 | 0/0 | 0/6 | 31.3 | 0 | 0/2 | 0/1 | 0/0 | 0/0 | 0/1 | 0/0 | 0/4 | 3.0 | 0 |
Summer | 4/4 | 1/5 | 0/0 | 0/0 | 0/1 | 0/0 | 5/10 | 50.0 | 0/1 | 0/2 | 0/3 | 0/4 | 1/5 | 0/2 | 1/17 | 5.9 | |||
Autumn | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0 | 0/1 | 0/4 | 0/6 | 0/1 | 0/0 | 0/0 | 0/12 | 0 | |||
Total | 24/49 | 7/85 | 11/76 | 0/30 | 1/24 | 0/10 | 43/274 | 22/65 | 20/88 | 7/107 | 6/55 | 11/41 | 1/21 | 67/377 | |||||
Seropos. (%) | 49.0 | 8.2 | 14.5 | 0 | 4.2 | 0 | 15.7 | 33.8 | 22.7 | 6.5 | 10.9 | 26.8 | 4.8 | 17.8 |
ID | Species | Sex | First Capture | Second Capture | Third Capture | |||||
---|---|---|---|---|---|---|---|---|---|---|
Sample | IIFA | Days upon 2nd Capture | Sample | IIFA | Days upon 3rd Capture | Sample | IIFA | |||
Seroconversion | ||||||||||
35_Heb | Cl glareolus. | f | serum | neg. | 42 | serum | pos. | |||
26_Heb | Cl. glareolus | f | serum | neg. | 43 | lavage | pos. | |||
31_Heb | Cl. glareolus | f | serum | neg. | 42 | lavage | pos. | |||
220_Heb | Cl. glareolus | f | serum | neg. | 293 | serum | pos. | |||
169_Heb | A. flavicollis | m | serum | neg. | 59 | serum | pos. | |||
250_Heb | A. flavicollis | f | serum | neg. | 308 | lavage | pos. | |||
224_Heb | Cl. glareolus | f | serum | neg. | 47 | serum | neg. | 142 | serum | pos. |
194_Heb | Cl. glareolus | m | n.a. | n.a. | 23 | serum | neg. | 293 | serum | pos. |
222_Heb | Cl. glareolus | m | serum | neg. | 47 | serum | neg. | 246 | serum | pos. |
59_Ham | Cl. glareolus | m | serum | neg. | 48 | serum | pos. | 36 | serum | pos. |
297_Heb | Cl. glareolus | f | serum | neg. | 294 | serum | pos. | 37 | serum | pos. |
275_Heb | A. flavicollis | f | serum | neg. | 244 | serum | pos. | 20 | serum | pos. |
465_Ham | Cl. glareolus | m | serum | neg. | 62 | serum | pos. | 29 | serum | pos. |
Positive recaptured once | ||||||||||
20_Ham | Cl. glareolus | m | serum | pos. | 92 | serum | pos. | |||
21_Ham | Cl. glareolus | m | serum | pos. | 92 | serum | pos. | |||
146_Ham | Cl. glareolus | m | serum | pos. | 59 | serum | pos. | |||
84_Ham | Cl. glareolus | m | serum | pos. | 92 | serum | pos. | |||
105_Ham | Cl. glareolus | f | serum | pos. | 59 | serum | pos. | |||
232_Heb | Cl. glareolus | f | serum | pos. | 48 | serum | pos. | |||
388_Heb | Cl. glareolus | m | serum | pos. | 29 | serum | pos. | |||
426_Heb | Cl. glareolus | m | serum | pos. | 30 | serum | pos. | |||
290_Heb | Cl. glareolus | f | serum | pos. | 17 | serum | pos. | |||
261_Heb | Cl. glareolus | m | serum | pos. | 141 | serum | pos. | |||
283_Heb | Cl. glareolus | f | serum | pos. | 17 | lavage | pos. | |||
Positive recaptured twice | ||||||||||
16_Ham | Cl. glareolus | f | serum | pos. | 42 | n.a. | n.a. | 50 | serum | pos. |
9_Ham | Cl. glareolus | m | serum | pos. | 91 | serum | pos. | 36 | serum | pos. |
80_Heb | Cl. glareolus | m | serum | pos. | 33 | serum | pos. | 59 | serum | pos. |
232_Heb | Cl. glareolus | f | serum | pos. | 47 | serum | pos. | 142 | serum | pos. |
294_Heb | Cl. glareolus | m | serum | pos. | 15 | serum | pos. | 21 | serum | pos. |
305_Heb | Cl. glareolus | m | serum | pos. | 20 | serum | pos. | 36 | serum | pos. |
385_Heb | Cl. glareolus | f | serum | pos. | 36 | serum | pos. | 28 | serum | pos. |
77_Heb | A. flavicollis | f | serum | pos. | 33 | serum | pos. | 36 | serum | pos. |
Seropositive to seronegative captures | ||||||||||
189_Ham | Cl. glareolus | f | n.a. | n.a. | 23 | serum | pos. | 48 | serum | neg. |
136_Heb | A. flavicollis | m | serum | pos. | 36 | lavage | neg. | |||
69_Heb | A. flavicollis | m | serum | pos. | 16 | n.a. | n.a. | 91 | serum | neg. |
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Brandenburg, P.J.; Obiegala, A.; Schmuck, H.M.; Dobler, G.; Chitimia-Dobler, L.; Pfeffer, M. Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany. Pathogens 2023, 12, 185. https://doi.org/10.3390/pathogens12020185
Brandenburg PJ, Obiegala A, Schmuck HM, Dobler G, Chitimia-Dobler L, Pfeffer M. Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany. Pathogens. 2023; 12(2):185. https://doi.org/10.3390/pathogens12020185
Chicago/Turabian StyleBrandenburg, Philipp Johannes, Anna Obiegala, Hannah Maureen Schmuck, Gerhard Dobler, Lidia Chitimia-Dobler, and Martin Pfeffer. 2023. "Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany" Pathogens 12, no. 2: 185. https://doi.org/10.3390/pathogens12020185
APA StyleBrandenburg, P. J., Obiegala, A., Schmuck, H. M., Dobler, G., Chitimia-Dobler, L., & Pfeffer, M. (2023). Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany. Pathogens, 12(2), 185. https://doi.org/10.3390/pathogens12020185