Investigation of Brucella spp. presence of amphibians collected from some regions in Türkiye
Year 2024,
Volume: 9 Issue: 2, 115 - 121, 22.08.2024
Kadir Akar
,
Ayfer Güllü Yücetepe
,
Gülseren Yıldız Öz
,
Emin Ayhan Baklan
,
Buket Eroğlu
,
Eray Atıl
,
Yaşar Tel
,
Oktay Keskin
,
Ahmet Murat Saytekin
,
Sevil Erdenlig Gürbilek
Abstract
Brucellosis is a zoonotic disease that causes economic losses in many countries worldwide, especially in livestock. Firstly, the African bullfrog and then B. inopinata and B. microti-like strains have been identified in various frog species worldwide. This study aimed to determine the presence of Brucella in amphibian frogs for the first time in Türkiye by bacteriological and molecular methods. Internal organ samples (spleen, liver, lung, kidney, etc.) of 150 frogs from different regions of Türkiye (Edirne/Ipsala (53 pieces), Adıyaman/Kâhta (97 pieces)) were used for the isolation of Brucella spp. As a result of Brucella genus-specific PCR (Polymerase Chain Reaction) and Multiplex PCR methods performed with these extracts, no positivity was detected in the frog samples taken from Edirne province, while in 4 of the frog samples taken from Adıyaman province, bands of approximately 250, 600, 700, 1000, 1500 and 3000 bp were observed in Multiplex PCR. Sphingomonas paucimobilis (S. paucimobilis) was identified by analysing the culture obtained from these samples with VITEK®2:Healtcare. As a result, the presence of Brucella spp. could not be detected both bacteriologically and molecularly in the study samples. However, observing similar multiple bands in multiplex PCR suggested that this bacterium and Brucella species are phylogenetically close. It was determined that S. paucimobilis, which belongs to the same class as Brucella species under the Alphaproteobacteria, may be dangerous for people who work on farms where frogs are raised for human consumption. This is because the bacteria can cause opportunistic infections, particularly in immunocompromised humans. Therefore, it may be imperative to take the appropriate precautions.
Ethical Statement
This research was approved by the Ethics Committee of Harran University Faculty of Veterinary Medicine (HRÜ-HADYEK, Ref No: 2020/007/01-2, Date: 25/12/2020).
Supporting Institution
This study covers some of the data of the projects titled "A Comprehensive Proteogenomic Analysis of Brucella for Understanding Epidemiology, Biology, Virulence Mechanisms and Host-Pathogen Interactions", 120N849 and 220N293, funded by TÜBİTAK-1071- Support Programme for Increasing the Capacity to Benefit from International Research Funds and Participation in International R&D Collaborations (ERA-NET/ICRAD Call).
Project Number
120N849 and 220N293
Thanks
We want to thank TUBITAK for their contribution to the realisation of the projects coded 120N849 and 220N293 and Dr Gamal WARETH for his contribution.
References
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- Amjadi, O., Rafiei, A., Mardani, M., Zafari, P., & Zarifian, A. (2019). A review of the immunopathogenesis of Brucellosis. Infectious Diseases, 51(5), 321–333. https://doi.org/10.1080/23744235.2019.1568545
- Aşkın, F. N., Erinmez, M., Ören, A. C., Manay, A. B., & Zer, Y. (2022). Sphingomonas paucimobilis outbreak a pediatric hematology-oncology hospital: Epidemiological investigation and literature review of an emerging healthcare-associated infection. Japanese Journal of Infectious Diseases, 75(4), 374–381. https://doi.org/10.7883/yoken.JJID.2021.661
- Baily, G. G., Krahn, J. B., Drasar, B. S., & Stoker, N. G. (1992). Detection of Brucella melitensis and Brucella abortus by DNA amplification. The Journal of Tropical Medicine and Hygiene, 95(4), 271–275.
- Buttigieg, S. C., Savic, S., Cauchi, D., Lautier, E., Canali, M., & Aragrande, M. (2018). Brucellosis control in Malta and Serbia: A one health evaluation. Frontiers in Veterinary Science, 5, 147. https://doi.org/10.3389/fvets.2018.00147
- Corbel, M. J., Nations, F. and A. O. of the U., Organization, W. H., & Health, W. O. for A. (2006). Brucellosis in humans and animals (WHO/CDS/EPR/2006.7). World Health Organization. https://apps.who.int/iris/handle/10665/43597
- Dökenel, G., & Özer, S. (2019). Bacterial agents isolated from cultured marsh frog (Pelophylax ridibundus, Pallas 1771). Ege Journal of Fisheries & Aquatic Sciences (EgeJFAS)/Su Ürünleri Dergisi, 36(2).
- Eisenberg, T., Hamann, H.-P., Kaim, U., Schlez, K., Seeger, H., Schauerte, N., Melzer, F., Tomaso, H., Scholz, H. C., Koylass, M. S., Whatmore, A. M., & Zschöck, M. (2012). Isolation of potentially novel Brucella spp. from frogs. Applied and Environmental Microbiology, 78(10), 3753–3755. https://doi.org/10.1128/AEM.07509-11
- El Beaino, M., Fares, J., Malek, A., & Hachem, R. (2018). Sphingomonas paucimobilis-related bone and soft-tissue infections: A systematic review. International Journal of Infectious Diseases, 77, 68–73. https://doi.org/10.1016/j.ijid.2018.09.021
- Fischer, D., Lorenz, N., Heuser, W., Kämpfer, P., Scholz, H. C., & Lierz, M. (2012). Abscesses associated with a Brucella inopinata-like bacterium in a big-eyed tree frog (Leptopelis vermiculatus). Journal of Zoo and Wildlife Medicine: Official Publication of the American Association of Zoo Veterinarians, 43(3), 625–628. https://doi.org/10.1638/2011-0005R2.1
- Godfroid, J., Cloeckaert, A., Liautard, J.-P., Kohler, S., Fretin, D., Walravens, K., Garin-Bastuji, B., & Letesson, J.-J. (2005). From the discovery of the Malta fever?s agent to the discovery of a marine mammal reservoir, brucellosis has continuously been a re-emerging zoonosis. Veterinary Research, 36(3), 313–326. https://doi.org/10.1051/vetres:2005003
- Göker, T., Aşık, R. Z., Yılmaz, M. B., Çelik, İ., & Tekiner, A. (2017). Sphingomonas Paucimobilis: A rare infectious agent found in cerebrospinal fluid. Journal of Korean Neurosurgical Society, 60(4), 481–483. https://doi.org/10.3340/jkns.2014.0102.004
- Gülçiçek, C. (2021). Ova kurbağası [Pelophylax Ridibundus (Pallas, 1771)] yetiştiriciliğinde değişik yem rasyonlarının gelişim hızına etkisi. [Yüksek Lisans Tezi, Eskişehir Teknik Üniversitesi].
- Gün, E., Ayaz, N., Uzun, H., Okur, M., Gönen, İ., Güneş, C., Soysal, Z., & Kocabay, K. (2014). A rare cause of nosocomial infections associated with Nephrolithiasis; Sphingomonas Paucimobilis. Journal of Pediatric Infection, 8(3), 125–127. https://doi.org/10.5152/ced.2013.47
- Hubálek, Z., Scholz, H. C., Sedláček, I., Melzer, F., Sanogo, Y. O., & Nesvadbová, J. (2007). Brucellosis of the Common Vole ( Microtus arvalis ). Vector-Borne and Zoonotic Diseases, 7(4), 679–688. https://doi.org/10.1089/vbz.2007.0143
- Jaÿ, M., Freddi, L., Mick, V., Durand, B., Girault, G., Perrot, L., Taunay, B., Vuilmet, T., Azam, D., Ponsart, C., & Zanella, G. (2020). Brucella microti‐ like prevalence in French farms producing frogs. Transboundary and Emerging Diseases, 67(2), 617–625. https://doi.org/10.1111/tbed.13377
- Jaý, M., Girault, G., Perrot, L., Taunay, B., Vuilmet, T., Rossignol, F., Pitel, P.-H., Picard, E., Ponsart, C., & Mick, V. (2018). Phenotypic and molecular characterization of Brucella microti-like bacteria from a fomestic Marsh frog (Pelophylax ridibundus). Frontiers in Veterinary Science, 5, 283. https://doi.org/10.3389/fvets.2018.00283
- Latheef, S., Keyburn, A., Broz, I., Bagnara, A., Bayley, C., Frith, S., & Dobson, E. (2020). Atypical Brucella sp in captive Australian green tree frogs ( Litoria caerulea ): Clinical features, pathology, culture and molecular characterization. Australian Veterinary Journal, 98(5), 216–221. https://doi.org/10.1111/avj.12925
- Leclercq, S. O., Cloeckaert, A., & Zygmunt, M. S. (2020). Taxonomic organization of the family Brucellaceae based on a phylogenomic approach. Frontiers in Microbiology, 10, 3083. https://doi.org/10.3389/fmicb.2019.03083
- Mayer-Scholl, A., Draeger, A., Göllner, C., Scholz, H. C., & Nöckler, K. (2010). Advancement of a multiplex PCR for the differentiation of all currently described Brucella species. Journal of Microbiological Methods, 80(1), 112–114. https://doi.org/10.1016/j.mimet.2009.10.015
- Mühldorfer, K., Wibbelt, G., Szentiks, C. A., Fischer, D., Scholz, H. C., Zschöck, M., & Eisenberg, T. (2017). The role of ‘atypical’ Brucella in amphibians: Are we facing novel emerging pathogens? Journal of Applied Microbiology, 122(1), 40–53. https://doi.org/10.1111/jam.13326
- Özeki̇nci̇, T., Habi̇p, Z., & Koçoğlu, M. E. (2022). 2014-2020 Yıllarında izole edilen Sphingomonas paucımobılıs suşlarının mikrobiyolojik açıdan değerlendirilmesi. Dicle Tıp Dergisi, 49(3), 486–490. https://doi.org/10.5798/dicletip.1170218
- Scholz, H. C., Hubalek, Z., Sedlacek, I., Vergnaud, G., Tomaso, H., Al Dahouk, S., Melzer, F., Kampfer, P., Neubauer, H., Cloeckaert, A., Maquart, M., Zygmunt, M. S., Whatmore, A. M., Falsen, E., Bahn, P., Gollner, C., Pfeffer, M., Huber, B., Busse, H.-J., & Nockler, K. (2008). Brucella microti sp. Nov., isolated from the common vole Microtus arvalis. Internatıonal Journal of Systematic and Evoluiıonary Microbiology, 58(2), 375–382. https://doi.org/10.1099/ijs.0.65356-0
- Scholz, H. C., Revilla-Fernández, S., Dahouk, S. A., Hammerl, J. A., Zygmunt, M. S., Cloeckaert, A., Koylass, M., Whatmore, A. M., Blom, J., Vergnaud, G., Witte, A., Aistleitner, K., & Hofer, E. (2016). Brucella vulpis sp. Nov., isolated from mandibular lymph nodes of red foxes (Vulpes vulpes). International Journal of Systematic and Evolutionary Microbiology, 66(5), 2090–2098. https://doi.org/10.1099/ijsem.0.000998
- Şimşek, E., Alkaya, A., Şereflişan, H., & Özyilmaz, A. (2022). Comparisons of biochemical compositions in marsh frog (Pelophylax ridibundus)(Anura; Ranidae) grown in different conditions; wild, semicultured and cultured ones. Turkish Journal of Zoology, 46(3), 261-269.
- Tai, M.L.S., & Velayuthan, R. D. (2014). Sphingomonas Paucimobilis: An unusual cause of meningitis—Case Report. Neurologia Medico-Chirurgica, 54(4), 337–340. https://doi.org/10.2176/nmc.cr2012-0429
- Walayat, S., Malik, A., Hussain, N., & Lynch, T. (2018). Sphingomonas paucimobilis presenting as acute phlebitis: A case report. IDCases, 11, 6–8. https://doi.org/10.1016/j.idcr.2017.11.006
- Whatmore, A. M., Dale, E., Stubberfield, E., Muchowski, J., Koylass, M., Dawson, C., Gopaul, K. K., Perrett, L. L., Jones, M., & Lawrie, A. (2015). Isolation of Brucella from a White’s tree frog (Litoria caerulea). JMM Case Reports, 2(1). https://doi.org/10.1099/jmmcr.0.000017
- Whatmore, A. M., Davison, N., Cloeckaert, A., Al Dahouk, S., Zygmunt, M. S., Brew, S. D., Perrett, L. L., Koylass, M. S., Vergnaud, G., Quance, C., Scholz, H. C., Dick, E. J., Hubbard, G., & Schlabritz-Loutsevitch, N. E. (2014). Brucella papionis sp. Nov., isolated from baboons (Papio spp.). International Journal of Systematic and Evolutionary Microbiology, 64(Pt_12), 4120–4128. https://doi.org/10.1099/ijs.0.065482-0
- Whatmore, A. M., Perrett, L. L., & MacMillan, A. P. (2007). Characterisation of the genetic diversity of Brucella by multilocus sequencing. BMC Microbiology, 7(1), 34. https://doi.org/10.1186/1471-2180-7-34
- World organisation for animal health Brucellosis (WOAH). (2022). Manual of diagnostic tests and vaccines for terrestrial animals. In Chapter 3.01.04: Brucellosis; OIE Listed 2021. Available online: https://www.oie.int/en/disease/brucellosis/.
- World organisation for animal health Brucellosis (WOAH). (2018). Manual of diagnostic tests and vaccines for terrestrial animals. In Chapter 3.01.04: Brucellosis; OIE: Paris, France. https://www.woah.org/en/produit/manual-of-diagnostic-tests-and-vaccines-for-terrestrial-animals-2018/.
Year 2024,
Volume: 9 Issue: 2, 115 - 121, 22.08.2024
Kadir Akar
,
Ayfer Güllü Yücetepe
,
Gülseren Yıldız Öz
,
Emin Ayhan Baklan
,
Buket Eroğlu
,
Eray Atıl
,
Yaşar Tel
,
Oktay Keskin
,
Ahmet Murat Saytekin
,
Sevil Erdenlig Gürbilek
Project Number
120N849 and 220N293
References
- Alton, G. G., Jones, L. M., Angus, R. D., & Verger, J. M. (1988). Techniques for the brucellosis laboratory. INRA.
- Amjadi, O., Rafiei, A., Mardani, M., Zafari, P., & Zarifian, A. (2019). A review of the immunopathogenesis of Brucellosis. Infectious Diseases, 51(5), 321–333. https://doi.org/10.1080/23744235.2019.1568545
- Aşkın, F. N., Erinmez, M., Ören, A. C., Manay, A. B., & Zer, Y. (2022). Sphingomonas paucimobilis outbreak a pediatric hematology-oncology hospital: Epidemiological investigation and literature review of an emerging healthcare-associated infection. Japanese Journal of Infectious Diseases, 75(4), 374–381. https://doi.org/10.7883/yoken.JJID.2021.661
- Baily, G. G., Krahn, J. B., Drasar, B. S., & Stoker, N. G. (1992). Detection of Brucella melitensis and Brucella abortus by DNA amplification. The Journal of Tropical Medicine and Hygiene, 95(4), 271–275.
- Buttigieg, S. C., Savic, S., Cauchi, D., Lautier, E., Canali, M., & Aragrande, M. (2018). Brucellosis control in Malta and Serbia: A one health evaluation. Frontiers in Veterinary Science, 5, 147. https://doi.org/10.3389/fvets.2018.00147
- Corbel, M. J., Nations, F. and A. O. of the U., Organization, W. H., & Health, W. O. for A. (2006). Brucellosis in humans and animals (WHO/CDS/EPR/2006.7). World Health Organization. https://apps.who.int/iris/handle/10665/43597
- Dökenel, G., & Özer, S. (2019). Bacterial agents isolated from cultured marsh frog (Pelophylax ridibundus, Pallas 1771). Ege Journal of Fisheries & Aquatic Sciences (EgeJFAS)/Su Ürünleri Dergisi, 36(2).
- Eisenberg, T., Hamann, H.-P., Kaim, U., Schlez, K., Seeger, H., Schauerte, N., Melzer, F., Tomaso, H., Scholz, H. C., Koylass, M. S., Whatmore, A. M., & Zschöck, M. (2012). Isolation of potentially novel Brucella spp. from frogs. Applied and Environmental Microbiology, 78(10), 3753–3755. https://doi.org/10.1128/AEM.07509-11
- El Beaino, M., Fares, J., Malek, A., & Hachem, R. (2018). Sphingomonas paucimobilis-related bone and soft-tissue infections: A systematic review. International Journal of Infectious Diseases, 77, 68–73. https://doi.org/10.1016/j.ijid.2018.09.021
- Fischer, D., Lorenz, N., Heuser, W., Kämpfer, P., Scholz, H. C., & Lierz, M. (2012). Abscesses associated with a Brucella inopinata-like bacterium in a big-eyed tree frog (Leptopelis vermiculatus). Journal of Zoo and Wildlife Medicine: Official Publication of the American Association of Zoo Veterinarians, 43(3), 625–628. https://doi.org/10.1638/2011-0005R2.1
- Godfroid, J., Cloeckaert, A., Liautard, J.-P., Kohler, S., Fretin, D., Walravens, K., Garin-Bastuji, B., & Letesson, J.-J. (2005). From the discovery of the Malta fever?s agent to the discovery of a marine mammal reservoir, brucellosis has continuously been a re-emerging zoonosis. Veterinary Research, 36(3), 313–326. https://doi.org/10.1051/vetres:2005003
- Göker, T., Aşık, R. Z., Yılmaz, M. B., Çelik, İ., & Tekiner, A. (2017). Sphingomonas Paucimobilis: A rare infectious agent found in cerebrospinal fluid. Journal of Korean Neurosurgical Society, 60(4), 481–483. https://doi.org/10.3340/jkns.2014.0102.004
- Gülçiçek, C. (2021). Ova kurbağası [Pelophylax Ridibundus (Pallas, 1771)] yetiştiriciliğinde değişik yem rasyonlarının gelişim hızına etkisi. [Yüksek Lisans Tezi, Eskişehir Teknik Üniversitesi].
- Gün, E., Ayaz, N., Uzun, H., Okur, M., Gönen, İ., Güneş, C., Soysal, Z., & Kocabay, K. (2014). A rare cause of nosocomial infections associated with Nephrolithiasis; Sphingomonas Paucimobilis. Journal of Pediatric Infection, 8(3), 125–127. https://doi.org/10.5152/ced.2013.47
- Hubálek, Z., Scholz, H. C., Sedláček, I., Melzer, F., Sanogo, Y. O., & Nesvadbová, J. (2007). Brucellosis of the Common Vole ( Microtus arvalis ). Vector-Borne and Zoonotic Diseases, 7(4), 679–688. https://doi.org/10.1089/vbz.2007.0143
- Jaÿ, M., Freddi, L., Mick, V., Durand, B., Girault, G., Perrot, L., Taunay, B., Vuilmet, T., Azam, D., Ponsart, C., & Zanella, G. (2020). Brucella microti‐ like prevalence in French farms producing frogs. Transboundary and Emerging Diseases, 67(2), 617–625. https://doi.org/10.1111/tbed.13377
- Jaý, M., Girault, G., Perrot, L., Taunay, B., Vuilmet, T., Rossignol, F., Pitel, P.-H., Picard, E., Ponsart, C., & Mick, V. (2018). Phenotypic and molecular characterization of Brucella microti-like bacteria from a fomestic Marsh frog (Pelophylax ridibundus). Frontiers in Veterinary Science, 5, 283. https://doi.org/10.3389/fvets.2018.00283
- Latheef, S., Keyburn, A., Broz, I., Bagnara, A., Bayley, C., Frith, S., & Dobson, E. (2020). Atypical Brucella sp in captive Australian green tree frogs ( Litoria caerulea ): Clinical features, pathology, culture and molecular characterization. Australian Veterinary Journal, 98(5), 216–221. https://doi.org/10.1111/avj.12925
- Leclercq, S. O., Cloeckaert, A., & Zygmunt, M. S. (2020). Taxonomic organization of the family Brucellaceae based on a phylogenomic approach. Frontiers in Microbiology, 10, 3083. https://doi.org/10.3389/fmicb.2019.03083
- Mayer-Scholl, A., Draeger, A., Göllner, C., Scholz, H. C., & Nöckler, K. (2010). Advancement of a multiplex PCR for the differentiation of all currently described Brucella species. Journal of Microbiological Methods, 80(1), 112–114. https://doi.org/10.1016/j.mimet.2009.10.015
- Mühldorfer, K., Wibbelt, G., Szentiks, C. A., Fischer, D., Scholz, H. C., Zschöck, M., & Eisenberg, T. (2017). The role of ‘atypical’ Brucella in amphibians: Are we facing novel emerging pathogens? Journal of Applied Microbiology, 122(1), 40–53. https://doi.org/10.1111/jam.13326
- Özeki̇nci̇, T., Habi̇p, Z., & Koçoğlu, M. E. (2022). 2014-2020 Yıllarında izole edilen Sphingomonas paucımobılıs suşlarının mikrobiyolojik açıdan değerlendirilmesi. Dicle Tıp Dergisi, 49(3), 486–490. https://doi.org/10.5798/dicletip.1170218
- Scholz, H. C., Hubalek, Z., Sedlacek, I., Vergnaud, G., Tomaso, H., Al Dahouk, S., Melzer, F., Kampfer, P., Neubauer, H., Cloeckaert, A., Maquart, M., Zygmunt, M. S., Whatmore, A. M., Falsen, E., Bahn, P., Gollner, C., Pfeffer, M., Huber, B., Busse, H.-J., & Nockler, K. (2008). Brucella microti sp. Nov., isolated from the common vole Microtus arvalis. Internatıonal Journal of Systematic and Evoluiıonary Microbiology, 58(2), 375–382. https://doi.org/10.1099/ijs.0.65356-0
- Scholz, H. C., Revilla-Fernández, S., Dahouk, S. A., Hammerl, J. A., Zygmunt, M. S., Cloeckaert, A., Koylass, M., Whatmore, A. M., Blom, J., Vergnaud, G., Witte, A., Aistleitner, K., & Hofer, E. (2016). Brucella vulpis sp. Nov., isolated from mandibular lymph nodes of red foxes (Vulpes vulpes). International Journal of Systematic and Evolutionary Microbiology, 66(5), 2090–2098. https://doi.org/10.1099/ijsem.0.000998
- Şimşek, E., Alkaya, A., Şereflişan, H., & Özyilmaz, A. (2022). Comparisons of biochemical compositions in marsh frog (Pelophylax ridibundus)(Anura; Ranidae) grown in different conditions; wild, semicultured and cultured ones. Turkish Journal of Zoology, 46(3), 261-269.
- Tai, M.L.S., & Velayuthan, R. D. (2014). Sphingomonas Paucimobilis: An unusual cause of meningitis—Case Report. Neurologia Medico-Chirurgica, 54(4), 337–340. https://doi.org/10.2176/nmc.cr2012-0429
- Walayat, S., Malik, A., Hussain, N., & Lynch, T. (2018). Sphingomonas paucimobilis presenting as acute phlebitis: A case report. IDCases, 11, 6–8. https://doi.org/10.1016/j.idcr.2017.11.006
- Whatmore, A. M., Dale, E., Stubberfield, E., Muchowski, J., Koylass, M., Dawson, C., Gopaul, K. K., Perrett, L. L., Jones, M., & Lawrie, A. (2015). Isolation of Brucella from a White’s tree frog (Litoria caerulea). JMM Case Reports, 2(1). https://doi.org/10.1099/jmmcr.0.000017
- Whatmore, A. M., Davison, N., Cloeckaert, A., Al Dahouk, S., Zygmunt, M. S., Brew, S. D., Perrett, L. L., Koylass, M. S., Vergnaud, G., Quance, C., Scholz, H. C., Dick, E. J., Hubbard, G., & Schlabritz-Loutsevitch, N. E. (2014). Brucella papionis sp. Nov., isolated from baboons (Papio spp.). International Journal of Systematic and Evolutionary Microbiology, 64(Pt_12), 4120–4128. https://doi.org/10.1099/ijs.0.065482-0
- Whatmore, A. M., Perrett, L. L., & MacMillan, A. P. (2007). Characterisation of the genetic diversity of Brucella by multilocus sequencing. BMC Microbiology, 7(1), 34. https://doi.org/10.1186/1471-2180-7-34
- World organisation for animal health Brucellosis (WOAH). (2022). Manual of diagnostic tests and vaccines for terrestrial animals. In Chapter 3.01.04: Brucellosis; OIE Listed 2021. Available online: https://www.oie.int/en/disease/brucellosis/.
- World organisation for animal health Brucellosis (WOAH). (2018). Manual of diagnostic tests and vaccines for terrestrial animals. In Chapter 3.01.04: Brucellosis; OIE: Paris, France. https://www.woah.org/en/produit/manual-of-diagnostic-tests-and-vaccines-for-terrestrial-animals-2018/.