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Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods

Year 2025, Volume: 72 Issue: 1, 9 - 21

Derya Altun , Halil Pir , Hakan Yardımcı

https://doi.org/10.33988/auvfd.1374292

Abstract

This study aims to investigate the genotypic similarities between human and animal-originated isolates by spoligotyping and 24 loci MIRU-VNTR for molecular epidemiological analysis of Mycobacterium bovis isolates. In this study, isolates were obtained between 2019 and 2022 from 58 humans and 50 bovines. Initially identified with the GenoType MTBC kit, all isolates were genotyped using spoligotyping and 24 loci Mycobacterial Interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods and their lineage relationships were illustrated in the dendrogram. When subjected to the spoligotyping method, the human and animal-originated isolates were revealed eight distinct clusters and 29 different genotypes. Notably the most prevalent genotypes were SIT1118/SB0989 (19.23%), SIT482/SB0120 (16.35%), SIT685/SB0288 (12.5%) detected in both human and animal-originated isolates. SB1593 (12.5%) was exclusively identified in animal-originated isolates. Additional genotypes included SIT3529/SB0920, SIT1185/SB0897, SIT3710/SB1595, SIT688/SB0129, SIT3687/SB1625, SB0419, SB2466, SB1231, and SB2510. MIRU-VNTR analysis resulted in nine distinct clusters and 55 different genotypes. ETR-C, QUB2163b, QUB26, and Mtub04 exhibited the highest allelic diversity, while MIRU02, MIRU20, MIRU24, MIRU27, and MIRU39 did not display allelic diversity. When the molecular typing results of the 95 isolates, tested with all three methods, 93.7 % agreement was observed between methods. In conclusion, it was determined that both tests could be safely employed. The presence of similar genotypes in humans and animals underscores the potential zoonotic transmission of Mycobacterium bovis.

Keywords

Epidemiology Genotyping MIRU-VNTR Mycobacterium bovis Spoligotyping

Ethical Statement

Etik Kurul onayı gerekli değildir. TİTCK izni gerekli değildir.

Supporting Institution

This project was supported by Ankara University BAP Coordinatorship with project code 21L0239012.

Project Number

21L0239012

Thanks

This study was derived from the PhD thesis of the first author. We would like to thank Prof. Dr. Mehmet AKAN (Department of Veterinary Microbiology, Ankara University) and Doç. Dr. Yasemin COŞGUN (National Virology Reference Laboratory, Public Health General Directorate) for their valuable contributions to the study.

References

  • Akdeşir E, Özyiğit MÖ, Kahraman MM (2018): Sığırlarda Mycobacterium bovis’in moleküler ve sito-histopatolojik tanı yöntemleri ile gösterilmesi ve sonuçlarının karşılaştırılması. Ankara Univ Vet Fak Derg, 66, 27-35.
  • Aranaz A, Lıébana E, Gómez-Mampaso E, et al (1999): Mycobacterium tuberculosis subsp. caprae subsp. nov.: a taxonomic study of a new member of the Mycobacterium tuberculosis complex isolated from goats in Spain. Int J Syst Bacteriol, 49, 1263-1273.
  • Aslan G, Kuyucu N, Çalıkoğlu M, et al (2009): Mycobacterium bovis’in etken olduğu tüberküloz olguları. ANKEM Derg, 23, 182-187.
  • Avsever ML, Çavuşoğlu C, Yazıcıoğlu Ö, et al (2017): New spoligotyping pattern of Mycobacterium bovis isolates from farm animals in Turkey. Ankara Univ Vet Fak Derg, 64, 37-43.
  • Avsever M, Çavuşoğlu C, Çamkerten I (2020): First isolation of Mycobacterium bovis SIT 482 BOV from beef cattle in Turkey. Journal of the Hellenic Veterinary Medical Society, 71, 2279–2282.
  • Belakehal F, Barth SA, Menge C, et al (2022): Evaluation of the discriminatory power of spoligotyping and 19-locus mycobacterial interspersed repetitive unit-variable number of tandem repeat analysis (MIRU-VNTR) of Mycobacterium bovis strains isolated from cattle in Algeria. PLoS One, 17, e0262390.
  • Bolado- Martínez E, Benavides-Dávila I, Candia-Plata Mdel C, et al (2015): Proposal of a screening MIRU-VNTR panel for the preliminary genotyping of Mycobacterium bovis in Mexico. Biomed Res Int, 2015, 416479.
  • Cadmus S, Akinseye VO, van Soolingen D (2019): Mycobacterium bovis in humans and M. tuberculosis in animals in Nigeria: an overview from 1975-2014. Int J Tuberc Lung Dis, 23, 1162-1170.
  • Cinoğlu H (2021): Adıyaman ilinde tüberküloz şüphesi olan sığırlarda Mycobacterium bovis varlığının araştırılması ve epidemiyolojik tiplendirilmesi. Yüksek Lisans Tezi.
  • Collins DM (2011): Advances in molecular diagnostics for Mycobacterium bovis. Vet Microbiol, 151, 2–7.
  • Çavuşoğlu C, Yılmaz FF (2017): Ege Bölgesi’nde insan Mycobacterium bovis enfeksiyonlarının moleküler epidemiyolojisi. Mikrobiyoloji Bülteni, 51, 165-170.
  • Dibaba AB, Kriek NPJ, Thoen CO (2019): Tuberculosis in Animals: An African Perspective. Cham: Springer.
  • Gagneux S (2012): Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci, 367, 850-859.
  • Gülcü Y, Hadımlı HH (2020): Typing of Mycobacterium bovis isolates from cattle using MIRU-VNTR analysis. Etlik Veteriner Mikrobiyoloji Dergisi, 31, 133-139.
  • Kremer K, Glynn JR, Lillebaek T, et al (2004): Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J Clin Microbiol, 42, 4040-4049.
  • Melo EH, Gomes HM, Suffys PN, et al (2021): Genotypic characterization of Mycobacterium bovis Isolates from dairy cattle diagnosed with clinical tuberculosis. Front Vet Sci, 8, 747226.
  • OIE WOAH (2023): Bovine tuberculosis. Available at https://www.oie.int/en/what-we-do/animal-health-and-welfare/animal-diseases/old-classification-of-diseases-notifiable-to-the-oie-list-b (Accessed October 5, 2023).
  • Oruene IS, Ndukwe SC (2020): An assessment of meat inspection for bovine tuberculosis and the functional conditions of major abattoirs/ slaughter slabs in rivers state. Black Sea Journal of Agriculture, 3, 205-210.
  • Parreiras PM, Andrade GI, Nascimento Tde F, et al (2012): Spoligotyping and variable number tandem repeat analysis of Mycobacterium bovis isolates from cattle in Brazil. Mem Inst Oswaldo Cruz, 107, 64-73.
  • Prodinger WM, Indra A, Koksalan OK, et al (2014): Mycobacterium caprae infection in humans. Expert Rev Anti Infect Ther, 12, 1501-1513.
  • Sahraoui N, Müller B, Guetarni D, et al (2009): Molecular characterization of Mycobacterium bovis strains isolated from cattle slaughtered at two abattoirs in Algeria. BMC Vet Res, 5, 4.
  • Sayın Z, Erganiş O (2011): Identification of Mycobacterium strains by PCR and PCR-REA. Bull Vet Inst Pulawy, 55, 641-644.
  • Supply P, Allix C, Lesjean S, et al (2006): Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol, 44, 4498–4510.
  • Thoen CO, Steele JH, Gilsdorf MJ (2006): Mycobacterium bovis infection in animals and humans. 2nd Edition. Ames, Iowa: Wiley-Blackwell; London: Eurospan.
  • Thoen CO, Steele JH, Kaneene JB (2014): Zoonotic tuberculosis: Mycobacterium bovis and other pathogenic mycobacteria. 3rd Edition. Ames, Iowa: Wiley-Blackwell.
  • Tuzcu N, Köksal F (2020): Genetic evaluation of Mycobacterium bovis isolates with MIRU-VNTR and spoligotyping. Turkish Journal of Medical Sciences, 50, 2017-2023.
  • UTTR (2014): Türkiye Halk Sağlığı Kurumu, Sağlık Bakanlığı Yayın No: 935, Ankara.
  • Wei CY, Hsu YH, Chou WJ, et al (2004): Molecular and histopathologic evidence for systetmic infection by Mycobacterium bovis in a patient with tuberculous enteritis, peritonitis, and meningitis: a case report. The Kaohsiung Journal of Medical Sciences, 20, 302–307.
  • WHO Global TB Report (2020): Geneva, Switzerland. Available at https://www.who.int/publications/i/item/ 9789240013131 (Accessed October 5, 2023).
  • Yardımcı H, Ünal CB, Ataseven LK, et al (2007): Sığır tüberkülozunun PCR ile tanısı ve Mycobacterium bovis’in spoligotiplendirme yöntemi ile genotiplendirilmesi. Ankara Univ Vet Fak Derg, 54, 183-189.

Year 2025, Volume: 72 Issue: 1, 9 - 21

Derya Altun , Halil Pir , Hakan Yardımcı

https://doi.org/10.33988/auvfd.1374292

Abstract

Project Number

21L0239012

References

  • Akdeşir E, Özyiğit MÖ, Kahraman MM (2018): Sığırlarda Mycobacterium bovis’in moleküler ve sito-histopatolojik tanı yöntemleri ile gösterilmesi ve sonuçlarının karşılaştırılması. Ankara Univ Vet Fak Derg, 66, 27-35.
  • Aranaz A, Lıébana E, Gómez-Mampaso E, et al (1999): Mycobacterium tuberculosis subsp. caprae subsp. nov.: a taxonomic study of a new member of the Mycobacterium tuberculosis complex isolated from goats in Spain. Int J Syst Bacteriol, 49, 1263-1273.
  • Aslan G, Kuyucu N, Çalıkoğlu M, et al (2009): Mycobacterium bovis’in etken olduğu tüberküloz olguları. ANKEM Derg, 23, 182-187.
  • Avsever ML, Çavuşoğlu C, Yazıcıoğlu Ö, et al (2017): New spoligotyping pattern of Mycobacterium bovis isolates from farm animals in Turkey. Ankara Univ Vet Fak Derg, 64, 37-43.
  • Avsever M, Çavuşoğlu C, Çamkerten I (2020): First isolation of Mycobacterium bovis SIT 482 BOV from beef cattle in Turkey. Journal of the Hellenic Veterinary Medical Society, 71, 2279–2282.
  • Belakehal F, Barth SA, Menge C, et al (2022): Evaluation of the discriminatory power of spoligotyping and 19-locus mycobacterial interspersed repetitive unit-variable number of tandem repeat analysis (MIRU-VNTR) of Mycobacterium bovis strains isolated from cattle in Algeria. PLoS One, 17, e0262390.
  • Bolado- Martínez E, Benavides-Dávila I, Candia-Plata Mdel C, et al (2015): Proposal of a screening MIRU-VNTR panel for the preliminary genotyping of Mycobacterium bovis in Mexico. Biomed Res Int, 2015, 416479.
  • Cadmus S, Akinseye VO, van Soolingen D (2019): Mycobacterium bovis in humans and M. tuberculosis in animals in Nigeria: an overview from 1975-2014. Int J Tuberc Lung Dis, 23, 1162-1170.
  • Cinoğlu H (2021): Adıyaman ilinde tüberküloz şüphesi olan sığırlarda Mycobacterium bovis varlığının araştırılması ve epidemiyolojik tiplendirilmesi. Yüksek Lisans Tezi.
  • Collins DM (2011): Advances in molecular diagnostics for Mycobacterium bovis. Vet Microbiol, 151, 2–7.
  • Çavuşoğlu C, Yılmaz FF (2017): Ege Bölgesi’nde insan Mycobacterium bovis enfeksiyonlarının moleküler epidemiyolojisi. Mikrobiyoloji Bülteni, 51, 165-170.
  • Dibaba AB, Kriek NPJ, Thoen CO (2019): Tuberculosis in Animals: An African Perspective. Cham: Springer.
  • Gagneux S (2012): Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci, 367, 850-859.
  • Gülcü Y, Hadımlı HH (2020): Typing of Mycobacterium bovis isolates from cattle using MIRU-VNTR analysis. Etlik Veteriner Mikrobiyoloji Dergisi, 31, 133-139.
  • Kremer K, Glynn JR, Lillebaek T, et al (2004): Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J Clin Microbiol, 42, 4040-4049.
  • Melo EH, Gomes HM, Suffys PN, et al (2021): Genotypic characterization of Mycobacterium bovis Isolates from dairy cattle diagnosed with clinical tuberculosis. Front Vet Sci, 8, 747226.
  • OIE WOAH (2023): Bovine tuberculosis. Available at https://www.oie.int/en/what-we-do/animal-health-and-welfare/animal-diseases/old-classification-of-diseases-notifiable-to-the-oie-list-b (Accessed October 5, 2023).
  • Oruene IS, Ndukwe SC (2020): An assessment of meat inspection for bovine tuberculosis and the functional conditions of major abattoirs/ slaughter slabs in rivers state. Black Sea Journal of Agriculture, 3, 205-210.
  • Parreiras PM, Andrade GI, Nascimento Tde F, et al (2012): Spoligotyping and variable number tandem repeat analysis of Mycobacterium bovis isolates from cattle in Brazil. Mem Inst Oswaldo Cruz, 107, 64-73.
  • Prodinger WM, Indra A, Koksalan OK, et al (2014): Mycobacterium caprae infection in humans. Expert Rev Anti Infect Ther, 12, 1501-1513.
  • Sahraoui N, Müller B, Guetarni D, et al (2009): Molecular characterization of Mycobacterium bovis strains isolated from cattle slaughtered at two abattoirs in Algeria. BMC Vet Res, 5, 4.
  • Sayın Z, Erganiş O (2011): Identification of Mycobacterium strains by PCR and PCR-REA. Bull Vet Inst Pulawy, 55, 641-644.
  • Supply P, Allix C, Lesjean S, et al (2006): Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol, 44, 4498–4510.
  • Thoen CO, Steele JH, Gilsdorf MJ (2006): Mycobacterium bovis infection in animals and humans. 2nd Edition. Ames, Iowa: Wiley-Blackwell; London: Eurospan.
  • Thoen CO, Steele JH, Kaneene JB (2014): Zoonotic tuberculosis: Mycobacterium bovis and other pathogenic mycobacteria. 3rd Edition. Ames, Iowa: Wiley-Blackwell.
  • Tuzcu N, Köksal F (2020): Genetic evaluation of Mycobacterium bovis isolates with MIRU-VNTR and spoligotyping. Turkish Journal of Medical Sciences, 50, 2017-2023.
  • UTTR (2014): Türkiye Halk Sağlığı Kurumu, Sağlık Bakanlığı Yayın No: 935, Ankara.
  • Wei CY, Hsu YH, Chou WJ, et al (2004): Molecular and histopathologic evidence for systetmic infection by Mycobacterium bovis in a patient with tuberculous enteritis, peritonitis, and meningitis: a case report. The Kaohsiung Journal of Medical Sciences, 20, 302–307.
  • WHO Global TB Report (2020): Geneva, Switzerland. Available at https://www.who.int/publications/i/item/ 9789240013131 (Accessed October 5, 2023).
  • Yardımcı H, Ünal CB, Ataseven LK, et al (2007): Sığır tüberkülozunun PCR ile tanısı ve Mycobacterium bovis’in spoligotiplendirme yöntemi ile genotiplendirilmesi. Ankara Univ Vet Fak Derg, 54, 183-189.
There are 30 citations in total.

Details

Primary Language English
Subjects Veterinary Bacteriology, Veterinary Epidemiology, Veterinary Microbiology
Journal Section Research Article
Authors

Derya Altun 0000-0003-1603-0725

Halil Pir 0000-0001-9078-3122

Hakan Yardımcı 0000-0002-5994-5792

Project Number 21L0239012
Early Pub Date June 28, 2024
Publication Date
Submission Date October 13, 2023
Acceptance Date March 11, 2024
Published in Issue Year 2025Volume: 72 Issue: 1

Cite

APA Altun, D., Pir, H., & Yardımcı, H. (n.d.). Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 72(1), 9-21. https://doi.org/10.33988/auvfd.1374292
AMA Altun D, Pir H, Yardımcı H. Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods. Ankara Univ Vet Fak Derg. 72(1):9-21. doi:10.33988/auvfd.1374292
Chicago Altun, Derya, Halil Pir, and Hakan Yardımcı. “Epidemiological Analysis of Human and Animal Originated Mycobacterium Bovis Subspecies by Spoligotyping and Mycobacterial Interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) Methods”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72, no. 1 n.d.: 9-21. https://doi.org/10.33988/auvfd.1374292.
EndNote Altun D, Pir H, Yardımcı H Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72 1 9–21.
IEEE D. Altun, H. Pir, and H. Yardımcı, “Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods”, Ankara Univ Vet Fak Derg, vol. 72, no. 1, pp. 9–21, doi: 10.33988/auvfd.1374292.
ISNAD Altun, Derya et al. “Epidemiological Analysis of Human and Animal Originated Mycobacterium Bovis Subspecies by Spoligotyping and Mycobacterial Interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) Methods”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72/1 (n.d.), 9-21. https://doi.org/10.33988/auvfd.1374292.
JAMA Altun D, Pir H, Yardımcı H. Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods. Ankara Univ Vet Fak Derg.;72:9–21.
MLA Altun, Derya et al. “Epidemiological Analysis of Human and Animal Originated Mycobacterium Bovis Subspecies by Spoligotyping and Mycobacterial Interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) Methods”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 72, no. 1, pp. 9-21, doi:10.33988/auvfd.1374292.
Vancouver Altun D, Pir H, Yardımcı H. Epidemiological analysis of human and animal originated Mycobacterium bovis subspecies by spoligotyping and mycobacterial interspersed Repetitive Unit-Variable Number of Tandem Repeat (MIRU-VNTR) methods. Ankara Univ Vet Fak Derg. 72(1):9-21.
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