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Incidence and Drug Resistance of Zoonotic Mycobacterium bovis Infection in Peshawar, Pakistan

  • Irfan Khattak
  • Muhammad Hassan Mushtaq
  • Sultan Ayaz
  • Sajid Ali
  • Anwar Sheed
  • Javed Muhammad
  • Muhammad Luqman Sohail
  • Haq Amanullah
  • Irshad Ahmad
  • Sadeeq ur Rahman
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1057)

Abstract

Prevalence of zoonotic Mycobacterium bovis (bTB) disease in human population is underreported from the North of Pakistan. Here, we report on the proportion of human bTB disease among the overall TB patients, drug resistance pattern of bTB isolates, and knowledge, attitude, and practices (KAP)-based analysis of bTB disease. For this purpose, sputum samples from a total of 300 clinically diagnosed TB patients and 100 randomly selected school children suspected of pulmonary TB were processed by culture as well as polymerase chain reaction (PCR) for isolation, identification, and confirmation of Mycobacterium tuberculosis (mTB) and bTB species. Isolates of bTB were processed for drug susceptibility tests. Data on KAP regarding TB were obtained on a pretested questionnaire. Sputum-based PCR results indicated that 288/300 (96%) were confirmed as mTB, while 12/300 (4%) were found as bTB diseases. Interestingly, none of the school child was declared positive for either mTB or bTB. Notably, 274/300 (91.3%) positively cultured samples were identified as mTB, 13/300 (4.3%) as bTB, while 5/300 (1.7%) as mixed containing both. Importantly, except one, all of the bTB isolates were found resistant to pyrazinamide. Surprisingly, most of the bTB isolates (~70%) were found resistant to a broad range of first- and second-line anti-TB drugs. SplitsTree and recombination analysis indicated no evidence of intergenic recombination. Finally, residence, occupation, presence of animals at home, and sleeping alongside animals were found significantly associated with occurrence of bTB disease. To the best of our knowledge, we report for the first time on the high (4%) burden of bTB disease in human TB patients in Peshawar, Pakistan.

Keywords

Drug resistance Knowledge, attitude, and practices Mycobacterium bovis Pakistan Pyrazinamide Tuberculosis Zoonosis 

References

  1. Ayaz S, Nosheen T, Khan S, Khan SN, Rubab L, Akhtar M (2012) Pulmonary tuberculosis: still prevalent in human in Peshawar, Khyber Pakhtunkhwa, Pakistan. Tuberculosis (TB) 10:39–41Google Scholar
  2. Ayele WY, Neill SD, Zinsstag J, Weiss MG, Pavlik I (2004) Bovine tuberculosis: an old disease but a new threat to Africa. Int J Tuberc Lung Dis 8:924–937PubMedGoogle Scholar
  3. Bobadilla-Del VALLE M, Torres-Gonzalez P, Cervera-Hernandez ME, Martinez-Gamboa A, Crabtree-Ramirez B, Chavez-Mazari B, Ortiz-Conchi N, Rodriguez-Cruz L, Cervantes-Sanchez A, Gudino-Enriquez T, Cinta-Severo C, Sifuentes-Osornio J, Ponce de Leon A (2015) Trends of Mycobacterium bovis isolation and first-line anti-tuberculosis drug susceptibility profile: a fifteen-year laboratory-based surveillance. PLoS Negl Trop Dis 9:e0004124CrossRefGoogle Scholar
  4. Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681CrossRefGoogle Scholar
  5. Cordova E, Gonzalo X, Boschi A, Lossa M, Robles M, Poggi S, Ambroggi M (2012) Human Mycobacterium bovis infection in Buenos Aires: epidemiology, microbiology and clinical presentation. Int J Tuberc Lung Dis 16:415–417CrossRefGoogle Scholar
  6. de Kantor IN, Ambroggi M, Poggi S, Morcillo N, Telles MADS, Ribeiro MO, Torres MCG, Polo CL, Ribón W, García V (2008) Human Mycobacterium bovis infection in ten Latin American countries. Tuberculosis 88:358–365CrossRefGoogle Scholar
  7. de la Rua-Domenech R (2006) Human Mycobacterium bovis infection in the United Kingdom: incidence, risks, control measures and review of the zoonotic aspects of bovine tuberculosis. Tuberculosis 86:77–109CrossRefGoogle Scholar
  8. de Lisle G, Bengis R, Schmitt S, O'brien D (2002) Tuberculosis in free-ranging wildlife: detection, diagnosis and management. Revue scientifique et technique (International Office of Epizootics) 21:317–334Google Scholar
  9. di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39:W13–W17CrossRefGoogle Scholar
  10. Grange J, Collins C (1987) Bovine tubercle bacilli and disease in animals and man. Epidemiol Infect 99:221–234CrossRefGoogle Scholar
  11. Grange JM (2001) Mycobacterium bovis infection in human beings. Tuberculosis (Edinb) 81:71–77CrossRefGoogle Scholar
  12. Hlavsa MC, Moonan PK, Cowan LS, Navin TR, Kammerer JS, Morlock GP, Crawford JT, Lobue PA (2008) Human tuberculosis due to Mycobacterium bovis in the United States, 1995-2005. Clin Infect Dis 47:168–175CrossRefGoogle Scholar
  13. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267CrossRefGoogle Scholar
  14. Jabbar A, Khan J, Ullah A, Rehman H, Ali I (2015) Detection of Mycobacterium tuberculosis and Mycobacterium bovis from human sputum samples through multiplex PCR. Pak J Pharm Sci 28:1275–1280PubMedGoogle Scholar
  15. Javed MT, Ahmad L, Feliziani F, Pasquali P, Akhtar M, Usman M, Irfan M, Severi G, Cagiola M (2012) Analysis of some of the epidemiological risk factors affecting the prevalence of tuberculosis in buffalo at seven livestock farms in Punjab Pakistan. Asian Biomed 6:35–42Google Scholar
  16. Kasai H, Ezaki T, Harayama S (2000) Differentiation of phylogenetically related slowly growing mycobacteria by their gyrB sequences. J Clin Microbiol 38:301–308PubMedPubMedCentralGoogle Scholar
  17. Khan IA, Khan A (2007) Prevalence and risk factors of bovine tuberculosis in Nili Ravi buffaloes in the Punjab, Pakistan. Ital J Anim Sci 6:817–820CrossRefGoogle Scholar
  18. Khattak I, Mushtaq MH, Ahmad MuD, Khan MS, Chaudhry M, Sadique U (2016) Risk factors associated with Mycobacterium bovis skin positivity in cattle and buffalo in Peshawar, Pakistan. Trop Anim Health Prod 48:479–485CrossRefGoogle Scholar
  19. Kilale AM, Ngadaya E, Kagaruki GB, Lema YL, Muhumuza J, Ngowi BJ, Mfinanga SG, Hinderaker SG (2015) Experienced and perceived risks of mycobacterial diseases: a cross sectional study among agropastoral communities in northern Tanzania. PLoS One 10:e0130180CrossRefGoogle Scholar
  20. Laniado-Laborin R, Muniz-Salazar R, Garcia-Ortiz RA, Vargas-Ojeda AC, Villa-Rosas C, Oceguera-Palao L (2014) Molecular characterization of Mycobacterium bovis isolates from patients with tuberculosis in Baja California, Mexico. Infect Genet Evol 27:1–5CrossRefGoogle Scholar
  21. Majoor CJ, Magis-Escurra C, van Ingen J, Boeree MJ, van Soolingen D (2011) Epidemiology of Mycobacterium bovis disease in humans, The Netherlands, 1993-2007. Emerg Infect Dis 17:457–463CrossRefGoogle Scholar
  22. Mclaughlin AM, Gibbons N, Fitzgibbon M, Power JT, Foley SC, Hayes JP, Rogers T, Keane J (2012) Primary isoniazid resistance in Mycobacterium bovis disease: a prospect of concern. Am J Respir Crit Care Med 186:110–111CrossRefGoogle Scholar
  23. Milian-Suazo F, Perez-Guerrero L, Arriaga-Diaz C, Escartin-Chavez M (2010) Molecular epidemiology of human cases of tuberculosis by Mycobacterium bovis in Mexico. Prev Vet Med 97:37–44CrossRefGoogle Scholar
  24. Morcillo N, Imperiale B, Palomino JC (2008) New simple decontamination method improves microscopic detection and culture of mycobacteria in clinical practice. Infect drug resist 1:21–26CrossRefGoogle Scholar
  25. Morris R, Pfeiffer D, Jackson R (1994) The epidemiology of Mycobacterium bovis infections. Vet Microbiol 40:153–177CrossRefGoogle Scholar
  26. Nawaz A, Chaudhry ZI, Shahid M, Gul S, Khan FA, Hussain M (2012) Detection of Mycobacterium tuberculosis and Mycobacterium bovis in sputum and blood samples of human. J Anim Plant Sci 22(2 suppl):117–120Google Scholar
  27. Niemann S, Harmsen D, Rusch-Gerdes S, Richter E (2000) Differentiation of clinical Mycobacterium tuberculosis complex isolates by gyrB DNA sequence polymorphism analysis. J Clin Microbiol 38:3231–3234PubMedPubMedCentralGoogle Scholar
  28. O'reilly LM, Daborn C (1995) The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tuber Lung Dis 76:1–46CrossRefGoogle Scholar
  29. Ojo O, Sheehan S, Corcoran GD, Okker M, Gover K, Nikolayevsky V, Brown T, Dale J, Gordon SV, Drobniewski F, Prentice MB (2008) Mycobacterium bovis strains causing smear-positive human tuberculosis, Southwest Ireland. Emerg Infect Dis 14:1931–1934CrossRefGoogle Scholar
  30. Phillips C, Foster C, Morris P, Teverson R (2003) The transmission of Mycobacterium bovis infection to cattle. Res Vet Sci 74:1–15CrossRefGoogle Scholar
  31. Rahman MM, Noor M, Islam KM, Uddin MB, Hossain FMA, Zinnah MA, Mamun MA, Islam MR, EO SK, Ashour HM (2015) Molecular diagnosis of bovine tuberculosis in bovine and human samples: implications for zoonosis. Future Microbiol 10:527–535CrossRefGoogle Scholar
  32. Rana M, Sayem A, Karim R, Islam N, Islam R, Zaman TK, Hossain G (2015) Assessment of knowledge regarding tuberculosis among non-medical university students in Bangladesh: a cross-sectional study. BMC Public Health 15:716CrossRefGoogle Scholar
  33. Rodriguez E, Sanchez LP, Perez S, Herrera L, Jimenez MS, Samper S, Iglesias MJ (2009) Human tuberculosis due to Mycobacterium bovis and M. caprae in Spain, 2004-2007. Int J Tuberc Lung Dis 13:1536–1541PubMedGoogle Scholar
  34. Rodriguez JG, Mejia GA, del Portillo P, Patarroyo ME, Murillo LA (1995) Species-specific identification of Mycobacterium bovis by PCR. Microbiology 141:2131–2138CrossRefGoogle Scholar
  35. Sanou A, Tarnagda Z, Kanyala E, Zingué D, Nouctara M, Ganamé Z, Combary A, Hien H, Dembele M, Kabore A, Meda N, van de Perre P, Neveu D, Bañuls AL, Godreuil S (2014) Mycobacterium bovis in Burkina Faso: epidemiologic and genetic links between human and cattle isolates. PLoS Negl Trop Dis 8:e3142CrossRefGoogle Scholar
  36. Silva MR, Rocha ADA S, da Costa RR, de Alencar AP, de Oliveira VM, Fonseca Junior AA, Sales ML, Issa MDE A, Filho PM, Pereira OT, Dos Santos EC, Mendes RS, Ferreira AM, Mota PM, Suffys PN, Guimaraes MD (2013) Tuberculosis patients co-infected with Mycobacterium bovis and Mycobacterium tuberculosis in an urban area of Brazil. Mem Inst Oswaldo Cruz 108:321–327CrossRefGoogle Scholar
  37. Sunder S, Lanotte P, Godreuil S, Martin C, Boschiroli ML, Besnier JM (2009) Human-to-human transmission of tuberculosis caused by Mycobacterium bovis in immunocompetent patients. J Clin Microbiol 47:1249–1251CrossRefGoogle Scholar
  38. Tolossa D, Medhin G, Legesse M (2014) Community knowledge, attitude, and practices towards tuberculosis in Shinile town, Somali regional state, eastern Ethiopia: a cross-sectional study. BMC Public Health 14:804CrossRefGoogle Scholar
  39. Tortoli E, Benedetti M, Fontanelli A, Simonetti MT (2002) Evaluation of automated BACTEC MGIT 960 system for testing susceptibility of Mycobacterium tuberculosis to four major Antituberculous drugs: comparison with the radiometric BACTEC 460TB method and the agar plate method of proportion. J Clin Microbiol 40:607–610CrossRefGoogle Scholar
  40. Traore B, Diarra B, Dembele BP, Somboro AM, Hammond AS, Siddiqui S, Maiga M, Kone B, Sarro YS, Washington J, Parta M, Coulibaly N, M'baye O, Diallo S, Koita O, Tounkara A, Polis MA (2012) Molecular strain typing of Mycobacterium tuberculosis complex in Bamako, Mali. Int J Tuberc Lung Dis 16:911–916CrossRefGoogle Scholar
  41. WHO (2014) Global tuberculosis report. World Health Organization, GenevaGoogle Scholar
  42. Zaman K (2010) Tuberculosis: a Global Health problem. J Health Popul Nutr 28:111–113CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Irfan Khattak
    • 1
    • 2
  • Muhammad Hassan Mushtaq
    • 1
  • Sultan Ayaz
    • 2
  • Sajid Ali
    • 3
  • Anwar Sheed
    • 3
  • Javed Muhammad
    • 4
  • Muhammad Luqman Sohail
    • 5
    • 6
  • Haq Amanullah
    • 6
  • Irshad Ahmad
    • 7
  • Sadeeq ur Rahman
    • 2
  1. 1.Department of Epidemiology and Public HealthUniversity of Veterinary and Animal SciencesLahorePakistan
  2. 2.College of Animal Husbandry & Veterinary SciencesAbdul Wali Khan UniversityMardanPakistan
  3. 3.Provincial Tuberculosis Reference LaboratoryPeshawarPakistan
  4. 4.University Diagnostic Lab, University of Veterinary and Animal SciencesLahorePakistan
  5. 5.University College of Veterinary and Animal SciencesThe Islamia university of BahawalpurBahawalpurPakistan
  6. 6.Department of Clinical Medicine and SurgeryUniversity of Veterinary and Animal SciencesLahorePakistan
  7. 7.School of Biomedical SciencesUniversity of LeedsLeedsUK

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