Mycobacterium bovis infection at the interface between domestic and wild animals in Zambia

BMC Veterinary Research

Yasuhiko Suzuki¹  Aaron S Mweene²  Akihiro Ishii³  Wigganson Matandiko⁴  Haruka Suzuki³  Yukari Fukushima³  Chie Nakajima³  Musso Munyeme²  Mudenda B Hang’ombe² 

[1] JST/JICA-SATREPS, Tokyo, 120-8666, Japan;School of Veterinary Medicine, University of Zambia, P. O. Box 32379, Lusaka, Zambia;Hokkaido University Research Center for Zoonosis Control, Kita-20, Nishi-10, Kita-ku, 001-0020, Sapporo, Japan;Zambia Wildlife Authority, Private Bag 001, Chilanga, Zambia

关键词: Kobus leche Kafuensis;    Wildlife;    Strains;    Mycobacterium bovis;    Cattle;    Bovine tuberculosis;   

Others  :  1119666
DOI  :  10.1186/1746-6148-8-221

 received in 2012-06-19, accepted in 2012-10-26,  发布年份 2012

【 摘 要 】

Background

In Zambia, the presence of bovine tuberculosis in both wild and domestic animals has long been acknowledged and mutual transmission between them has been predicted without any direct evidence. Elucidation of the circulating Mycobacterium bovis strains at wild and domestic animals interphase area in Zambia, where bovine tuberculosis was diagnosed in wildlife seemed to be important.

Results

A PCR identified 15 and 37 M. bovis isolates from lechwe and cattle, respectively. Spoligotype analysis revealed that M. bovis strains from lechwe and cattle in Kafue basin clustered into a major node SB0120, where isolates outside the Kafue basin clustered into different nodes of SB0131 and SB0948. The comparatively higher variety of strains in cattle compared to lechwe elucidated by Mycobacterial Interspersed Repetitive Units–Variable Number Tandem Repeats analyses are consistent with cattle being the probable source of M. bovis in wild and domestic animals interphase area in Zambia.

Conclusions

These results provide strong evidence of M. bovis strains transfer between cattle and lechwe, with the latter having developed into a sylvatic reservoir host.

【 授权许可】

   
2012 Hang'ombe et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, Eiglmeier K, Garnier T, Gutierrez C, Hewinson G, Kremer K, Parsons LM, Pym AS, Samper S, van Soolingen D, Cole ST: A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 2002, 99:3684-3689.
• [2]Huard RC, Fabre M, de Haas P, Lazzarini LC, van Soolingen D, Cousins D, Ho JL: Novel genetic polymorphisms that further delineate the phylogeny of the Mycobacterium tuberculosis complex. J Bacteriol 2006, 188:4271-4287.
• [3]Acha PN, Szyfres B: Zoonotic tuberculosis. In Zoonoses and communicable diseases common to man and animals. 2nd edition. Washington: Pan American Health Organization/World Health Organization; 1987. [Scientific Publication No 503]
• [4]Cosivi O, Grange JM, Daborn CJ, Raviglione MC, Fujikura T, Cousins D, Robinson RA, Huchzermeyer HF, de Kantor I, Meslin FX: Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerg Infect Dis 1998, 4:59-70.
• [5]Moda G, Daborn CJ, Grange JM, Cosivi O: The zoonotic importance of Mycobacterium bovis. Tuber Lung Dis 1996, 77:103-108.
• [6]Gortazar C, Vicente J, Samper S, Garrido JM, Fernandez-De-Mera IG, Gavin P, Juste RA, Martin C, Acevedo P, De La Puente M, Hofle U: Molecular characterization of Mycobacterium tuberculosis complex isolates from wild ungulates in south-central Spain. Vet Res 2005, 36:43-52.
• [7]Munyeme M, Muma JB, Samui KL, Skjerve E, Nambota AM, Phiri IG, Rigouts L, Tryland M: Prevalence of bovine tuberculosis and animal level risk factors for indigenous cattle under different grazing strategies in the livestock/wildlife interface areas of Zambia. Trop Anim Health Prod 2009, 41:345-352.
• [8]Cook AJ, Tuchili LM, Buve A, Foster SD, Godfrey-Fausett P, Pandey GS, McAdam KP: Human and bovine tuberculosis in the Monze District of Zambia-a cross-sectional study. Br Vet J 1996, 152:37-46.
• [9]Pandey GS: Studies of the infectious diseases of the Kafue lechwe (Kobus leche kafuensis) with particular reference to tuberculosis in Zambia. PhD thesis. Azabu University, Tokyo; 1998.
• [10]Bengis RG, Leighton FA, Fischer JR, Artois M, Morner T, Tate CM: The role of wildlife in emerging and re-emerging zoonoses. Rev Sci Tech 2004, 23:497-511.
• [11]Munyeme M, Muma JB, Siamudaala VM, Skjerve E, Munang'andu HM, Tryland M: Tuberculosis in Kafue lechwe antelopes (Kobus leche Kafuensis) of the Kafue Basin in Zambia. Prev Vet Med 2010, 95:305-308.
• [12]Chansa W, Kampamba G: The population status of the Kafue Lechwe in the Kafue Flats, Zambia. Afr J Ecol 2010, 48:837-840.
• [13]Anonymous: Annual report of the Department of Veterinary Services and Livestock Development. Printers G. Lusaka: Government of the Republic of Zambia; 2004.
• [14]Kamweneshe B, Beilfesus R, Simukonda C: Population and distribution of the Kafue lechwe and other large mammals on the Kafue flats, Zambia. Lusaka: WWF Partners for Wetlands; 2002:23.
• [15]Munyeme M, Muma JB, Skjerve E, Nambota AM, Phiri IG, Samui KL, Dorny P, Tryland M: Risk factors associated with bovine tuberculosis in traditional cattle of the livestock/wildlife interface areas in the Kafue basin of Zambia. Prev Vet Med 2008, 85:317-328.
• [16]Hang'ombe BM, Nakajima C, Ishii A, Fukushima Y, Munyeme M, Matandiko W, Mweene AS, Suzuki Y: Rapid detection ofMycobacterium tuberculosiscomplex in cattle and lechwe (Kobus leche kafuensis) at the slaughter house. Vet Sci Dev 2011, 1:e5.
• [17]Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett J, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson GR: The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 2003, 100:7877-7882.
• [18]Cole ST: Comparative mycobacterial genomics. Curr Opin Microbiol 1998, 1:567-571.
• [19]Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentiles S, Hamlin N, Holroyd S, Hornsby T, Jegels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, et al.: Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393:537-544.
• [20]Brosch R, Gordon SV, Billault A, Garnier T, Eiglmeier K, Soravito C, Barrell BG, Cole ST: Use of a Mycobacterium tuberculosis H37Rv bacterial artificial chromosome library for genome mapping, sequencing, and comparative genomics. Infect Immun 1998, 66:2221-2229.
• [21]Philipp WJ, Schwartz DC, Telenti A, Cole ST: Mycobacterial genome structure. Electrophoresis 1998, 19:573-576.
• [22]Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J: Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 1997, 35:907-914.
• [23]Bauer J, Andersen AB, Kremer K, Miorner H: Usefulness of spoligotyping to discriminate IS6110 low-copy-number Mycobacterium tuberculosis complex strains cultured in Denmark. J Clin Microbiol 1999, 37:2602-2606.
• [24]Mycobacterium bovis Database. http://www.mbovis.org webcite
• [25]Roring S, Scott A, Brittain D, Walker I, Hewinson G, Neill S, Skuce R: Development of variable-number tandem repeat typing of Mycobacterium bovis: comparison of results with those obtained by using existing exact tandem repeats and spoligotyping. J Clin Microbiol 2002, 40:2126-2133.
• [26]Frothingham R, Meeker-O'Connell WA: Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats. Microbiology 1998, 144:1189-1196.
• [27]Stafford KJ: A review of diseases of parasites of the Kafue lechwe (Kobus leche kafuensis). J Wildl Dis 1991, 27:661-667.
• [28]Munyeme M, Munang'andu HM: A review of bovine tuberculosis in the Kafue basin ecosystem. Vet Med Int 2011, 2011:918743.
• [29]Nakajima C, Rahim Z, Fukushima Y, Sugawara I, van der Zanden AG, Tamaru A, Suzuki Y: Identification of Mycobacterium tuberculosis clinical isolates in Bangladesh by a species distinguishable multiplex PCR. BMC Infect Dis 2010, 10:118. BioMed Central Full Text
• [30]Huard RC, de Oliveira Lazzarini LC, Butler WR, van Soolingen D, Ho JL: PCR based method to differentiate the subspecies of the Mycobacterium tuberculosis complex on the basis of genome deletions. J Clin Microbiol 2003, 41:1637-1650.
• [31]Huard RC, Chitale S, Leung M, Lazzarini LC, Zhu H, Shashkina E, Laal S, Conde MB, Kritski AL, Belisle JT, Kreiswirth BN, Lapa e Silva JR, Ho JL: The Mycobacterium tuberculosis complex restricted gene cfp32 encodes an expressed protein that is detectable in tuberculosis patients and is positively correlated with pulmonary interleukin-10. Infect Immun 2003, 71:6871-6883.
• [32]Corner LA: The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: How to assess the risk. Vet Microbiol 2006, 112:303-312.
• [33]Parra A, Larrasa J, Garcia A, Alonso JM, Mendoza de Hermoso J: Molecular epidemiology of bovine tuberculosis in wild animals in Spain: A first approach to risk factor analysis. Vet Microbiol 2005, 110:293-300.
• [34]Munyeme M, Rigouts L, Shamputa IC, Muma JB, Tryland M, Skjerve E, Djonne B: Isolation and characterization of Mycobacterium bovis strains from indigenous Zambian cattle using Spacer oligonucleotide typing technique. BMC Microbiol 2009, 9:144. BioMed Central Full Text
• [35]Mignard S, Pichat C, Carret G: Mycobacterium bovis infection, Lyon, France. Emerg Infect Dis 2006, 12:1431-1433.
• [36]Sahraoui N, Muller B, Guetarni D, Boulahbal F, Yala D, Ouzrout R, Berg S, Smith NH, Zinsstag J: Molecular characterization of Mycobacterium bovis strains isolated from cattle slaughtered at two abattoirs in Algeria. BMC Vet Res 2009, 5:4. BioMed Central Full Text
• [37]Duarte EL, Domingos M, Amado A, Botelho A: Spoligotype diversity of Mycobacterium bovis and Mycobacterium caprae animal isolates. Vet Microbiol 2008, 130:415-421.
• [38]Serraino A, Marchetti G, Sanguinetti V, Rossi MC, Zanoni RG, Catozzi L, Bandera A, Dini W, Mignone W, Franzetti F, Gori A: Monitoring of transmission of tuberculosis between wild boars and cattle: genotypical analysis of strains by molecular epidemiology techniques. J Clin Microbiol 1999, 37:2766-2771.
• [39]Aranaz A, Liebana E, Mateos A, Dominguez L, Vidal D, Domingo M, Gonzolez O, Rodriguez-Ferri EF, Bunschoten AE, Van Embden JD, Cousins D: Spacer oligonucletide typing of Mycobacterium bovis strains from cattle and other animasl: a tool for studying epidemiology of tuberculosis. J Clin Microbiol 1996, 34:2734-2740.
• [40]Cousins D, Williams S, Liebana E, Aranaz A, Bunschoten A, Van Embden J, Ellis T: Evaluation of four DNA typing techniques in epidemiological investigations of bovine tuberculosis. J Clin Microbiol 1998, 36:168-178.
• [41]Njanpop Lafourcade BM, Inwad J, Ostyn A, Durand B, Hughes S, Thorel MF, Hewinson G, Haddad N: Molecular typing of Mycobacterium bovis isolates from Cameroon. J Clin Microbiol 2001, 39:222-227.
• [42]Michel LA, Hlokwe MT, Coetzee LM, Mare L, Connoway L, Rutten GMPV, Kremer K: High Mycobacterium bovis genetic diversity in a low prevalence setting. Vet Microbiol 2008, 126:151-159.
• [43]Gracey JF, Collins DS, Huey RJ: Meat Hygiene. 10th edition. London, NewYork: W. B. Saunders & Company Toronto;
• [44]Suzuki Y, Katsukawa C, Inoue K, Yin Y, Tasaka H, Ueba N, Makino M: Mutations in rpoB gene of rifampicin resistant clinical isolates of Mycobacterium tuberculosis in Japan. Kansenshogaku Zasshi 1995, 69:413-419.
• [45]Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, Willery E, Savine E, de Haas P, van Deutekom H, Roring S, Bifani P, Kurepina N, Kreiswirth B, Sola C, Rastogi N, Vatin V, Gutierrez MC, Fauville M, Niemann S, Skuce R, Kremer K, Locht C, van Soolingen D: Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 2006, 44:4498-4510.