Skip to main content
Top
Published in: BMC Public Health 1/2011

Open Access 01-12-2011 | Research article

Isolation of non-tuberculous mycobacteria from pastoral ecosystems of Uganda: Public Health significance

Authors: Clovice Kankya, Adrian Muwonge, Berit Djønne, Musso Munyeme, John Opuda-Asibo, Eystein Skjerve, James Oloya, Vigdis Edvardsen, Tone B Johansen

Published in: BMC Public Health | Issue 1/2011

Login to get access

Abstract

Background

The importance of non-tuberculous mycobacteria (NTM) infections in humans and animals in sub-Saharan Africa at the human-environment-livestock-wildlife interface has recently received increased attention. NTM are environmental opportunistic pathogens of humans and animals. Recent studies in pastoral ecosystems of Uganda detected NTM in humans with cervical lymphadenitis and cattle with lesions compatible with bovine tuberculosis. However, little is known about the source of these mycobacteria in Uganda. The aim of this study was to isolate and identify NTM in the environment of pastoral communities in Uganda, as well as assess the potential risk factors and the public health significance of NTM in these ecosystems.

Method

A total of 310 samples (soil, water and faecal from cattle and pigs) were examined for mycobacteria. Isolates were identified by the INNO-Lipa test and by 16S rDNA sequencing. Additionally, a questionnaire survey involving 231 pastoralists was conducted during sample collection. Data were analysed using descriptive statistics followed by a multivariable logistic regression analysis.

Results

Forty-eight isolates of NTM were detected; 25.3% of soil samples, 11.8% of water and 9.1% from animal faecal samples contained mycobacteria. Soils around water sources were the most contaminated with NTM (29.8%). Of these samples, M. fortuitum-peregrinum complex, M. avium complex, M. gordonae, and M. nonchromogenicum were the most frequently detected mycobacteria. Drinking untreated compared to treated water (OR = 33), use of valley dam versus stream water for drinking and other domestic use (OR = 20), sharing of water sources with wild primates compared to antelopes (OR = 4.6), sharing of water sources with domestic animals (OR = 5.3), and close contact with cattle or other domestic animals (OR = 13.8) were the most plausible risk factors for humans to come in contact with NTM in the environment.

Conclusions

The study detected a wide range of potentially pathogenic NTM from the environment around the pastoral communities in Uganda. Drinking untreated water and living in close contact with cattle or other domestic animals may be risk factors associated with the possibility of humans and animals acquiring NTM infections from these ecosystems.
Appendix
Available only for authorised users
Literature
1.
go back to reference van Ingen J, Boeree MJ, Dekhuijzen PN, van Soolingen D: Environmental sources of rapid growing nontuberculous mycobacteria causing disease in humans. Clin Microbiol Infect. 2009, 15: 888-893. 10.1111/j.1469-0691.2009.03013.x.CrossRefPubMed van Ingen J, Boeree MJ, Dekhuijzen PN, van Soolingen D: Environmental sources of rapid growing nontuberculous mycobacteria causing disease in humans. Clin Microbiol Infect. 2009, 15: 888-893. 10.1111/j.1469-0691.2009.03013.x.CrossRefPubMed
3.
go back to reference Covert TC, Rodgers MR, Reyes AL, Stelma GN: Occurrence of nontuberculous mycobacteria in environmental samples. Appl Environ Microbiol. 1999, 65: 2492-2496.PubMedPubMedCentral Covert TC, Rodgers MR, Reyes AL, Stelma GN: Occurrence of nontuberculous mycobacteria in environmental samples. Appl Environ Microbiol. 1999, 65: 2492-2496.PubMedPubMedCentral
5.
go back to reference Rastogi N, Legrand E, Sola C: The mycobacteria: an introduction to nomenclature and pathogenesis. Rev Sci Tech. 2001, 20: 21-54.PubMed Rastogi N, Legrand E, Sola C: The mycobacteria: an introduction to nomenclature and pathogenesis. Rev Sci Tech. 2001, 20: 21-54.PubMed
6.
go back to reference Schroder KH, Naumann L, Kroppenstedt RM, Reischl U: Mycobacterium hassiacum sp. nov., a new rapidly growing thermophilic mycobacterium. Int J Syst Bacteriol. 1997, 47: 86-91. 10.1099/00207713-47-1-86.CrossRefPubMed Schroder KH, Naumann L, Kroppenstedt RM, Reischl U: Mycobacterium hassiacum sp. nov., a new rapidly growing thermophilic mycobacterium. Int J Syst Bacteriol. 1997, 47: 86-91. 10.1099/00207713-47-1-86.CrossRefPubMed
7.
go back to reference Dailloux M, Laurain C, Weber R, Hartemann P: Water and nontuberculous mycobacteria. Water Res. 2010, 33: 2219-2228.CrossRef Dailloux M, Laurain C, Weber R, Hartemann P: Water and nontuberculous mycobacteria. Water Res. 2010, 33: 2219-2228.CrossRef
8.
go back to reference Falkinham JO: Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol. 2009, 107: 356-367. 10.1111/j.1365-2672.2009.04161.x.CrossRefPubMed Falkinham JO: Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol. 2009, 107: 356-367. 10.1111/j.1365-2672.2009.04161.x.CrossRefPubMed
9.
go back to reference von Reyn CF, Waddell RD, Eaton T, Arbeit RD, Maslow JN, Barber TW: Isolation of Mycobacterium avium complex from water in the United States, Finland, Zaire, and Kenya. J Clin Microbiol. 1993, 31: 3227-3230.PubMedPubMedCentral von Reyn CF, Waddell RD, Eaton T, Arbeit RD, Maslow JN, Barber TW: Isolation of Mycobacterium avium complex from water in the United States, Finland, Zaire, and Kenya. J Clin Microbiol. 1993, 31: 3227-3230.PubMedPubMedCentral
10.
go back to reference Fine PE, Floyd S, Stanford JL, Nkhosa P, Kasunga A, Chaguluka S: Environmental mycobacteria in northern Malawi: implications for the epidemiology of tuberculosis and leprosy. Epidemiol Infect. 2001, 126: 379-387.CrossRefPubMedPubMedCentral Fine PE, Floyd S, Stanford JL, Nkhosa P, Kasunga A, Chaguluka S: Environmental mycobacteria in northern Malawi: implications for the epidemiology of tuberculosis and leprosy. Epidemiol Infect. 2001, 126: 379-387.CrossRefPubMedPubMedCentral
11.
go back to reference Phillips P, Bonner S, Gataric N, Bai T, Wilcox P, Hogg R: Nontuberculous mycobacterial immune reconstitution syndrome in HIV-infected patients: spectrum of disease and long-term follow-up. Clin Infect Dis. 2005, 41: 1483-1497. 10.1086/497269.CrossRefPubMed Phillips P, Bonner S, Gataric N, Bai T, Wilcox P, Hogg R: Nontuberculous mycobacterial immune reconstitution syndrome in HIV-infected patients: spectrum of disease and long-term follow-up. Clin Infect Dis. 2005, 41: 1483-1497. 10.1086/497269.CrossRefPubMed
12.
go back to reference Jarzembowski JA, Young MB: Nontuberculous mycobacterial infections. Arch Pathol Lab Med. 2008, 132: 1333-1341.PubMed Jarzembowski JA, Young MB: Nontuberculous mycobacterial infections. Arch Pathol Lab Med. 2008, 132: 1333-1341.PubMed
13.
go back to reference Kourbeti IS, Maslow MJ: Nontuberculous Mycobacterial Infections of the Lung. Curr Infect Dis Rep. 2000, 2: 193-200. 10.1007/s11908-000-0035-7.CrossRefPubMed Kourbeti IS, Maslow MJ: Nontuberculous Mycobacterial Infections of the Lung. Curr Infect Dis Rep. 2000, 2: 193-200. 10.1007/s11908-000-0035-7.CrossRefPubMed
14.
go back to reference Bouts T, Vordermeier M, Flach E, Routh A: Positive skin and serologic test results of diagnostic assays for bovine tuberculosis and subsequent isolation of Mycobacterium interjectum in a pygmy hippopotamus (Hexaprotodon liberiensis). J Zoo Wildl Med. 2009, 40: 536-542. 10.1638/2008-0001.1.CrossRefPubMed Bouts T, Vordermeier M, Flach E, Routh A: Positive skin and serologic test results of diagnostic assays for bovine tuberculosis and subsequent isolation of Mycobacterium interjectum in a pygmy hippopotamus (Hexaprotodon liberiensis). J Zoo Wildl Med. 2009, 40: 536-542. 10.1638/2008-0001.1.CrossRefPubMed
15.
16.
go back to reference Kazda J, Cook BR: Mycobacteria in pond waters as a source of non-specific reactions to bovine tuberculin in New Zealand. N Z Vet J. 1988, 36: 184-188. 10.1080/00480169.1988.35527.CrossRefPubMed Kazda J, Cook BR: Mycobacteria in pond waters as a source of non-specific reactions to bovine tuberculin in New Zealand. N Z Vet J. 1988, 36: 184-188. 10.1080/00480169.1988.35527.CrossRefPubMed
17.
18.
go back to reference Falkinham JO: Nontuberculous mycobacteria in the environment. Clin Chest Med. 2002, 23: 529-551. 10.1016/S0272-5231(02)00014-X.CrossRefPubMed Falkinham JO: Nontuberculous mycobacteria in the environment. Clin Chest Med. 2002, 23: 529-551. 10.1016/S0272-5231(02)00014-X.CrossRefPubMed
19.
go back to reference Chilima BZ, Clark IM, Floyd S, Fine PE, Hirsch PR: Distribution of environmental mycobacteria in Karonga District, northern Malawi. Appl Environ Microbiol. 2006, 72: 2343-2350. 10.1128/AEM.72.4.2343-2350.2006.CrossRefPubMedPubMedCentral Chilima BZ, Clark IM, Floyd S, Fine PE, Hirsch PR: Distribution of environmental mycobacteria in Karonga District, northern Malawi. Appl Environ Microbiol. 2006, 72: 2343-2350. 10.1128/AEM.72.4.2343-2350.2006.CrossRefPubMedPubMedCentral
20.
go back to reference Oloya J, Kazwala R, Lund A, Opuda-Asibo J, Demelash AB, Skjerve E, Johansen TB, Djonne B: Characterisation of mycobacteria isolated from slaughter cattle in pastoral regions of Uganda. BMC Microbiol. 2007, 7: 95-10.1186/1471-2180-7-95.CrossRefPubMedPubMedCentral Oloya J, Kazwala R, Lund A, Opuda-Asibo J, Demelash AB, Skjerve E, Johansen TB, Djonne B: Characterisation of mycobacteria isolated from slaughter cattle in pastoral regions of Uganda. BMC Microbiol. 2007, 7: 95-10.1186/1471-2180-7-95.CrossRefPubMedPubMedCentral
21.
go back to reference Oloya J, Opuda-Asibo J, Kazwala R, Demelash AB, Skjerve E, Lund A, Johansen TB, Djonne B: Mycobacteria causing human cervical lymphadenitis in pastoral communities in the Karamoja region of Uganda. Epidemiol Infect. 2008, 136: 636-643.CrossRefPubMed Oloya J, Opuda-Asibo J, Kazwala R, Demelash AB, Skjerve E, Lund A, Johansen TB, Djonne B: Mycobacteria causing human cervical lymphadenitis in pastoral communities in the Karamoja region of Uganda. Epidemiol Infect. 2008, 136: 636-643.CrossRefPubMed
22.
go back to reference Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C: An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 2007, 175: 367-416. 10.1164/rccm.200604-571ST.CrossRefPubMed Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C: An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 2007, 175: 367-416. 10.1164/rccm.200604-571ST.CrossRefPubMed
23.
go back to reference Ashbolt NJ: Microbial contamination of drinking water and disease outcomes in developing regions. Toxicol. 2004, 198: 229-238. 10.1016/j.tox.2004.01.030.CrossRef Ashbolt NJ: Microbial contamination of drinking water and disease outcomes in developing regions. Toxicol. 2004, 198: 229-238. 10.1016/j.tox.2004.01.030.CrossRef
24.
go back to reference Anonymous: District State of Environment Report for Nakasongola District. 2004, 67- Anonymous: District State of Environment Report for Nakasongola District. 2004, 67-
25.
go back to reference Anonymous: District State of Environment, Mubende District. 2004, 129- Anonymous: District State of Environment, Mubende District. 2004, 129-
26.
go back to reference Anonymous: Nakasongola District Council and the National Environment Authority Nakasongola District Emvironment Policy. 2008, Draft 03, 1-3. Anonymous: Nakasongola District Council and the National Environment Authority Nakasongola District Emvironment Policy. 2008, Draft 03, 1-3.
27.
go back to reference Kakuru W, Okorio J: Strategy for Agro-forestry Development in Uganda's Drylands. In Kampala. 2004, 1-11. Kakuru W, Okorio J: Strategy for Agro-forestry Development in Uganda's Drylands. In Kampala. 2004, 1-11.
28.
go back to reference Kankya C, Muwonge A, Olet S, Munyeme M, Biffa D, Opuda-Asibo J, Skjerve E, Oloya J: Factors associated with pastoral community knowledge and occurrence of mycobacterial infections in Human-Animal Interface areas of Nakasongola and Mubende districts, Uganda. BMC Public Health. 2010, 10: 471-10.1186/1471-2458-10-471.CrossRefPubMedPubMedCentral Kankya C, Muwonge A, Olet S, Munyeme M, Biffa D, Opuda-Asibo J, Skjerve E, Oloya J: Factors associated with pastoral community knowledge and occurrence of mycobacterial infections in Human-Animal Interface areas of Nakasongola and Mubende districts, Uganda. BMC Public Health. 2010, 10: 471-10.1186/1471-2458-10-471.CrossRefPubMedPubMedCentral
29.
go back to reference Moore D, Liechty C, Ekwaru P, Were W, Mwima G, Solberg P, Rutherford G, Mermin J: Prevalence, incidence and mortality associated with tuberculosis in HIV-infected patients initiating antiretroviral therapy in rural Uganda. AIDS. 2007, 21: 713-719. 10.1097/QAD.0b013e328013f632.CrossRefPubMed Moore D, Liechty C, Ekwaru P, Were W, Mwima G, Solberg P, Rutherford G, Mermin J: Prevalence, incidence and mortality associated with tuberculosis in HIV-infected patients initiating antiretroviral therapy in rural Uganda. AIDS. 2007, 21: 713-719. 10.1097/QAD.0b013e328013f632.CrossRefPubMed
31.
go back to reference Valheim M, Djonne B, Heiene R, Caugant DA: Disseminated Mycobacterium celatum (type 3) infection in a domestic ferret (Mustela putorius furo). Vet Pathol. 2001, 38: 460-463. 10.1354/vp.38-4-460.CrossRefPubMed Valheim M, Djonne B, Heiene R, Caugant DA: Disseminated Mycobacterium celatum (type 3) infection in a domestic ferret (Mustela putorius furo). Vet Pathol. 2001, 38: 460-463. 10.1354/vp.38-4-460.CrossRefPubMed
32.
go back to reference Johansen TB, Olsen I, Jensen MR, Dahle UR, Holstad G, Djønne B: New probes used for IS1245 and IS1311 restriction fragment length polymorphism of Mycobacterium avium subsp. avium and Mycobacterium avium subsp. hominissuis isolates of human and animal origin in Norway. BMC Microbiol. 2007, 7: 14-10.1186/1471-2180-7-14.CrossRefPubMedPubMedCentral Johansen TB, Olsen I, Jensen MR, Dahle UR, Holstad G, Djønne B: New probes used for IS1245 and IS1311 restriction fragment length polymorphism of Mycobacterium avium subsp. avium and Mycobacterium avium subsp. hominissuis isolates of human and animal origin in Norway. BMC Microbiol. 2007, 7: 14-10.1186/1471-2180-7-14.CrossRefPubMedPubMedCentral
33.
go back to reference van Ingen J, de Zwaan R, Enaimi M, Richard Dekhuijzen PN, Boeree MJ, van Soolingen D: Re-analysis of 178 previously unidentifiable Mycobacterium isolates in the Netherlands from the 1999-2007 period. Clin Microbiol Infect. 2009 van Ingen J, de Zwaan R, Enaimi M, Richard Dekhuijzen PN, Boeree MJ, van Soolingen D: Re-analysis of 178 previously unidentifiable Mycobacterium isolates in the Netherlands from the 1999-2007 period. Clin Microbiol Infect. 2009
34.
go back to reference Tortoli E: Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s. Clin Microbiol Rev. 2003, 16: 319-354. 10.1128/CMR.16.2.319-354.2003.CrossRefPubMedPubMedCentral Tortoli E: Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s. Clin Microbiol Rev. 2003, 16: 319-354. 10.1128/CMR.16.2.319-354.2003.CrossRefPubMedPubMedCentral
35.
go back to reference Edwards U, Rogall T, Blocker H, Emde M, Bottger EC: Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 1989, 17: 7843-7853. 10.1093/nar/17.19.7843.CrossRefPubMedPubMedCentral Edwards U, Rogall T, Blocker H, Emde M, Bottger EC: Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 1989, 17: 7843-7853. 10.1093/nar/17.19.7843.CrossRefPubMedPubMedCentral
36.
go back to reference Eaton T, Falkinham JO, Aisu TO, Daniel TM: Isolation and characteristics of Mycobacterium avium complex from water and soil samples in Uganda. Tuber Lung Dis. 1995, 76: 570-574. 10.1016/0962-8479(95)90536-7.CrossRefPubMed Eaton T, Falkinham JO, Aisu TO, Daniel TM: Isolation and characteristics of Mycobacterium avium complex from water and soil samples in Uganda. Tuber Lung Dis. 1995, 76: 570-574. 10.1016/0962-8479(95)90536-7.CrossRefPubMed
37.
go back to reference Kirschner RA, Parker BC, Falkinham JO: Epidemiology of infection by nontuberculous mycobacteria. Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum in acid, brown-water swamps of the southeastern United States and their association with environmental variables. Am Rev Respir Dis. 1992, 145: 271-275.CrossRefPubMed Kirschner RA, Parker BC, Falkinham JO: Epidemiology of infection by nontuberculous mycobacteria. Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum in acid, brown-water swamps of the southeastern United States and their association with environmental variables. Am Rev Respir Dis. 1992, 145: 271-275.CrossRefPubMed
38.
go back to reference Briancesco R, Semproni M, Della LS, Sdanganelli M, Bonadonna L: Non-tuberculous mycobacteria and microbial populations in drinking water distribution systems. Ann Ist Super Sanita. 2010, 46: 254-258.PubMed Briancesco R, Semproni M, Della LS, Sdanganelli M, Bonadonna L: Non-tuberculous mycobacteria and microbial populations in drinking water distribution systems. Ann Ist Super Sanita. 2010, 46: 254-258.PubMed
39.
go back to reference Buijtels PC, van der Sande MA, de Graaff CS, Parkinson S, Verbrugh HA, Petit PL: Nontuberculous mycobacteria, Zambia. Emerg Infect Dis. 2009, 15: 242-249. 10.3201/eid1502.080006.CrossRefPubMedPubMedCentral Buijtels PC, van der Sande MA, de Graaff CS, Parkinson S, Verbrugh HA, Petit PL: Nontuberculous mycobacteria, Zambia. Emerg Infect Dis. 2009, 15: 242-249. 10.3201/eid1502.080006.CrossRefPubMedPubMedCentral
40.
go back to reference Zamarioli LA, Coelho AG, Pereira CM, Nascimento AC, Ueki SY, Chimara E: Descriptive study of the frequency of nontuberculous mycobacteria in the Baixada Santista region of the state of Sao Paulo, Brazil. J Bras Pneumol. 2008, 34: 590-594.42. 10.1590/S1806-37132008000800008.CrossRefPubMed Zamarioli LA, Coelho AG, Pereira CM, Nascimento AC, Ueki SY, Chimara E: Descriptive study of the frequency of nontuberculous mycobacteria in the Baixada Santista region of the state of Sao Paulo, Brazil. J Bras Pneumol. 2008, 34: 590-594.42. 10.1590/S1806-37132008000800008.CrossRefPubMed
41.
go back to reference Ssali FN, Kamya MR, Wabwire-Mangen F, Kasasa S, Joloba M, Williams D, Mugerwa RD, Ellner JJ, Johnson JL: A prospective study of community-acquired bloodstream infections among febrile adults admitted to Mulago Hospital in Kampala, Uganda. J Acquir Immune Defic Syndr Hum Retrovirol. 1998, 19: 484-489. 10.1097/00042560-199812150-00007.CrossRefPubMed Ssali FN, Kamya MR, Wabwire-Mangen F, Kasasa S, Joloba M, Williams D, Mugerwa RD, Ellner JJ, Johnson JL: A prospective study of community-acquired bloodstream infections among febrile adults admitted to Mulago Hospital in Kampala, Uganda. J Acquir Immune Defic Syndr Hum Retrovirol. 1998, 19: 484-489. 10.1097/00042560-199812150-00007.CrossRefPubMed
42.
go back to reference Cloud JL, Meyer JJ, Pounder JI, Jost KC, Sweeney A, Carroll KC: Mycobacterium arupense sp. nov., a non-chromogenic bacterium isolated from clinical specimens. Int J Syst Evol Microbiol. 2006, 56: 1413-1418. 10.1099/ijs.0.64194-0.CrossRefPubMed Cloud JL, Meyer JJ, Pounder JI, Jost KC, Sweeney A, Carroll KC: Mycobacterium arupense sp. nov., a non-chromogenic bacterium isolated from clinical specimens. Int J Syst Evol Microbiol. 2006, 56: 1413-1418. 10.1099/ijs.0.64194-0.CrossRefPubMed
43.
go back to reference Masaki T, Ohkusu K, Hata H, Fujiwara N, Iihara H, Yamada-Noda M: Mycobacterium kumamotonense Sp. Nov. recovered from clinical specimen and the first isolation report of Mycobacterium arupense in Japan: Novel slowly growing, nonchromogenic clinical isolates related to Mycobacterium terrae complex. Microbiol Immunol. 2006, 50: 889-897.CrossRefPubMed Masaki T, Ohkusu K, Hata H, Fujiwara N, Iihara H, Yamada-Noda M: Mycobacterium kumamotonense Sp. Nov. recovered from clinical specimen and the first isolation report of Mycobacterium arupense in Japan: Novel slowly growing, nonchromogenic clinical isolates related to Mycobacterium terrae complex. Microbiol Immunol. 2006, 50: 889-897.CrossRefPubMed
44.
go back to reference Lai CC, Tan CK, Chou CH, Hsu HL, Liao CH, Huang YT: Increasing incidence of nontuberculous mycobacteria, Taiwan, 2000-2008. Emerg Infect Dis. 2010, 16: 294-296.CrossRefPubMedPubMedCentral Lai CC, Tan CK, Chou CH, Hsu HL, Liao CH, Huang YT: Increasing incidence of nontuberculous mycobacteria, Taiwan, 2000-2008. Emerg Infect Dis. 2010, 16: 294-296.CrossRefPubMedPubMedCentral
45.
go back to reference Milne BW, Arnold MH, Hudson B, Coolican MR: Infectious arthritis of the knee caused by Mycobacterium terrae: a case report. J Orthop Surg (Hong Kong). 2009, 17: 103-108. Milne BW, Arnold MH, Hudson B, Coolican MR: Infectious arthritis of the knee caused by Mycobacterium terrae: a case report. J Orthop Surg (Hong Kong). 2009, 17: 103-108.
46.
go back to reference Chan TH, Ng KC, Ho A, Scheel O, Lai CK, Leung R: Urinary tract infection caused by Mycobacterium terrae complex. Tuber Lung Dis. 1996, 77: 555-557. 10.1016/S0962-8479(96)90055-6.CrossRefPubMed Chan TH, Ng KC, Ho A, Scheel O, Lai CK, Leung R: Urinary tract infection caused by Mycobacterium terrae complex. Tuber Lung Dis. 1996, 77: 555-557. 10.1016/S0962-8479(96)90055-6.CrossRefPubMed
47.
go back to reference Alvarez-Uria G: Lung disease caused by nontuberculous mycobacteria. Curr Opin Pulm Med. 2010, 16: 251-256.PubMed Alvarez-Uria G: Lung disease caused by nontuberculous mycobacteria. Curr Opin Pulm Med. 2010, 16: 251-256.PubMed
48.
go back to reference Muwonge A, Kankya C, Godfroid J, Djonne B, Opuda-Asibo J, Biffa D, Takele A, Munyeme M, Skjerve E: Prevalence and associated risk factors of mycobacterial infections in slaughter pigs from Mubende district in Uganda. Trop Anim Health Prod. 2010, 42: 905-913. 10.1007/s11250-009-9506-5.CrossRefPubMed Muwonge A, Kankya C, Godfroid J, Djonne B, Opuda-Asibo J, Biffa D, Takele A, Munyeme M, Skjerve E: Prevalence and associated risk factors of mycobacterial infections in slaughter pigs from Mubende district in Uganda. Trop Anim Health Prod. 2010, 42: 905-913. 10.1007/s11250-009-9506-5.CrossRefPubMed
49.
go back to reference Muller B, de Klerk-Lorist LM, Henton MM, Lane E, Parsons S, Gey van Pittius NC, Kotze A, van Helden PD, Tanner M: Mixed infections of Corynebacterium pseudotuberculosis and non-tuberculous mycobacteria in South African antelopes presenting with tuberculosis-like lesions. Vet Microbiol. 2010 Muller B, de Klerk-Lorist LM, Henton MM, Lane E, Parsons S, Gey van Pittius NC, Kotze A, van Helden PD, Tanner M: Mixed infections of Corynebacterium pseudotuberculosis and non-tuberculous mycobacteria in South African antelopes presenting with tuberculosis-like lesions. Vet Microbiol. 2010
50.
go back to reference Cosivi O, Grange JM, Daborn CJ, Raviglione MC, Fujikura T, Cousins D, Robnison RA, Huchzermeyer HF, de Kantor I, Meslin FX: Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerg Infect Dis. 1998, 4: 59-70. 10.3201/eid0401.980108.CrossRefPubMedPubMedCentral Cosivi O, Grange JM, Daborn CJ, Raviglione MC, Fujikura T, Cousins D, Robnison RA, Huchzermeyer HF, de Kantor I, Meslin FX: Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerg Infect Dis. 1998, 4: 59-70. 10.3201/eid0401.980108.CrossRefPubMedPubMedCentral
Metadata
Title
Isolation of non-tuberculous mycobacteria from pastoral ecosystems of Uganda: Public Health significance
Authors
Clovice Kankya
Adrian Muwonge
Berit Djønne
Musso Munyeme
John Opuda-Asibo
Eystein Skjerve
James Oloya
Vigdis Edvardsen
Tone B Johansen
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2011
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/1471-2458-11-320

Other articles of this Issue 1/2011

BMC Public Health 1/2011 Go to the issue