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Published in: BMC Infectious Diseases 1/2015

Open Access 01-12-2015 | Research article

Investigation of the high rates of extrapulmonary tuberculosis in Ethiopia reveals no single driving factor and minimal evidence for zoonotic transmission of Mycobacterium bovis infection

Authors: Stefan Berg, Esther Schelling, Elena Hailu, Rebuma Firdessa, Balako Gumi, Girume Erenso, Endalamaw Gadisa, Araya Mengistu, Meseret Habtamu, Jemal Hussein, Teklu Kiros, Shiferaw Bekele, Wondale Mekonnen, Yohannes Derese, Jakob Zinsstag, Gobena Ameni, Sebastien Gagneux, Brian D Robertson, Rea Tschopp, Glyn Hewinson, Lawrence Yamuah, Stephen V Gordon, Abraham Aseffa

Published in: BMC Infectious Diseases | Issue 1/2015

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Abstract

Background

Ethiopia, a high tuberculosis (TB) burden country, reports one of the highest incidence rates of extra-pulmonary TB dominated by cervical lymphadenitis (TBLN). Infection with Mycobacterium bovis has previously been excluded as the main reason for the high rate of extrapulmonary TB in Ethiopia.

Methods

Here we examined demographic and clinical characteristics of 953 pulmonary (PTB) and 1198 TBLN patients visiting 11 health facilities in distinct geographic areas of Ethiopia. Clinical characteristics were also correlated with genotypes of the causative agent, Mycobacterium tuberculosis.

Results

No major patient or bacterial strain factor could be identified as being responsible for the high rate of TBLN, and there was no association with HIV infection. However, analysis of the demographic data of involved patients showed that having regular and direct contact with live animals was more associated with TBLN than with PTB, although no M. bovis was isolated from patients with TBLN. Among PTB patients, those infected with Lineage 4 reported “contact with other TB patient” more often than patients infected with Lineage 3 did (OR = 1.6, CI 95% 1.0-2.7; p = 0.064). High fever, in contrast to low and moderate fever, was significantly associated with Lineage 4 (OR = 2.3; p = 0.024). On the other hand, TBLN cases infected with Lineage 4 tended to get milder symptoms overall for the constitutional symptoms than those infected with Lineage 3.

Conclusions

The study suggests a complex role for multiple interacting factors in the epidemiology of extrapulmonary TB in Ethiopia, including factors that can only be derived from population-based studies, which may prove to be significant for TB control in Ethiopia.
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Literature
2.
go back to reference Black TC, Chapman JS, German JL. Tuberculosis of superficial lymph nodes. Diseases of the Chest. 1956;30(3):326–37.CrossRefPubMed Black TC, Chapman JS, German JL. Tuberculosis of superficial lymph nodes. Diseases of the Chest. 1956;30(3):326–37.CrossRefPubMed
3.
go back to reference Fontanilla J-M, Barnes A, von Reyn F. Current diagnosis and management of peripheral tuberculous lymphadenitis. Clin Infect Dis. 2011;53:555–62.CrossRefPubMed Fontanilla J-M, Barnes A, von Reyn F. Current diagnosis and management of peripheral tuberculous lymphadenitis. Clin Infect Dis. 2011;53:555–62.CrossRefPubMed
4.
go back to reference Sunder S, Lanotte P, Godreuil S, Martin C, Boschiroli M, Besnier JM. Human-to-human transmission of tuberculosis caused by mycobacterium bovis in immunocompetent patients. J Clin Microbiol. 2009;47(4):1249–51.CrossRefPubMedPubMedCentral Sunder S, Lanotte P, Godreuil S, Martin C, Boschiroli M, Besnier JM. Human-to-human transmission of tuberculosis caused by mycobacterium bovis in immunocompetent patients. J Clin Microbiol. 2009;47(4):1249–51.CrossRefPubMedPubMedCentral
5.
go back to reference Grange JM. Mycobacterium bovis infection in human beings. Tuberculosis (Edinb). 2001;81(1–2):71–7.CrossRef Grange JM. Mycobacterium bovis infection in human beings. Tuberculosis (Edinb). 2001;81(1–2):71–7.CrossRef
7.
go back to reference Berg S, Firdessa R, Habtamu M, Gadisa E, Mengistu A, Yamuah L, et al. The burden of mycobacterial disease in ethiopian cattle: implications for public health. PLoS One. 2009;4(4):e5068.CrossRefPubMedPubMedCentral Berg S, Firdessa R, Habtamu M, Gadisa E, Mengistu A, Yamuah L, et al. The burden of mycobacterial disease in ethiopian cattle: implications for public health. PLoS One. 2009;4(4):e5068.CrossRefPubMedPubMedCentral
8.
go back to reference Shitaye JETW, Pavlik I. Bovine tuberculosis infection in animal and human populations in Ethiopia: a review. Veterinarni Medicina. 2007;52(8):317–32. Shitaye JETW, Pavlik I. Bovine tuberculosis infection in animal and human populations in Ethiopia: a review. Veterinarni Medicina. 2007;52(8):317–32.
9.
go back to reference Elias K, Hussein D, Asseged B, Wondwossen T, Gebeyehu M. Status of bovine tuberculosis in Addis Ababa dairy farms. Rev Sci Tech. 2008;27(3):915–23.PubMed Elias K, Hussein D, Asseged B, Wondwossen T, Gebeyehu M. Status of bovine tuberculosis in Addis Ababa dairy farms. Rev Sci Tech. 2008;27(3):915–23.PubMed
10.
go back to reference Ameni G, Aseffa A, Engers H, Young D, Gordon S, Hewinson G, et al. High prevalence and increased severity of pathology of bovine tuberculosis in Holsteins compared to zebu breeds under field cattle husbandry in central Ethiopia. Clin Vaccine Immunol. 2007;14(10):1356–61.CrossRefPubMedPubMedCentral Ameni G, Aseffa A, Engers H, Young D, Gordon S, Hewinson G, et al. High prevalence and increased severity of pathology of bovine tuberculosis in Holsteins compared to zebu breeds under field cattle husbandry in central Ethiopia. Clin Vaccine Immunol. 2007;14(10):1356–61.CrossRefPubMedPubMedCentral
11.
go back to reference Firdessa R, Tschopp R, Wubete A, Sombo M, Hailu E, Erenso G, et al. High prevalence of bovine tuberculosis in dairy cattle in central ethiopia: implications for the dairy industry and public health. PLoS One. 2012;7(12):e52851.CrossRefPubMedPubMedCentral Firdessa R, Tschopp R, Wubete A, Sombo M, Hailu E, Erenso G, et al. High prevalence of bovine tuberculosis in dairy cattle in central ethiopia: implications for the dairy industry and public health. PLoS One. 2012;7(12):e52851.CrossRefPubMedPubMedCentral
12.
go back to reference Firdessa R, Berg S, Hailu E, Schelling E, Gumi B, Erenso G, et al. Mycobacterial lineages causing pulmonary and extrapulmonary tuberculosis. Ethiopia Emerg Infect Dis. 2013;19(3):460–3.CrossRefPubMed Firdessa R, Berg S, Hailu E, Schelling E, Gumi B, Erenso G, et al. Mycobacterial lineages causing pulmonary and extrapulmonary tuberculosis. Ethiopia Emerg Infect Dis. 2013;19(3):460–3.CrossRefPubMed
13.
go back to reference FMoH. National guideline for Lab, HIV testing in blood safely, surveillance, VCT and ARV use. Addis Ababa, Ethiopia: Federal Ministry of Health; 2003. FMoH. National guideline for Lab, HIV testing in blood safely, surveillance, VCT and ARV use. Addis Ababa, Ethiopia: Federal Ministry of Health; 2003.
14.
go back to reference Gallagher J, Horwill DM. A selective oleic acid albumin agar medium for the cultivation of Mycobacterium bovis. Journal of Hygiene. 1977;79(1):155–60.CrossRefPubMedPubMedCentral Gallagher J, Horwill DM. A selective oleic acid albumin agar medium for the cultivation of Mycobacterium bovis. Journal of Hygiene. 1977;79(1):155–60.CrossRefPubMedPubMedCentral
15.
go back to reference Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, Homolka S, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6(12):e311.CrossRefPubMedPubMedCentral Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, Homolka S, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6(12):e311.CrossRefPubMedPubMedCentral
16.
go back to reference Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35(4):907–14.PubMedPubMedCentral Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35(4):907–14.PubMedPubMedCentral
17.
go back to reference Iwnetu R, van den Hombergh J, Woldeamanuel Y, Asfaw M, Gebrekirstos C, Negussie Y, et al. Is tuberculous lymphadenitis over-diagnosed in Ethiopia? Comparative performance of diagnostic tests for mycobacterial lymphadenitis in a high-burden country. Scand J Infect Dis. 2009;41(6–7):462–8.CrossRefPubMed Iwnetu R, van den Hombergh J, Woldeamanuel Y, Asfaw M, Gebrekirstos C, Negussie Y, et al. Is tuberculous lymphadenitis over-diagnosed in Ethiopia? Comparative performance of diagnostic tests for mycobacterial lymphadenitis in a high-burden country. Scand J Infect Dis. 2009;41(6–7):462–8.CrossRefPubMed
18.
go back to reference Lin JN, Lai CH, Chen YH, Lee SS, Tsai SS, Huang CK, et al. Risk factors for extra-pulmonary tuberculosis compared to pulmonary tuberculosis. Int J Tuberc Lung Dis. 2009;13(5):620–5.PubMed Lin JN, Lai CH, Chen YH, Lee SS, Tsai SS, Huang CK, et al. Risk factors for extra-pulmonary tuberculosis compared to pulmonary tuberculosis. Int J Tuberc Lung Dis. 2009;13(5):620–5.PubMed
19.
go back to reference Yang Z, Kong Y, Wilson F, Foxman B, Fowler AH, Marrs CF, et al. Identification of risk factors for extrapulmonary tuberculosis. Clin Infect Dis. 2004;38(2):199–205.CrossRefPubMed Yang Z, Kong Y, Wilson F, Foxman B, Fowler AH, Marrs CF, et al. Identification of risk factors for extrapulmonary tuberculosis. Clin Infect Dis. 2004;38(2):199–205.CrossRefPubMed
20.
go back to reference Tschopp R, Schelling E, Hattendorf J, Young D, Aseffa A, Zinsstag J. Repeated cross-sectional skin testing for bovine tuberculosis in cattle kept in a traditional husbandry system in Ethiopia. Vet Rec. 2010;167(7):250–6.CrossRefPubMed Tschopp R, Schelling E, Hattendorf J, Young D, Aseffa A, Zinsstag J. Repeated cross-sectional skin testing for bovine tuberculosis in cattle kept in a traditional husbandry system in Ethiopia. Vet Rec. 2010;167(7):250–6.CrossRefPubMed
21.
go back to reference Gumi B, Schelling E, Firdessa R, Aseffa A, Tschopp R, Yamuah L, et al. Prevalence of bovine tuberculosis in pastoral cattle herds in the Oromia region, southern Ethiopia. Trop Anim Health Prod. 2011;43(6):1081–7.CrossRefPubMed Gumi B, Schelling E, Firdessa R, Aseffa A, Tschopp R, Yamuah L, et al. Prevalence of bovine tuberculosis in pastoral cattle herds in the Oromia region, southern Ethiopia. Trop Anim Health Prod. 2011;43(6):1081–7.CrossRefPubMed
22.
go back to reference de la Rua-Domenech R. Human mycobacterium bovis infection in the United Kingdom: incidence, risks, control measures and review of the zoonotic aspects of bovine tuberculosis. Tuberculosis (Edinb). 2006;86(2):77–109.CrossRef de la Rua-Domenech R. Human mycobacterium bovis infection in the United Kingdom: incidence, risks, control measures and review of the zoonotic aspects of bovine tuberculosis. Tuberculosis (Edinb). 2006;86(2):77–109.CrossRef
23.
go back to reference Hardie RM, Watson JM. Mycobacterium bovis in England and Wales: past, present and future. Epidemiol Infect. 1992;109(1):23–33.PubMedPubMedCentral Hardie RM, Watson JM. Mycobacterium bovis in England and Wales: past, present and future. Epidemiol Infect. 1992;109(1):23–33.PubMedPubMedCentral
24.
go back to reference Rakotosamimanana N, Raharimanga V, Andriamandimby SF, Soares JL, Doherty TM, Ratsitorahina M, et al. Variation in gamma interferon responses to different infecting strains of Mycobacterium tuberculosis in acid-fast bacillus smear-positive patients and household contacts in Antananarivo, Madagascar. Clin Vaccine Immunol. 2010;17(7):1094–103.CrossRefPubMedPubMedCentral Rakotosamimanana N, Raharimanga V, Andriamandimby SF, Soares JL, Doherty TM, Ratsitorahina M, et al. Variation in gamma interferon responses to different infecting strains of Mycobacterium tuberculosis in acid-fast bacillus smear-positive patients and household contacts in Antananarivo, Madagascar. Clin Vaccine Immunol. 2010;17(7):1094–103.CrossRefPubMedPubMedCentral
25.
go back to reference Ouassa T, Borroni E, Loukou GY, Faye-Kette H, Kouakou J, et al. High prevalence of shared international type 53 among Mycobacterium tuberculosis complex strains in retreated patients from Côte d’Ivoire. PLoS ONE. 2012;7(9):e45363. doi:10.1371/journal.pone.0045363.CrossRefPubMedPubMedCentral Ouassa T, Borroni E, Loukou GY, Faye-Kette H, Kouakou J, et al. High prevalence of shared international type 53 among Mycobacterium tuberculosis complex strains in retreated patients from Côte d’Ivoire. PLoS ONE. 2012;7(9):e45363. doi:10.1371/journal.pone.0045363.CrossRefPubMedPubMedCentral
26.
go back to reference Rocha A, Elias AR, Sobral LF, Soares DF, Santos AC, Marsico AG, et al. Genotyping did not evidence any contribution of Mycobacterium bovis to human tuberculosis in Brazil. Tuberculosis (Edinb). 2011;91(1):14–21.CrossRef Rocha A, Elias AR, Sobral LF, Soares DF, Santos AC, Marsico AG, et al. Genotyping did not evidence any contribution of Mycobacterium bovis to human tuberculosis in Brazil. Tuberculosis (Edinb). 2011;91(1):14–21.CrossRef
27.
go back to reference Diguimbaye C, Hilty M, Ngandolo R, Mahamat HH, Pfyffer GE, Baggi F, et al. Molecular characterization and drug resistance testing of Mycobacterium tuberculosis isolates from Chad. J Clin Microbiol. 2006;44(4):1575–7.CrossRefPubMedPubMedCentral Diguimbaye C, Hilty M, Ngandolo R, Mahamat HH, Pfyffer GE, Baggi F, et al. Molecular characterization and drug resistance testing of Mycobacterium tuberculosis isolates from Chad. J Clin Microbiol. 2006;44(4):1575–7.CrossRefPubMedPubMedCentral
28.
go back to reference Quirin R, Rasolofo V, Andriambololona R, Ramboasolo A, Rasolonavalona T, Raharisolo C, et al. Validity of intradermal tuberculin testing for the screening of bovine tuberculosis in Madagascar. Onderstepoort J Vet Res. 2001;68(3):231–8.PubMed Quirin R, Rasolofo V, Andriambololona R, Ramboasolo A, Rasolonavalona T, Raharisolo C, et al. Validity of intradermal tuberculin testing for the screening of bovine tuberculosis in Madagascar. Onderstepoort J Vet Res. 2001;68(3):231–8.PubMed
29.
go back to reference Nassar AF, Miyashiro S, Oliveira CG, Pacheco WA, Ogata RA. Isolation and identification of bovine tuberculosis in a Brazilian herd (São Paulo). Mem Inst Oswaldo Cruz. 2007;102(5):639–42.CrossRefPubMed Nassar AF, Miyashiro S, Oliveira CG, Pacheco WA, Ogata RA. Isolation and identification of bovine tuberculosis in a Brazilian herd (São Paulo). Mem Inst Oswaldo Cruz. 2007;102(5):639–42.CrossRefPubMed
30.
go back to reference Franco MM, Paes AC, Ribeiro MG, de Figueiredo Pantoja JC, Santos AC, Miyata M, et al. Occurrence of mycobacteria in bovine milk samples from both individual and collective bulk tanks at farms and informal markets in the southeast region of Sao Paulo, Brazil. BMC Vet Res. 2013;24(9):85. doi:10.1186/1746-6148-9-85.CrossRef Franco MM, Paes AC, Ribeiro MG, de Figueiredo Pantoja JC, Santos AC, Miyata M, et al. Occurrence of mycobacteria in bovine milk samples from both individual and collective bulk tanks at farms and informal markets in the southeast region of Sao Paulo, Brazil. BMC Vet Res. 2013;24(9):85. doi:10.1186/1746-6148-9-85.CrossRef
31.
go back to reference Müller B, Dürr S, Alonso S, Hattendorf J, Laisse CJ, Parsons SD, et al. Zoonotic Mycobacterium bovis-induced tuberculosis in humans. Emerg Infect Dis. 2013;19(6):899–908. doi:10.3201/eid1906.120543.CrossRefPubMedPubMedCentral Müller B, Dürr S, Alonso S, Hattendorf J, Laisse CJ, Parsons SD, et al. Zoonotic Mycobacterium bovis-induced tuberculosis in humans. Emerg Infect Dis. 2013;19(6):899–908. doi:10.3201/eid1906.120543.CrossRefPubMedPubMedCentral
32.
go back to reference Diguimbaye-Djaibe C, Hilty M, Ngandolo R, Mahamat HH, Pfyffer GE, Baggi F, et al. Mycobacterium bovis isolates from tuberculous lesions in Chadian zebu carcasses. Emerg Infect Dis. 2006;12(5):769–71.CrossRefPubMedPubMedCentral Diguimbaye-Djaibe C, Hilty M, Ngandolo R, Mahamat HH, Pfyffer GE, Baggi F, et al. Mycobacterium bovis isolates from tuberculous lesions in Chadian zebu carcasses. Emerg Infect Dis. 2006;12(5):769–71.CrossRefPubMedPubMedCentral
33.
go back to reference Milian-Suazo F, Perez-Guerrero L, Arriaga-Diaz C, Escartin-Chavez M. Molecular epidemiology of human cases of tuberculosis by Mycobacterium bovis in Mexico. Prev Vet Med. 2010;97(1):37–44.CrossRefPubMed Milian-Suazo F, Perez-Guerrero L, Arriaga-Diaz C, Escartin-Chavez M. Molecular epidemiology of human cases of tuberculosis by Mycobacterium bovis in Mexico. Prev Vet Med. 2010;97(1):37–44.CrossRefPubMed
34.
go back to reference Portillo-Gomez L, Sosa-Iglesias EG. Molecular identification of Mycobacterium bovis and the importance of zoonotic tuberculosis in Mexican patients. Int J Tuberc Lung Dis. 2011;15(10):1409–14.CrossRefPubMed Portillo-Gomez L, Sosa-Iglesias EG. Molecular identification of Mycobacterium bovis and the importance of zoonotic tuberculosis in Mexican patients. Int J Tuberc Lung Dis. 2011;15(10):1409–14.CrossRefPubMed
35.
go back to reference Tsegaye A, Aseffa A, Mache A, Mengistu Y, Berg S, Ameni G. Conventional and Molecular Epidemiology of bovine tuberculosis in dairy farms in Addis Ababa City, the capital of Ethiopia. J Appl Res Vet Med. 2010;8(2):143–51. Tsegaye A, Aseffa A, Mache A, Mengistu Y, Berg S, Ameni G. Conventional and Molecular Epidemiology of bovine tuberculosis in dairy farms in Addis Ababa City, the capital of Ethiopia. J Appl Res Vet Med. 2010;8(2):143–51.
37.
go back to reference Teo J, Jureen R, Chiang D, Chan D, Lin R. Comparison of two nucleic acid amplification assays, the Xpert MTB/RIF assay and the amplified Mycobacterium tuberculosis direct assay, for detection of Mycobacterium tuberculosis in respiratory and nonrespiratory specimens. J Clin Microbiol. 2011;49(10):3659–62.CrossRefPubMedPubMedCentral Teo J, Jureen R, Chiang D, Chan D, Lin R. Comparison of two nucleic acid amplification assays, the Xpert MTB/RIF assay and the amplified Mycobacterium tuberculosis direct assay, for detection of Mycobacterium tuberculosis in respiratory and nonrespiratory specimens. J Clin Microbiol. 2011;49(10):3659–62.CrossRefPubMedPubMedCentral
38.
go back to reference Virtanen S. A study of nitrate reduction by mycobacteria. The use of the nitrate reduction test in the identification of mycobacteria. Acta tuberculosea Scandinavica Supplementum. 1960;48:1–119.PubMed Virtanen S. A study of nitrate reduction by mycobacteria. The use of the nitrate reduction test in the identification of mycobacteria. Acta tuberculosea Scandinavica Supplementum. 1960;48:1–119.PubMed
39.
go back to reference Wayne LG. Simple pyrazinamidase and urease tests for routine identification of mycobacteria. Am Rev Respir Dis. 1974;109(1):147–51.PubMed Wayne LG. Simple pyrazinamidase and urease tests for routine identification of mycobacteria. Am Rev Respir Dis. 1974;109(1):147–51.PubMed
40.
go back to reference Witebsky FG, Kruczak-Filipov P. Identification of mycobacteria by conventional methods. Clin Lab Med. 1996;16(3):569–601.PubMed Witebsky FG, Kruczak-Filipov P. Identification of mycobacteria by conventional methods. Clin Lab Med. 1996;16(3):569–601.PubMed
41.
go back to reference Kubica T, Agzamova R, Wright A, Rakishev G, Rusch-Gerdes S, Niemann S. Mycobacterium bovis isolates with M. tuberculosis specific characteristics. Emerg Infect Dis. 2006;12(5):763–5.CrossRefPubMedPubMedCentral Kubica T, Agzamova R, Wright A, Rakishev G, Rusch-Gerdes S, Niemann S. Mycobacterium bovis isolates with M. tuberculosis specific characteristics. Emerg Infect Dis. 2006;12(5):763–5.CrossRefPubMedPubMedCentral
42.
go back to reference Ameni G, Vordermeier M, Firdessa R, Aseffa A, Hewinson G, Gordon SV, et al. Mycobacterium tuberculosis infection in grazing cattle in central Ethiopia. Vet J. 2011;188(3):359–61.CrossRefPubMedPubMedCentral Ameni G, Vordermeier M, Firdessa R, Aseffa A, Hewinson G, Gordon SV, et al. Mycobacterium tuberculosis infection in grazing cattle in central Ethiopia. Vet J. 2011;188(3):359–61.CrossRefPubMedPubMedCentral
43.
go back to reference Ameni G, Tadesse K, Hailu E, Deresse Y, Medhin G, Aseffa A, et al. Transmission of Mycobacterium tuberculosis between farmers and cattle in central Ethiopia. PLoS One. 2013;8(10):e76891.CrossRefPubMedPubMedCentral Ameni G, Tadesse K, Hailu E, Deresse Y, Medhin G, Aseffa A, et al. Transmission of Mycobacterium tuberculosis between farmers and cattle in central Ethiopia. PLoS One. 2013;8(10):e76891.CrossRefPubMedPubMedCentral
44.
go back to reference Srivastava K, Chauhan DS, Gupta P, Singh HB, Sharma VD, Yadav VS, et al. Isolation of Mycobacterium bovis & M. tuberculosis from cattle of some farms in north India--possible relevance in human health. Indian J Med Res. 2008;128(1):26–31.PubMed Srivastava K, Chauhan DS, Gupta P, Singh HB, Sharma VD, Yadav VS, et al. Isolation of Mycobacterium bovis & M. tuberculosis from cattle of some farms in north India--possible relevance in human health. Indian J Med Res. 2008;128(1):26–31.PubMed
45.
go back to reference Caws M, Thwaites G, Dunstan S, Hawn TR, Lan NT, Thuong NT, et al. The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog. 2008;4(3):e1000034.CrossRefPubMedPubMedCentral Caws M, Thwaites G, Dunstan S, Hawn TR, Lan NT, Thuong NT, et al. The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog. 2008;4(3):e1000034.CrossRefPubMedPubMedCentral
46.
go back to reference Lari N, Rindi L, Cristofani R, Rastogi N, Tortoli E, Garzelli C. Association of Mycobacterium tuberculosis complex isolates of BOVIS and Central Asian (CAS) genotypic lineages with extrapulmonary disease. Clin Microbiol Infect. 2009;15(6):538–43.CrossRefPubMed Lari N, Rindi L, Cristofani R, Rastogi N, Tortoli E, Garzelli C. Association of Mycobacterium tuberculosis complex isolates of BOVIS and Central Asian (CAS) genotypic lineages with extrapulmonary disease. Clin Microbiol Infect. 2009;15(6):538–43.CrossRefPubMed
47.
go back to reference Tsenova L, Ellison E, Harbacheuski R, Moreira AL, Kurepina N, Reed MB, et al. Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis. 2005;192(1):98–106.CrossRefPubMed Tsenova L, Ellison E, Harbacheuski R, Moreira AL, Kurepina N, Reed MB, et al. Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis. 2005;192(1):98–106.CrossRefPubMed
48.
go back to reference Reed MB, Gagneux S, Deriemer K, Small PM, Barry 3rd CE. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol. 2007;189(7):2583–9.CrossRefPubMedPubMedCentral Reed MB, Gagneux S, Deriemer K, Small PM, Barry 3rd CE. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol. 2007;189(7):2583–9.CrossRefPubMedPubMedCentral
49.
50.
go back to reference Sharaf Eldin GS, Fadl-Elmula I, Ali MS, Ali AB, Salih AL, Mallard K, et al. Tuberculosis in Sudan: a study of Mycobacterium tuberculosis strain genotype and susceptibility to anti-tuberculosis drugs. BMC Infect Dis. 2011;11:219.CrossRefPubMedPubMedCentral Sharaf Eldin GS, Fadl-Elmula I, Ali MS, Ali AB, Salih AL, Mallard K, et al. Tuberculosis in Sudan: a study of Mycobacterium tuberculosis strain genotype and susceptibility to anti-tuberculosis drugs. BMC Infect Dis. 2011;11:219.CrossRefPubMedPubMedCentral
51.
go back to reference Bem C. Human immunodeficiency virus-positive tuberculous lymphadenitis in Central Africa: clinical presentation of 157 cases. Int J Tuberc Lung Dis. 1997;1(3):215–9.PubMed Bem C. Human immunodeficiency virus-positive tuberculous lymphadenitis in Central Africa: clinical presentation of 157 cases. Int J Tuberc Lung Dis. 1997;1(3):215–9.PubMed
52.
go back to reference Bem C, Patil PS, Bharucha H, Namaambo K, Luo N. Importance of human immunodeficiency virus-associated lymphadenopathy and tuberculous lymphadenitis in patients undergoing lymph node biopsy in Zambia. Br J Surgery. 1996;83(1):75–8.CrossRef Bem C, Patil PS, Bharucha H, Namaambo K, Luo N. Importance of human immunodeficiency virus-associated lymphadenopathy and tuberculous lymphadenitis in patients undergoing lymph node biopsy in Zambia. Br J Surgery. 1996;83(1):75–8.CrossRef
53.
go back to reference Harries AD, Dye C. Tuberculosis. Ann Trop Med Parasitol. 2006;100(5–6):415–31.PubMed Harries AD, Dye C. Tuberculosis. Ann Trop Med Parasitol. 2006;100(5–6):415–31.PubMed
54.
go back to reference Yassin MA, Olobo JO, Kidane D, Negesse Y, Shimeles E, Tadesse A, et al. Diagnosis of tuberculous lymphadenitis in Butajira, rural Ethiopia. Scand J Infect Dis. 2003;35(4):240–3.CrossRefPubMed Yassin MA, Olobo JO, Kidane D, Negesse Y, Shimeles E, Tadesse A, et al. Diagnosis of tuberculous lymphadenitis in Butajira, rural Ethiopia. Scand J Infect Dis. 2003;35(4):240–3.CrossRefPubMed
55.
go back to reference Belay M, Bjune G, Ameni G, Abebe F. Diagnostic and treatment delay among Tuberculosis patients in Afar Region, Ethiopia: a cross-sectional study. BMC Public Health. 2012;12:369.CrossRefPubMedPubMedCentral Belay M, Bjune G, Ameni G, Abebe F. Diagnostic and treatment delay among Tuberculosis patients in Afar Region, Ethiopia: a cross-sectional study. BMC Public Health. 2012;12:369.CrossRefPubMedPubMedCentral
56.
go back to reference Hargreaves JR, Boccia D, Evans CA, Adato M, Petticrew M, Porter JDH. The social determinants of tuberculosis: from evidence to action. Am J Public Health. 2011;101(4):654–62.CrossRefPubMedPubMedCentral Hargreaves JR, Boccia D, Evans CA, Adato M, Petticrew M, Porter JDH. The social determinants of tuberculosis: from evidence to action. Am J Public Health. 2011;101(4):654–62.CrossRefPubMedPubMedCentral
57.
go back to reference Kivisild T, Reidla M, Metspalu E, Rosa A, Brehm A, Pennarun E, et al. Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears. Am J Hum Genet. 2004;75(5):752–70.CrossRefPubMedPubMedCentral Kivisild T, Reidla M, Metspalu E, Rosa A, Brehm A, Pennarun E, et al. Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears. Am J Hum Genet. 2004;75(5):752–70.CrossRefPubMedPubMedCentral
58.
go back to reference Lovell A, Moreau C, Yotova V, Xiao F, Bourgeois S, Gehl D, et al. Ethiopia: between Sub-Saharan Africa and western Eurasia. Ann Hum Genet. 2005;69(Pt 3):275–87.CrossRefPubMed Lovell A, Moreau C, Yotova V, Xiao F, Bourgeois S, Gehl D, et al. Ethiopia: between Sub-Saharan Africa and western Eurasia. Ann Hum Genet. 2005;69(Pt 3):275–87.CrossRefPubMed
59.
go back to reference Pareek M, Evans J, Innes J, Smith G, Hingley-Wilson S, Lougheed KE, et al. Ethnicity and mycobacterial lineage as determinants of tuberculosis disease phenotype. Thorax. 2013;68(3):221–9.CrossRefPubMed Pareek M, Evans J, Innes J, Smith G, Hingley-Wilson S, Lougheed KE, et al. Ethnicity and mycobacterial lineage as determinants of tuberculosis disease phenotype. Thorax. 2013;68(3):221–9.CrossRefPubMed
60.
go back to reference Oki NO, Motsinger-Reif AA, Antas PR, Levy S, Holland SM, Sterling TR. Novel human genetic variants associated with extrapulmonary tuberculosis: a pilot genome wide association study. BMC Res Notes. 2011;4(1):28.CrossRefPubMedPubMedCentral Oki NO, Motsinger-Reif AA, Antas PR, Levy S, Holland SM, Sterling TR. Novel human genetic variants associated with extrapulmonary tuberculosis: a pilot genome wide association study. BMC Res Notes. 2011;4(1):28.CrossRefPubMedPubMedCentral
61.
go back to reference Thye T, Vannberg FO, Wong SH, Owusu-Dabo E, Osei I, Gyapong J, et al. Genome-wide association analyses identifies a susceptibility locus for tuberculosis on chromosome 18q11.2. Nature Genet. 2010;42(9):739–41.CrossRefPubMedPubMedCentral Thye T, Vannberg FO, Wong SH, Owusu-Dabo E, Osei I, Gyapong J, et al. Genome-wide association analyses identifies a susceptibility locus for tuberculosis on chromosome 18q11.2. Nature Genet. 2010;42(9):739–41.CrossRefPubMedPubMedCentral
Metadata
Title
Investigation of the high rates of extrapulmonary tuberculosis in Ethiopia reveals no single driving factor and minimal evidence for zoonotic transmission of Mycobacterium bovis infection
Authors
Stefan Berg
Esther Schelling
Elena Hailu
Rebuma Firdessa
Balako Gumi
Girume Erenso
Endalamaw Gadisa
Araya Mengistu
Meseret Habtamu
Jemal Hussein
Teklu Kiros
Shiferaw Bekele
Wondale Mekonnen
Yohannes Derese
Jakob Zinsstag
Gobena Ameni
Sebastien Gagneux
Brian D Robertson
Rea Tschopp
Glyn Hewinson
Lawrence Yamuah
Stephen V Gordon
Abraham Aseffa
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2015
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-015-0846-7

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