A systematic review of East African-Indian family of <i>Mycobacterium tuberculosis</i> in Brazil

Duarte, Tonya Azevedo; Nery, Joilda Silva; Boechat, Neio; Pereira, Susan Martins; Simonsen, Vera; Oliveira, Martha; Gomes, Maria Gabriela Miranda; Penha-Gonçalves, Carlos; Barreto, Mauricio Lima; Barbosa, Theolis

doi:10.1016/j.bjid.2017.01.005

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Brazilian Journal of Infectious Diseases

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Original Articles • Braz J Infect Dis 21 (3) • May-Jun 2017 • https://doi.org/10.1016/j.bjid.2017.01.005 copy

A systematic review of East African-Indian family of Mycobacterium tuberculosis in Brazil

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Introduction:

The Mycobacterium tuberculosis East African-Indian (EAI) spoligotyping family (belonging to lineage 1, Indo-Oceanic, defined by the region of deletion RD239) is distributed worldwide, but is more prevalent in Southeast Asia, India, and East Africa. Studies in Latin America have rarely identified EAI. In this study, we describe the occurrence of the EAI family in Brazil.

Methods:

EAI was identified in a systematic literature review of genetic diversity studies pertaining to M. tuberculosis in Brazil, as well as in a survey conducted in Salvador, Bahia, located in the northeastern region of this country.

Results:

The EAI6-BGD1 spoligotyping family and the EAI5 Spoligotype International Type (SIT) 1983 clade were the most frequently reported, with wide distribution of this particular clade described in Brazil. The distribution of other EAI spoligotyping patterns with broader worldwide distribution was restricted to the southeastern region of the country.

Conclusions:

EAI may be endemic at a low frequency in Brazil, with some clades indicating increased fitness with respect to this population.

Keywords:
Mycobacterium tuberculosis; Phylogeography; Genotyping; Epidemiology

Genome location	Gene	Gene position and nucleotide	S or NS	Reference
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43945	Rv0041	Rv0041_384a>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
92199	Rv0083	Rv0083_188t>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
157292	Rv0129c	Rv0129c_309g>A	S	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
220050	Rv0189c	Rv0189c_1674g>A	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
311613	Rv0260c	Rv0260c_1047c>A	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
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797736	Rv0697	Rv0697_804c>T	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
918316	Rv0824c	Rv0824c_435a>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
923065	Rv0831c	Rv0831c_645a>T	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
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1068151	Rv0956	Rv0956_591t>C	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
1139222	Rv1020	Rv1020_256g>A	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
1163134	Rv1040c	Rv1040c_243a>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
1178116	Rv1056	Rv1056_489t>C	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
1477588	Rv1316c	Rv1316c_44c>G	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
1479085	Rv1317c	Rv1317c_34a>G	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
1548149	Rv1375	Rv1375_318G<A	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
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1595342	Rv1420	Rv1420_1301t>C	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
1884697	Rv1662	Rv1662_2994G>a	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
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1920120	Rv1696	Rv1696_438g>T	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
1960391	Rv1733c	Rv1733c_97c>T	NS	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
2134215	Rv1884c	Rv1884c_47a>G	S	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
2239349	Rv1996	Rv1996_346a>G	NS	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
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2627946	Rv2349c	Rv2349c_753T>c	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
2643653	Rv2362c	Rv2362c_606c>T	S	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
2825581	Rv2510c	Rv2510c_1509a>C	S	³⁶36 Niemann S, Köser CU, Gagneux S, et al. Genomic diversity among drug sensitive and multidrug resistant isolates of Mycobacterium tuberculosis with identical DNA fingerprints. PLoS ONE. 2009;4:e7407.
2880702	Rv2560	Rv2560_628g>C	NS	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
2891267	Rv2567	Rv2567_1473c>T	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
3300104	Rv2949c	Rv2949c_467g>A	NS	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
3300196	Rv2949c	Rv2949c_375c>T	S	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
3312632	Rv2959c	Rv2959c_207g>A	NS	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
3332254	Rv2976c	Rv2976c_501g>A	S	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
3335708	Rv2979c	Rv2979c_41c>G	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
3426795	Rv3062	Rv3062_1212c>G	S	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
3438386	Rv3075c	Rv3075c_588c>T	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
3440542	Rv3077	Rv3077_1002a>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
3455686	Rv3088	Rv3088_1347g>C	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
3544710	Rv3176c	Rv3176c_591a>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
3597737	Rv3221c	Rv3221c_30g>A	S	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
3641447	Rv3261	Rv3261_905c>T	NS	³³33 Hershberg R, Lipatov M, Small PM, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.
3681548	Rv3297	Rv3297_229a>C	S	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
3783058	Rv3370c	Rv3370c_1683c>T	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
4024273	Rv3581c	Rv3581c_75a>G	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
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4081996	Rv3644c	Rv3644c_726c>G	S	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
4119246	Rv3679	Rv3679_471T>c	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
4137829	Rv3695	Rv3695_624c>T	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.
4156239	Rv3711c	Rv3711c_491t>C	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
4156503	Rv3711c	Rv3711c_227g>A	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
4182695	Rv3731	Rv3731_938g>A	NS	¹³13 Dos Vultos T, Mestre O, Rauzier J, et al. Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS ONE. 2008;3:e1538.
4255922	Rv3799c	Rv3799c_27t>C	S	³⁴34 Filliol I, Motiwala AS, Cavatore M, et al. Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol. 2006;188:759-72.

Study period	Study site	Nr. of EAI isolates (%)	SIT	Spoligotype subfamily	Octal pattern	Refs.
1995-2003	Paraná	1 (14.3)	1427	EAI5	457001777413771	¹⁶16 de Freitas FAD, Bernardo V, Gomgnimbou MK, et al. Multidrug resistant Mycobacterium tuberculosis: a retrospective katG and rpoB mutation profile analysis in isolates from a reference center in Brazil. PLOS ONE. 2014;9:e104100.
1997-2005	Rio de Janeiro	1 (0.1)	11	EAI3-IND	477777777413071	²²22 Gomes HM, Elias AR, Oelemann MAC, et al. Spoligotypes of Mycobacterium tuberculosis complex isolates from patients residents of 11 states of Brazil. Infect Genet Evol. 2012;12:649-56.
1997-2005	Pernambuco	1 (1.3)	1983	EAI3-IND	474000377413031	22
			48 (N=4)	EAI1-SOM	777777777413731
			702 (N=4)	EAI6-BGD1	700775747413771
			2543 (N=2)	EAI5	773601757013371
1997-2005	Pará	15 (8.1)	129	EAI6-BGD1	700777747413771	²²22 Gomes HM, Elias AR, Oelemann MAC, et al. Spoligotypes of Mycobacterium tuberculosis complex isolates from patients residents of 11 states of Brazil. Infect Genet Evol. 2012;12:649-56.
1997-2005	Pará	15 (8.1)	924	EAI5	777600007413371
			Orphan	EAI5	777600007413771
			Orphan	EAI6-BGD1	700776747413771
			Orphan	EAI6-BGD1	700677747413771	¹⁸18 Gomes T, Vinhas SA, Reis-Santos B, et al. Extrapulmonary tuberculosis: Mycobacterium tuberculosis strains and host risk factors in a large urban setting in Brazil. PLoS ONE. 2013;8:e74517.
1998-2007	Espírito Santo	1 (0.2)	1983	EAI5	474000377413031
			Orphan	Orphan	437777777413071
			Orphan	Orphan	500777747413771
			129 (N=5)	EAI6-BGD1	700777747413771
2000-2003	Pará	11 (15.3)	Orphan	Orphan	700677747413771	²⁴24 Cardoso Oelemann M, Gomes HM, Willery E, et al. The forest behind the tree: phylogenetic exploration of a dominant Mycobacterium tuberculosis strain lineage from a high tuberculosis burden country. PLoS ONE. 2011;6:e18256.
			Orphan	EAI6-BGD1	777777747413731
				/EAI1-SOM^a a Ambiguous.
			Orphan (N=2)	EAI5	777600007413771
2000-2010	Espírito Santo	1 (0.2)	1983	EAI5	474000377413031	²⁰20 Vinhas SA, Palaci M, Marques HS, et al. Mycobacterium tuberculosis DNA fingerprint clusters and its relationship with RDRio genotype in Brazil. Tuberculosis. 2013;93:207-12.
2001-2002	São Paulo	1 (2.5)	48	EAI1-SOM	777777777413731	¹⁷17 Martins MC, Giampaglia CMS, Chimara E, et al. Viability of stressed Mycobacterium tuberculosis and association with multidrug resistance. Braz J Microbiol. 2013;44:465-8.
2002-2003	Rio de Janeiro	1 (0.3)	11	EAI3-IND	477777777413071	²⁷27 Lazzarini LCO, Huard RC, Boechat NL, et al. Discovery of a novel Mycobacterium tuberculosis lineage that is a major cause of tuberculosis in Rio de Janeiro, Brazil. J Clin Microbiol. 2007;45:3891-902.
2004	Minas Gerais	1 (0.9)	1983	EAI3-IND	474000377413031	²³23 Miranda SSde, Carvalho W da S, Suffys PN, et al. Spoligotyping of clinical Mycobacterium tuberculosis isolates from the state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2011;106:267-73.
2005-2006	Rio Grande do Sul	1 (2.0)	1435	EAI1-SOM	774777777413731	²⁶26 Von Groll A, Martin A, Felix C, et al. Fitness study of the RDRio lineage and Latin American-Mediterranean family of Mycobacterium tuberculosis in the city of Rio Grande, Brazil. FEMS Immunol Med Microbiol. 2010;58:119-27.
2005-2008	Paraná	1 (1.4)	48	EAI1-SOM	777777777413731^b b Pattern retrieved from the SITVIT WEB based on the SIT informed by the authors.	²⁵25 Noguti EN, Leite CQF, Malaspina AC, et al. Genotyping of Mycobacterium tuberculosis isolates from a low-endemic setting in northwestern state of Paraná in Southern Brazil. Memórias Do Instituto Oswaldo Cruz. 2010;105:779-85.
			Orphan	Orphan	777617705413371
2006-2008	São Paulo	4 (0.5)	11	EAI3-IND	477777777413071	²¹21 Martins MC, Giampaglia CMS, Oliveira RS, et al. Population structure and circulating genotypes of drug-sensitive and drug-resistant Mycobacterium tuberculosis clinical isolates in São Paulo state, Brazil. Infect Genet Evol. 2013;14:39-45.
			1983 (N=2)	EAI5	474000377413031
2007-2008	Fortaleza	2 (1.7)	NA	EAI5^c c As described by the authors.	NA	¹⁹19 Luiz RDSS, Suffys P, Barroso EC, et al. Genotyping and drug resistance patterns of Mycobacterium tuberculosis strains observed in a tuberculosis high-burden municipality in Northeast, Brazil. Braz J Infect Dis. 2013;17:338-45.
2008-2009	Rio de Janeiro	1 (0.5)	Orphan	EAI	777741777413600	¹⁵15 Vasconcellos SEG, Acosta CC, Gomes LL, et al. Strain classification of Mycobacterium tuberculosis isolates in Brazil based on genotypes obtained by spoligotyping, mycobacterial interspersed repetitive unit typing and the presence of large sequence and single nucleotide polymorphism. PLOS ONE. 2014;9:e107747.
2010-2011	Santa Catarina	10 (2.6)	1983	EAI5	474000377413031	¹⁴14 Nogueira CL, Prim RI, Senna SG, et al. First insight into the molecular epidemiology of Mycobacterium tuberculosis in Santa Catarina, southern Brazil. Tuberculosis (Edinb). 2016;97:57-64.
2010-2011	Santa Catarina	10 (2.6)	Orphan (N=9)	EAI5^c c As described by the authors. ,^d d No match was found in the SITVIT WEB database; the closest matches found in the MIRU-VNTRplus database pertain to the LAM family.	777777607700171

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[1] *Corresponding authors. E-mail addresses: tonya.duarte@gmail.com (T.A. Duarte), theolis@bahia.fiocruz.br (T. Barbosa).