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Genetic Epidemiology of Tuberculosis Susceptibility: Impact of Study Design


Several candidate gene studies have provided evidence for a role of host genetics in susceptibility to tuberculosis (TB). However, the results of these studies have been very inconsistent, even within a study population. Here, we review the design of these studies from a genetic epidemiological perspective, illustrating important differences in phenotype definition in both cases and controls, consideration of latent M. tuberculosis infection versus active TB disease, population genetic factors such as population substructure and linkage disequilibrium, polymorphism selection, and potential global differences in M. tuberculosis strain. These considerable differences between studies should be accounted for when examining the current literature. Recommendations are made for future studies to further clarify the host genetics of TB.


Vyšlo v časopise: Genetic Epidemiology of Tuberculosis Susceptibility: Impact of Study Design. PLoS Pathog 7(1): e32767. doi:10.1371/journal.ppat.1001189
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001189

Souhrn

Several candidate gene studies have provided evidence for a role of host genetics in susceptibility to tuberculosis (TB). However, the results of these studies have been very inconsistent, even within a study population. Here, we review the design of these studies from a genetic epidemiological perspective, illustrating important differences in phenotype definition in both cases and controls, consideration of latent M. tuberculosis infection versus active TB disease, population genetic factors such as population substructure and linkage disequilibrium, polymorphism selection, and potential global differences in M. tuberculosis strain. These considerable differences between studies should be accounted for when examining the current literature. Recommendations are made for future studies to further clarify the host genetics of TB.


Zdroje

1. RaviglioneM

SniderD

KochiA

1995 Global epidemiology of tuberculosis: morbidity and mortality of a worldwide epidemic. JAMA 273 220 226

2. KaufmannSH

BaumannS

NasserEA

2006 Exploiting immunology and molecular genetics for rational vaccine design against tuberculosis. Int J Tuberc Lung Dis 10 1068 1079

3. ComstockG

1978 Tuberculosis in twins: a re-analysis of the Prophit Study. Am Rev Resp Dis 117 621 624

4. KallmannF

ReisnerD

1943 Twin studies on the significance of genetic factors in tuberculosis. Am Rev Tuberculosis 47 549 574

5. BlackwellJ

BartonC

WhiteJ

SearleS

BakerA

WilliamsH

ShawM

2004 Genomic organizaton and sequence of the human NRAMP gene: identification and mapping of a promotor region polymorphism. Mol Med 1 194 205

6. FlynnJ

GoldsteinM

ChanJ

TrieboldK

PfefferK

LowensteinC

SchreiberR

MakT

BloomB

1995 Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2 561 572

7. KramnikI

DietrickW

DemantP

BloomB

2000 Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. Proc Natl Acad Sci 97 8560 8565

8. LurieM

1941 Heredity, constitution and tuberculosis: An experimental study. Am Rev Tuberc 44 1 125

9. ShawMA

CollinsA

PeacockCS

MillerEN

BlackGF

SibthorpeD

Lins-LainsonZ

ShawJJ

RamosF

SilveiraF

BlackwellJM

1997 Evidence that genetic susceptibility to Mycobacterium tuberculosis in a Brazilian population is under oligogenic control: linkage study of the candidate genes NRAMP1 and TNFA. Tuberc Lung Dis 78 35 45

10. SteinCM

NshutiL

ChiundaAB

BoomWH

ElstonRC

MugerwaRD

IyengarSK

WhalenCC

2005 Evidence for a major gene influence on tumor necrosis factor-alpha expression in tuberculosis: path and segregation analysis. Hum Hered 60 109 118

11. BellamyR

BeyersN

McAdamK

RuwendeC

GieR

SamaaiP

BesterD

MeyerM

CorrahT

CollinM

CamidgeD

WilkinsonD

Hoal-van HeldenE

WhittleH

AmosW

van HeldenP

HillA

2000 Genetic susceptibility to tuberculosis in Africans: A genome-wide scan. Proc Natl Acad Sci 97 8005 8009

12. JamiesonS

MillerE

BlackG

PeacockC

CordellH

HowsonJ

ShawM

BurgnerD

XuW

Lins-LainsonZ

RamosF

SilveiraF

BlackwellJ

2004 Evidence for a cluster of genes on chromosome 17q11-q21 controlling susceptibility to tuberculosis and leprosy in Brazilians. Genes and Immunity 5 46 57

13. MillerE

JamiesonS

JobertyC

FakiolaM

HudsonD

PeacockC

CordellH

ShawM

Lins-LainsonZ

RamosF

SilveiraF

BlackwellJ

2004 Genome-wide scans for leprosy and tuberculosis susceptibility genes in Brazilians. Genes Immun 5 63 67

14. CookeGS

CampbellSJ

BennettS

LienhardtC

McAdamKP

SowO

GustafsonP

MwanguluF

vanHP

FineP

HoalEG

HillAV

2008 Mapping of a Novel Susceptibility Locus Suggests a Role for MC3R and CTSZ in Human Tuberculosis. Am J Respir Crit Care Med 178 203 207

15. SteinCM

ZalwangoS

MaloneLL

WonS

Mayanja-KizzaH

MugerwaRD

LeontievDV

ThompsonCL

CartierKC

ElstonRC

IyengarSK

BoomWH

WhalenCC

2008 Genome scan of M. tuberculosis infection and disease in Ugandans. PLoS ONE 3 e4094 doi:10.1371/journal.pone.0004094

16. BaghdadiJE

OrlovaM

AlterA

RanqueB

ChentoufiM

LazrakF

ArchaneMI

CasanovaJL

BenslimaneA

SchurrE

AbelL

2006 An autosomal dominant major gene confers predisposition to pulmonary tuberculosis in adults. J Exp Med 203 1679 1684

17. MahasirimongkolS

YanaiH

NishidaN

RidruechaiC

MatsushitaI

OhashiJ

SummanapanS

YamadaN

MoolphateS

ChuchotawornC

ChaiprasertA

ManosuthiW

KantipongP

KanitwittayaS

SuraT

KhusmithS

TokunagaK

SawanpanyalertP

KeichoN

2009 Genome-wide SNP-based linkage analysis of tuberculosis in Thais. Genes Immun 10 77 83

18. ComstockG

1982 Epidemiology of tuberculosis. Am Rev Resp Dis 125 8 15

19. [No authors listed] 2000 Diagnostic Standards and Classification of Tuberculosis in Adults and Children. This official statement of the American Thoracic Society and the Centers for Disease Control and Prevention was adopted by the ATS Board of Directors, July 1999. This statement was endorsed by the Council of the Infectious Disease Society of America, September 1999. Am J Respir Crit Care Med 161 1376 1395

20. NyendakM

LewinsohnDA

LewinsohnD

2008 The use of interferon-gamma release assays in clinical practice.

DaviesP

BarnesPF

GordonSB

Clinical tuberculosis London Hodder Arnold

21. GarayS

2004 Pulmonary tuberculosis.

RomWN

GaraySM

Tuberculosis Philadelphia Lippincott Williams & Wilkins 345 394

22. MollerM

de WitE

HoalEG

2010 Past, present and future directions in human genetic susceptibility to tuberculosis. FEMS Immunol Med Microbiol 58 3 26

23. MaX

ReichR

WrightJ

TookerH

TeeterL

MusserJ

GravissE

2003 Association between Interleukin-8 gene alleles and human susceptbility to tuberculosis disease. J Infect Dis 188 349 355

24. RossouwM

NelHJ

CookeGS

van HeldenPD

HoalEG

2003 Association between tuberculosis and a polymorphic NFκB binding site in the interferon γ gene. Lancet 361 1871 1872

25. TaypeCA

CastroJC

AccinelliRA

Herrera-VelitP

ShawMA

EspinozaJR

2006 Association between SLC11A1 polymorphisms and susceptibility to different clinical forms of tuberculosis in the Peruvian population. Infect Genet Evol 6 361 367

26. VelezDR

HulmeWF

MyersJL

StryjewskiME

AbbateE

EstevanR

PatilloSG

GilbertJR

HamiltonCD

ScottWK

2009 Association of SLC11A1 with tuberculosis and interactions with NOS2A and TLR2 in African-Americans and Caucasians. Int J Tuberc Lung Dis 13 1068 1076

27. Motsinger-ReifAA

AntasPR

OkiNO

LevyS

HollandSM

SterlingTR

2010 Polymorphisms in IL-1beta, vitamin D receptor Fok1, and Toll-like receptor 2 are associated with extrapulmonary tuberculosis. BMC Med Genet 11 37

28. ThyeT

BrowneEN

ChinbuahMA

GyapongJ

OseiI

Owusu-DaboE

BrattigNW

NiemannS

Rusch-GerdesS

HorstmannRD

MeyerCG

2009 IL10 haplotype associated with tuberculin skin test response but not with pulmonary TB. PLoS ONE 4 e5420 doi:10.1371/journal.pone.0005420

29. CobatA

GallantCJ

SimkinL

BlackGF

StanleyK

HughesJ

DohertyTM

HanekomWA

EleyB

JaisJP

Boland-AugeA

vanHP

CasanovaJL

AbelL

HoalEG

SchurrE

AlcaisA

2009 Two loci control tuberculin skin test reactivity in an area hyperendemic for tuberculosis. J Exp Med 206 2583 2591

30. Flores-VillanuevaPO

Ruiz-MoralesJA

SongCH

FloresLM

JoEK

MontanoM

BarnesPF

SelmanM

GranadosJ

2005 A functional promoter polymorphism in monocyte chemoattractant protein-1 is associated with increased susceptibility to pulmonary tuberculosis. J Exp Med 202 1649 1658

31. SteinCM

ZalwangoS

ChiundaAB

MillardC

LeontievDV

HorvathAL

CartierKC

ChervenakK

BoomWH

ElstonRC

MugerwaRD

WhalenCC

IyengarSK

2007 Linkage and association analysis of candidate genes for TB and TNFalpha cytokine expression: evidence for association with IFNGR1, IL-10, and TNF receptor 1 genes. Hum Genet 121 663 673

32. HoalEG

LewisLA

JamiesonSE

TanzerF

RossouwM

VictorT

HillermanR

BeyersN

BlackwellJM

Van HeldenPD

2004 SLC11A1 (NRAMP1) but not SLC11A2 (NRAMP2) polymorphisms are associated with susceptibility to tuberculosis in a high-incidence community in South Africa. Int J Tuberc Lung Dis 8 1464 1471

33. 2007 Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447 661 678

34. EdwardsBJ

HaynesC

LevenstienMA

FinchSJ

GordonD

2005 Power and sample size calculations in the presence of phenotype errors for case/control genetic association studies. BMC Genet 6 18

35. McCarthyMI

AbecasisGR

CardonLR

GoldsteinDB

LittleJ

IoannidisJPA

HirschhornJN

2008 Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9 356 369

36. CervinoA

LakissS

SowO

HillA

2000 Allelic association between the NRAMP1 gene and susceptibility to tuberculosis in Guinea-Conakry. Ann Hum Genet 64 507 512

37. El BaghdadiJ

RemusN

BenslinaneA

El AnnazH

ChentoufiM

AbelL

SchurrE

2004 Variants of the human NRAMP1 gene and susceptibility to tuberculosis in Morocco. Int J Tuberc Lung Dis 7 599 602

38. DubaniewiczA

JamiesonSE

Dubaniewicz-WybieralskaM

FakiolaM

NancyME

BlackwellJM

2005 Association between SLC11A1 (formerly NRAMP1) and the risk of sarcoidosis in Poland. Eur J Hum Genet 13 829 834

39. ChapmanJS

DyerlyMD

1964 Social and other factors in intrafamilial transmission of tuberculosis. Am Rev Respir Dis 90 48 60

40. EnarsonD

ChiangC-Y

MurrayJ

2004 Global epidemiology of tuberculosis.

RomWN

GaraySM

Tuberculosis Philadelphia Lippincott Williams & Wilkins 13 30

41. GuwattudeD

NakakeetoM

Jones-LopezE

MagandaA

ChiundaA

MugerwaR

EllnerJ

BukenyaG

WhalenC

2003 Tuberculosis in household contacts of infectious cases in Kampala, Uganda. Am J Epidemiol 158 887 898

42. SattenGA

FlandersWD

YangQ

2001 Accounting for unmeasured population substructure in case-control studies of genetic association using a novel latent-class model. Am J Hum Genet 68 466 477

43. MarchiniJ

CardonLR

PhillipsMS

DonnellyP

2004 The effects of human population structure on large genetic association studies. Nat Genet 36 512 517

44. MaX

ReichR

GonzálezA

PanX

FothergillA

StarkeJ

TeeterL

MusserJ

GravissE

2003 No evidence for association between the polymorphism in the 3′ untranslated region of interleukin-12B and human susceptibility to tuberculosis. J Infect Dis 188 1116 1118

45. VelezDR

HulmeWF

MyersJL

WeinbergJB

LevesqueMC

StryjewskiME

AbbateE

EstevanR

PatilloSG

GilbertJR

HamiltonCD

ScottWK

2009 NOS2A, TLR4, and IFNGR1 interactions influence pulmonary tuberculosis susceptibility in African-Americans. Hum Genet 126 643 653

46. VelezDR

WejseC

StryjewskiME

AbbateE

HulmeWF

MyersJL

EstevanR

PatilloSG

OlesenR

TacconelliA

SirugoG

GilbertJR

HamiltonCD

ScottWK

2010 Variants in toll-like receptors 2 and 9 influence susceptibility to pulmonary tuberculosis in Caucasians, African-Americans, and West Africans. Hum Genet 127 65 73

47. BarreiroLB

NeyrollesO

BabbCL

TailleuxL

QuachH

McElreaveyK

HeldenPD

HoalEG

GicquelB

Quintana-MurciL

2006 Promoter variation in the DC-SIGN-encoding gene CD209 is associated with tuberculosis. PLoS Med 3 e20 doi:10.1371/journal.pmed.0030020

48. MollerM

NebelA

ValentonyteR

Van HeldenPD

SchreiberS

HoalEG

2009 Investigation of chromosome 17 candidate genes in susceptibility to TB in a South African population. Tuberculosis (Edinb) 89 189 194

49. DavilaS

HibberdML

HariDR

WongHE

SahiratmadjaE

BonnardC

AlisjahbanaB

SzeszkoJS

BalabanovaY

DrobniewskiF

van CrevelR

van de VosseE

NejentsevS

OttenhoffTHM

SeielstadM

2008 Genetic association and expression studies indicate a role of toll-like receptor 8 in pulmonary tuberculosis. PLoS Genet 4 e1000218 doi:10.1371/journal.pgen.1000218

50. DengHW

2001 Population admixture may appear to mask, change or reverse genetic effects of genes underlying complex traits. Genetics 159 1319 1323

51. International HapMap Consortium 2003 The International HapMap Project. Nature 426 789 796

52. International HapMap Consortium 2005 A haplotype map of the human genome. Nature 437 1299 1320

53. GabrielSB

SchaffnerSF

NguyenH

MooreJM

RoyJ

BlumenstielB

HigginsJ

DefeliceM

LochnerA

FaggartM

Liu-CorderoSN

RotimiC

AdeyemoA

CooperR

WardR

LanderES

DalyMJ

AltshulerD

2002 The structure of haplotype blocks in the human genome. Science 296 2225 2229

54. HindorffLA

SethupathyP

JunkinsHA

RamosEM

MehtaJP

CollinsFS

ManolioTA

2009 Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A 106 9362 9367

55. TangNL

FanHP

ChangKC

ChingJK

KongKP

YewWW

KamKM

LeungCC

TamCM

BlackwellJ

ChanCY

2009 Genetic association between a chemokine gene CXCL-10 (IP-10, interferon gamma inducible protein 10) and susceptibility to tuberculosis. Clin Chim Acta 406 98 102

56. DissanayekeSR

LevinS

PienaarS

WoodK

EleyB

BeattyD

HendersonH

AndersonS

LevinM

2009 Polymorphic variation in TIRAP is not associated with susceptibility to childhood TB but may determine susceptibility to TBM in some ethnic groups. PLoS ONE 4 e6698 doi:10.1371/journal.pone.0006698

57. HawnTR

DunstanSJ

ThwaitesGE

SimmonsCP

ThuongNT

LanNT

QuyHT

ChauTT

HieuNT

RodriguesS

JanerM

ZhaoLP

HienTT

FarrarJJ

AderemA

2006 A polymorphism in Toll-interleukin 1 receptor domain containing adaptor protein is associated with susceptibility to meningeal tuberculosis. J Infect Dis 194 1127 1134

58. ThuongNT

HawnTR

ThwaitesGE

ChauTT

LanNT

QuyHT

HieuNT

AderemA

HienTT

FarrarJJ

DunstanSJ

2007 A polymorphism in human TLR2 is associated with increased susceptibility to tuberculous meningitis. Genes Immun 8 422 428

59. ReichDE

LanderES

2001 On the allelic spectrum of human disease. Trends Genet 17 502 510

60. BodmerW

BonillaC

2008 Common and rare variants in multifactorial susceptibility to common diseases. Nat Genet 40 695 701

61. MaX

LiuY

GowenBB

GravissEA

ClarkAG

MusserJM

2007 Full-exon resequencing reveals toll-like receptor variants contribute to human susceptibility to tuberculosis disease. PLoS ONE 2 e1318 doi:10.1371/journal.pone.0001318

62. BakerA

RandhawaA

SheyM

de KockM

KaplanG

AdamsM

HanekomWA

BoomWH

HawnTR

SteinCM

2009 Comparison of genotype frequencies in Toll-like receptor genes in Ugandans, South Africans, and African HapMap populations. Presented at the American Society of Human Genetics 59th annual meeting; 20–24 October 2009; Honolulu, Hawaii, United States of America. 1808/T/Poster Board #357

63. McCarrollSA

AltshulerDM

2007 Copy-number variation and association studies of human disease. Nat Genet 39 S37 S42

64. GagneuxS

SmallPM

2007 Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 7 328 337

65. ThwaitesG

CawsM

ChauTT

D'SaA

LanNT

2008 The relationship between Mycobacterium tuberculosis genotype and the clinical phenotype of pulmonary and meningeal tuberculosis. J Clin Microbiol 46 1363 1368

66. de JongBC

HillPC

AikenA

AwineT

AntonioM

AdetifaIM

Jackson-SillahDJ

FoxA

DeriemerK

GagneuxS

BorgdorffMW

McAdamKP

CorrahT

SmallPM

AdegbolaRA

2008 Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in The Gambia. J Infect Dis 198 1037 1043

67. CawsM

ThwaitesG

DunstanS

HawnTR

LanNT

ThuongNT

StepniewskaK

HuyenMN

BangND

LocTH

GagneuxS

VanSD

KremerK

van derSM

SmallP

AnhPT

ChinhNT

QuyHT

DuyenNT

ThoDQ

HieuNT

TorokE

HienTT

DungNH

NhuNT

DuyPM

van VinhCN

FarrarJ

2008 The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog 4 e1000034 doi:10.1371/journal.ppat.1000034

68. BerringtonWR

HawnTR

2007 Mycobacterium tuberculosis, macrophages, and the innate immune response: does common variation matter? Immunol Rev 219 167 186

69. BaficaA

ScangaCA

FengCG

LeiferC

CheeverA

SherA

2005 TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 202 1715 1724

70. GomezLM

AnayaJM

VilchezJR

CadenaJ

HinojosaR

VelezL

Lopez-NevotMA

MartinJ

2007 A polymorphism in the inducible nitric oxide synthase gene is associated with tuberculosis. Tuberculosis (Edinb) 87 288 294

71. GiacominiE

RemoliME

GafaV

PardiniM

FattoriniL

CocciaEM

2009 IFN-beta improves BCG immunogenicity by acting on DC maturation. J Leukoc Biol 85 462 468

72. GustafsonP

GomesVF

VieiraCS

JensenH

SengR

NorbergR

SambB

NauclerA

AabyP

2001 Tuberculosis mortality during a civil war in Guinea-Bissau. JAMA 286 599 603

73. ParrishNM

DickJD

BishaiWR

1998 Mechanisms of latency in Mycobacterium tuberculosis. Trends Microbiol 6 107 112

74. ComasI

GagneuxS

2009 The past and future of tuberculosis research. PLoS Pathog 5 e1000600 doi:10.1371/journal.ppat.1000600

75. WheelerE

MillerEN

PeacockCS

DonaldsonIJ

ShawMA

JamiesonSE

BlackwellJM

CordellHJ

2006 Genome-wide scan for loci influencing quantitative immune response traits in the Belem family study: comparison of methods and summary of results. Ann Hum Genet 70 78 97

76. HawnTR

MischEA

DunstanSJ

ThwaitesGE

LanNT

2007 A common human TLR1 polymorphism regulates the innate immune response to lipopeptides. Eur J Immunol 37 2280 2289

77. SheyMS

RandhawaAK

BowmakerM

SmithE

ScribaTJ

de KockM

MahomedH

HusseyG

HawnTR

HanekomWA

2010 Single nucleotide polymorphisms in toll-like receptor 6 are associated with altered lipopeptide- and mycobacteria-induced interleukin-6 secretion. Genes Immun 11 561 572

78. ThuongNT

DunstanSJ

ChauTT

ThorssonV

SimmonsCP

QuyenNT

ThwaitesGE

Thi Ngoc LanN

HibberdM

TeoYY

SeielstadM

AderemA

FarrarJJ

HawnTR

2008 Identification of tuberculosis susceptibility genes with human macrophage gene expression profiles. PLoS Pathog 4 e1000229 doi:10.1371/journal.ppat.1000229

79. ManolioTA

CollinsFS

CoxNJ

GoldsteinDB

HindorffLA

HunterDJ

McCarthyMI

RamosEM

CardonLR

ChakravartiA

ChoJH

GuttmacherAE

KongA

KruglyakL

MardisE

RotimiCN

SlatkinM

ValleD

WhittemoreAS

BoehnkeM

ClarkAG

EichlerEE

GibsonG

HainesJL

MackayTF

McCarrollSA

VisscherPM

2009 Finding the missing heritability of complex diseases. Nature 461 747 753

80. BellamyR

RuwendeC

CorrahT

McAdamK

WhittleH

HillA

1998 Variations in the NRAMP1 gene and susceptibility to tuberculosis in West Africans. N Engl J Med 338 640 644

81. AwomoyiA

MarchantA

HowsonJ

McAdamK

BlackwellJ

NewportM

2002 Interleukin-10, Polymorphism in SLC11A1 (formerly NRAMP1), and susceptibility to tuberculosis. J Infect Dis 186 1808 1814

82. FitnessJ

FloydS

WarndorffD

SichaliL

MalemaS

CrampinA

FineP

HillA

2004 Large-scale candidate gene study of tuberculosis susceptibility in the Karonga district of Nothern Malawi. Am J Trop Med Hyg 71 341 349

83. SoborgC

AndersenAB

RangeN

MalenganishoW

FriisH

MagnussenP

TemuMM

ChangaluchaJ

MadsenHO

GarredP

2007 Influence of candidate susceptibility genes on tuberculosis in a high endemic region. Mol Immunol 44 2213 2220

84. MaX

WrightJ

ReichR

TeeterL

El SahlyH

AweR

MusserJ

GravissE

2002 5′ dinucleotide repeat polymorphism of NRAMP1 and susceptibility to tuberculosis among Caucasian patients in Houston, Texas. Int J Tuberc Lung Dis 6 818 823

85. DelgadoJ

BaenaA

ThimS

GoldfeldA

2002 Ethnic-specific genetic associations with pulmonary tuberculosis. J Infect Dis 186 1463 1468

86. LiuW

CaoW

ZhangC

TianL

WuX

HabbemaJ

ZhaoQ

ZhangP

XinZ-T

LiC

YangH

2004 VDR and NRAMP1 gene polymorphisms in susceptibility to pulmonary tuberculosis among the Chinese Han population: a case-control study. Int J Tuberc Lung Dis 8 428 434

87. AbeT

IinumaY

AndoM

YokoyamaT

YamamotoT

NakashimaK

TakagiN

BabaH

HasegawaY

ShimokataK

2003 NRAMP1 polymorphisms, susceptibility and clinical features of tuberculosis. J Infect 46 215 220

88. GaoP-S

FujishimaS

MaoX-Q

RemusN

KandaM

EnomotoT

DakeY

BottiniN

TabuchiM

HasegawaN

YamaguchiK

TiemessenC

HopkinJ

ShirakawaT

KishiF

2000 Genetic variants of NRAMP1 and active tuberculosis in Japanese populations. Clin Genet 58 74 76

89. LiawY-S

WuJ-JT

WuC-H

HungC-C

LeeC-N

YangP-C

LuhK-T

KuoS-H

2002 Variations in the NRAMP1 gene and susceptibility of tuberculosis in Taiwanese. Int J Tuberc Lung Dis 6 454 460

90. AkahoshiM

IshiharaM

RemusN

UnoK

MiyakeK

HirotaT

NakashimaK

MatsudaA

KandaM

EnomotoT

OhnoS

NakashimaH

CasanovaJL

HopkinJM

TamariM

MaoXQ

ShirakawaT

2004 Association between IFNA genotype and the risk of sarcoidosis. Hum Genet 114 503 509

91. VejbaesyaS

ChierakulN

LuangtrakoolP

SermduangprateepC

2007 NRAMP1 and TNF-alpha polymorphisms and susceptibility to tuberculosis in Thais. Respirology 12 202 206

92. LeungKH

YipSP

WongWS

YiuLS

ChanKK

LaiWM

ChowEY

LinCK

YamWC

ChanKS

2007 Sex- and age-dependent association of SLC11A1 polymorphisms with tuberculosis in Chinese: a case control study. BMC Infect Dis 7 19

93. RyuS

ParkY-K

BaiG-H

KimS-J

ParkS-N

KangS

2000 3′UTR polymorphisms in the NRAMP1 gene are associated with susceptibility to tuberculosis in Koreans. Int J Tuberc Lung Dis 4 577 580

94. KusuharaK

YamamotoK

OkadaK

MizunoY

HaraT

2007 Association of IL12RB1 polymorphisms with susceptibility to and severity of tuberculosis in Japanese: a gene-based association analysis of 21 candidate genes. Int J Immunogenet 34 35 44

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