Tuberculosis Transmission Based on Molecular Epidemiologic Research

Molecular genotyping techniques developed during the past decade and conventional epidemiological methods have been used synergistically in studies of the transmission and pathogenesis of Mycobacterium tuberculosis. Research studies assessing contacts and outbreaks, risk factors for ongoing transmission, and exogenous reinfection with M. tuberculosis have advanced with applied molecular epidemiologic techniques. In addition, molecular epidemiologic approaches have enabled scientists to assess the impact of drug resistance on the transmission and pathogenesis of M. tuberculosis and to identify strains with broad temporal and spatial distributions. In the near future, the intersection of molecular epidemiology, bacterial population genetics, comparative genomics, immunology, and other disciplines will further our understanding of tuberculosis transmission and pathogenesis, contributing to the development of effective drugs and a vaccine against this important human pathogen.

Tuberculosis - transmission - molecular epidemiology - genotyping - Mycobacterium tuberculosis

REFERENCES

• 1 van Embden J D, Cave M D, Crawford J T et al.. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology.  J Clin Microbiol. 1993;  31 406-409
• 2 Yang Z H, Ijaz K, Bates J H, Eisenach K D, Cave M D. Spoligotyping and polymorphic GC-rich repetitive sequence fingerprinting of Mycobacterium tuberculosis strains having few copies of IS6110 .  J Clin Microbiol. 2000;  38 3572-3576
• 3 Groenen P M, Bunschoten A E, van Soolingen D, van Embden J D. Nature of DNA polymorphism in the direct repeat cluster of Mycobacterium tuberculosis; application for strain differentiation by a novel typing method.  Mol Microbiol. 1993;  10 1057-1065
• 4 Barnes P F, Cave D M. Molecular epidemiology of tuberculosis.  N Engl J Med. 2003;  349 1149-1156
• 5 Wilson S M, Goss S, Drobniewski F. Evaluation of strategies for molecular fingerprinting for use in the routine work of a Mycobacterium tuberculosis reference unit.  J Clin Microbiol. 1998;  36 3385-3388
• 6 Soini H, Pan X, Amin A et al.. Characterization of Mycobacterium tuberculosis isolates from patients on Houston, Texas, by spoligotyping.  J Clin Microbiol. 2000;  38 669-676
• 7 Supply P, Lesjean S, Savine E et al.. Automated high throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units.  J Clin Microbiol. 2001;  39 3563-3571
• 8 Mazars E, Lesjean S, Banuls A L et al.. High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology.  Proc Natl Acad Sci USA. 2001;  98 1901-1906
• 9 Kwara A, Schiro R, Cowan L S et al.. Evaluation of the epidemiologic utility of secondary typing methods for differentiation of Mycobacterium tuberculosis isolates.  J Clin Microbiol. 2003;  41 2683-2685
• 10 Braden C R, Templeton G L, Cave M D et al.. Interpretation of restriction fragment length polymorphism analysis of Mycobacterium tuberculosis isolates from a state with a large rural population.  J Infect Dis. 1997;  175 1446-1452
• 11 Godfrey-Faussett P, Sonnenberg P, Shearer S C et al.. Tuberculosis control and molecular epidemiology in a South African gold-mining community.  Lancet. 2000;  356 1066-1071
• 12 Murray M, Alland D. Methodological problems in the molecular epidemiology of tuberculosis.  Am J Epidemiol. 2002;  155 565-571
• 13 Glynn J R, Vynnycky E, Pine P E. Influence of sampling on estimates of clustering and recent transmission of Mycobacterium tuberculosis derived from DNA fingerprinting techniques.  Am J Epidemiol. 1999;  149 366-371
• 14 Jasmer R M, Hahn J A, Small P M et al.. A molecular epidemiologic analysis of tuberculosis trends in San Francisco, 1991-1997.  Ann Intern Med. 1999;  130 971-978
• 15 van Soolingen D, Borgdorff M W, de Haas P E et al.. Molecular epidemiology of tuberculosis in the Netherlands: a nationwide study from 1993 through 1997.  J Infect Dis. 1999;  180 726-736
• 16 Veen J. Microepidemics of tuberculosis: the stone-in-the-pond principle.  Tuber Lung Dis. 1992;  73 73-76
• 17 Small P M, Hopewell P C, Singh S et al.. The epidemiology of tuberculosis in San Francisco: a population-based study using conventional and molecular methods.  N Engl J Med. 1994;  330 1703-1709
• 18 van Deutekom H, Gerritsen J J, van Soolingen D et al.. A molecular epidemiological approach to studying the transmission of tuberculosis in Amsterdam.  Clin Infect Dis. 1997;  25 1071-1077
• 19 Chin D P, Crane C M, Diul M Y et al.. Spread of Mycobacterium tuberculosis in a community implementing recommended elements of tuberculosis control.  JAMA. 2000;  283 2968-2974
• 20 Kimerling M E, Benjamin W H, Lok K H et al.. Restriction fragment length polymorphism screening of Mycobacterium tuberculosis isolates: population surveillance for targeting disease transmission in a community.  Int J Tuberc Lung Dis. 1998;  2 655-662
• 21 Lemaitre N, Sougakoff W, Truffot-Pernot C et al.. Use of DNA fingerprinting for primary surveillance of nosocomial tuberculosis in a large urban hospital: detection of outbreaks in homeless people and migrant workers.  Int J Tuberc Lung Dis. 1998;  2 390-396
• 22 Barnes P F, Yang Z, Preston-Martin S et al.. Patterns of tuberculosis transmission in Central Los Angeles.  JAMA. 1997;  278 1159-1163
• 23 Bishai W R, Graham N M, Harrington S et al.. Molecular and geographic patterns of tuberculosis transmission after 15 years of directly observed therapy.  JAMA. 1998;  280 1679-1684
• 24 Daley C L, Small P M, Schecter G F et al.. An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus: an analysis using restriction-fragment-length polymorphisms.  N Engl J Med. 1992;  326 231-235
• 25 Kline S E, Hedemark L L, Davies S F. Outbreak of tuberculosis among regular patrons of a neighborhood bar.  N Engl J Med. 1995;  333 222-227
• 26 Yaganehdoost A, Graviss E A, Ross M W et al.. Complex transmission dynamics of clonally related virulent Mycobacterium tuberculosis associated with barhopping by predominantly human immunodeficiency virus-positive gay men.  J Infect Dis. 1999;  180 1245-1251
• 27 García-García M, Palacios-Martínez M, Ponce-de-León A et al.. The role of core groups in transmitting Mycobacterium tuberculosis in a high prevalence community in Southern Mexico.  Int J Tuberc Lung Dis. 2000;  4 12-17
• 28 Leonhardt K K, Gentile F, Gilbert B P, Aiken M. A cluster of tuberculosis among crack house contacts in San Mateo County, California.  Am J Public Health. 1994;  84 1834-1836
• 29 Bock N N, Mallory J P, Mobley N et al.. Outbreak of tuberculosis associated with a floating card game in the rural south: lessons for tuberculosis contact investigations.  Clin Infect Dis. 1998;  27 1221-1226
• 30 Kim S J, Bai G H, Lee H et al.. Transmission of Mycobacterium tuberculosis among high school students in Korea.  Int J Tuberc Lung Dis. 2001;  5 824-830
• 31 Bauer J, Kok-Jensen A, Faurschow P et al.. A prospective evaluation of the clinical value of nation-wide DNA fingerprinting of tuberculosis isolates in Denmark.  Int J Tuberc Lung Dis. 2000;  4 295-299
• 32 Edlin B R, Tokars J I, Grieco M H et al.. An outbreak of multidrug-resistant tuberculosis among hospitalized patients with the acquired immunodeficiency syndrome.  N Engl J Med. 1992;  326 1514-1521
• 33 Haas D W, Milton S, Kreiswirth B N et al.. Nosocomial transmission of a drug-sensitive W-variant Mycobacterium tuberculosis strain among patients with acquired immunodeficiency syndrome in Tennessee.  Infect Control Hosp Epidemiol. 1998;  19 635-639
• 34 Chaves F, Dronda F, Cave M D et al.. A longitudinal study of transmission of tuberculosis in a large prison population.  Am J Respir Crit Care Med. 1997;  155 719-725
• 35 Hanau-Bercot B, Gremy I, Raskine L et al.. A one-year prospective study (1994-1995) for a first evaluation of tuberculosis transmission in French prisons.  Int J Tuberc Lung Dis. 2000;  4 853-859
• 36 Mohle-Boetani J C, Miguelino V, Dewsnup D et al.. Tuberculosis outbreak in a housing unit for human immunodeficiency virus-infected patients in a correctional facility: transmission risk factors and effective outbreak control.  Clin Infect Dis. 2002;  34 668-676
• 37 Mangura B T, Napolitano E C, Passannante M R et al.. Mycobacterium tuberculosis miniepidemic in a church gospel choir.  Chest. 1998;  113 234-237
• 38 Anon. HIV-related tuberculosis in a transgender network: Baltimore, Maryland and New York City area, 1998-2000.  MMWR Morb Mortal Wkly Rep. 2000;  49 317-320
• 39 Jereb J A, Burwen D R, Dooley S W et al.. Nosocomial outbreak of tuberculosis in a renal transplant unit: application of a new technique for restriction fragment length polymorphism analysis of Mycobacterium tuberculosis isolates.  J Infect Dis. 1993;  168 1219-1224
• 40 Wilkinson D, Crump J, Pillay M, Sturm A W. Nosocomial transmission of tuberculosis in Africa documented by restriction fragment length polymorphism.  Trans R Soc Trop Med Hyg. 1997;  91 318
• 41 Frieden T R, Woodley C L, Crawford J T et al.. The molecular epidemiology of tuberculosis in New York City: the importance of nosocomial transmission and laboratory error.  Tuber Lung Dis. 1996;  77 407-413
• 42 Ikeda R M, Birkhead G S, DiFerdinando Jr G T et al.. Nosocomial tuberculosis: an outbreak of a strain resistant to seven drugs.  Infect Control Hosp Epidemiol. 1995;  16 152-159
• 43 Johnson K R, Braden C R, Cairns K L et al.. Transmission of Mycobacterium tuberculosis from medical waste.  JAMA. 2000;  284 1683-1688
• 44 Agerton T, Valway S, Gore B et al.. Transmission of a highly drug-resistant strain (strain W1) of Mycobacterium tuberculosis: community outbreak and nosocomial transmission via a contaminated bronchoscope.  JAMA. 1997;  278 1073-1077
• 45 Michele T M, Cronin W A, Graham N M et al.. Transmission of Mycobacterium tuberculosis by a fiberoptic bronchoscope: identification by DNA fingerprinting.  JAMA. 1997;  278 1093-1095
• 45a Behr M A, Warren S A, Salamon H et al.. Transmission of Mycobacterium tuberculosis from patients smear-negative for acid-fast bacilli.  Lancet. 1999;  353 444-449
• 45b Ong A, Creasman J, Hopewell P C et al.. A molecular epidemiological assessment of extrapulmonary tuberculosis in San Francisco.  Clin Infect Dis. 2004;  38 25-31
• 45c World Health Organization Global .Tuberculosis Programme. An expanded DOTS framework for effective tuberculosis control. WHO/CDS/TB/2002.297 Geneva; WHO 2002
• 46 Hernández-Garduño E, Kunimoto D, Wang L et al.. Predictors of clustering of tuberculosis in Greater Vancouver: a molecular epidemiologic study.  CMAJ. 2002;  167 349-352
• 47 Diel R, Schneider S, Meywald-Walter K et al.. Epidemiology of tuberculosis in Hamburg, Germany: long-term population-based analysis applying classical and molecular epidemiologic techniques.  J Clin Microbiol. 2002;  40 532-539
• 48 Lockman S, Sheppard J D, Braden C R et al.. Molecular and conventional epidemiology of Mycobacterium tuberculosis in Botswana: a population-based prospective study of 301 pulmonary tuberculosis patients.  J Clin Microbiol. 2001;  39 1042-1047
• 49 Jasmer R M, Hahn J A, Small P M et al.. Differences in contributing factors to tuberculosis incidence in U.S.-born and foreign-born persons.  Am J Respir Crit Care Med. 1998;  158 1797-1803
• 50 Geng E, Kreiswirth B, Driver C et al.. Changes in the transmission of tuberculosis in New York City from 1990 to 1999.  N Engl J Med. 2002;  346 1453-1458
• 51 Soborg C, Soborg B, Poulesen S et al.. Doubling of the tuberculosis incidence in Greenland over an 8-year period (1990-1997).  Int J Tuberc Lung Dis. 2001;  5 257-265
• 52 Alland D, Kalkut G E, Moss A R et al.. Transmission of tuberculosis in New York City: an analysis by DNA fingerprinting and conventional epidemiologic methods.  N Engl J Med. 1994;  330 1710-1716
• 53 Small P M, Shafer R W, Hopewell P C et al.. Exogenous reinfection with multidrug-resistant Mycobacterium tuberculosis in patients with advanced HIV infection.  N Engl J Med. 1993;  328 1137-1144
• 54 Sudre P, Pfyffer G E, Bodmer T et al.. Molecular epidemiology of tuberculosis among HIV-infected persons in Switzerland: a country-wide 9-year cohort study.  Infection. 1999;  27 323-330
• 55 Heldal E, Docker H, Caugant D A et al.. Pulmonary tuberculosis in Norwegian patients: the role of reactivation, re-infection and primary infection assessed by previous mass screening data and restriction fragment length polymorphism analysis.  Int J Tuberc Lung Dis. 2000;  4 300-307
• 56 van Rie A, Warren R M, Richardson M et al.. Exogenous reinfection as a cause of recurrent tuberculosis after curative treatment.  N Engl J Med. 1999;  341 1174-1179
• 57 Lambert M L, Hasker E, van Deun A et al.. Recurrence in tuberculosis: relapse of reinfection?.  Lancet Infect Dis. 2003;  3 282-287
• 58 de Boer A S, Kremer K, Borgdorff M W et al.. Genetic heterogeneity in Mycobacterium tuberculosis isolates reflected in IS6110 restriction fragment length polymorphism patterns as low-intensity bands.  J Clin Microbiol. 2000;  3 4478-4484
• 59 Das S, Paramasivan C N, Lowrie D B. IS6110 restriction fragment length polymorphism typing of clinical isolates of Mycobacterium tuberculosis from patients with pulmonary tuberculosis in Madras South India.  Tuber Lung Dis. 1995;  76 550-554
• 60 Caminero J A, Pena M J, Campos-Herrero M I et al.. Exogenous reinfection with tuberculosis on a European island with a moderate incidence of disease.  Am J Respir Crit Care Med. 2001;  163 717-720
• 61 Lourenço M C, Grinsztejn B, Fadinho-Montes F C et al.. Genotypic patterns of multiple isolates of M. tuberculosis from tuberculous HIV patients.  Trop Med Int Health. 2000;  5 488-494
• 62 García de Viedma D G, Marin M, Hernangomez S et al.. Tuberculosis recurrences: reinfection plays a role in a population whose clinical/epidemiological characteristics do not favor reinfection.  Arch Intern Med. 2002;  162 1873-1879
• 63 Krüüner A, Pehme L, Ghebremichael S et al.. Use of molecular techniques to distinguish between treatment failure and exogenous reinfection with Mycobacterium tuberculosis .  Clin Infect Dis. 2002;  35 146-155
• 64 Yeh R W, Hopewell P C, Daley C L. Simultaneous infection with two strains of Mycobacterium tuberculosis identified by restriction fragment length polymorphism analysis.  Int J Tuberc Lung Dis. 1999;  3 537-539
• 65 Braden C R, Morlock G P, Woodley C L et al.. Simultaneous infection with multiple strains of Mycobacterium tuberculosis .  J Infect Dis. 2001;  33 42-47
• 66 Chaves F, Dronda F, Alonso-Sanz M, Noriega A R. Evidence of exogenous reinfection and mixed infection with more than one strain of Mycobacterium tuberculosis among Spanish HIV-infected inmates.  AIDS. 1999;  13 615-620
• 67 Niemann S, Richter E, Rusch-Gerdes S et al.. Double infection with a resistant and a multidrug-resistant strain of Mycobacterium tuberculosis .  Emerg Infect Dis. 2000;  6 548-551
• 68 García-García M L, Ponce-de-León A, Jimenez-Corona M E et al.. Clinical consequences and transmissibility of drug-resistant tuberculosis in southern Mexico.  Arch Intern Med. 2000;  160 630-636
• 69 Burgos M, DeRiemer K, Small P M et al.. Impact of drug-resistance on the generation of secondary cases of tuberculosis.  J Infect Dis. 2003;  188 1878-1885
• 70 Cohn M, Kovitz C, Oda U. Studies on isoniazid and tubercle bacilli: the growth requirements, catalase activities, and pathogenic properties of isoniazid resistant mutants.  Am Rev Tuberc. 1954;  70 641-664
• 71 Pym A S, Domenech P, Honore N, Song J, Deretic V, Cole S T. Regulation of catalase-peroxidase (KatG) expression, isoniazid sensitivity and virulence by furA of Mycobacterium tuberculosis .  Mol Microbiol. 2001;  40 879-889
• 72 Bradford W Z, Koehler J, El-Hajj H et al.. Dissemination of Mycobacterium tuberculosis across the San Francisco Bay Area.  J Infect Dis. 1998;  177 1104-1107
• 73 van Soolingen D, Qian L, de Haas P E et al.. Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia.  J Clin Microbiol. 1995;  33 3234-3238
• 74 Anh D D, Borgdorff M W, Van L N et al.. Mycobacterium tuberculosis in Beijing genotypes emerging in Vietnam.  Emerg Infect Dis. 2000;  6 302-305
• 75 Toungoussova O S, Mariandyshev A, Bjune G et al.. Molecular epidemiology and drug resistance of Mycobacterium tuberculosis isolates in the Archangel prison in Russia: predominance of the W-Beijing clone family.  J Infect Dis. 2003;  37 665-672
• 76 Krüüner A, Hoffner S E, Sillastu H et al.. Spread of drug-resistant pulmonary tuberculosis in Estonia.  J Clin Microbiol. 2001;  39 3339-3345
• 77 Niemann S, Rusch-Gerdes S, Richter E. IS6110 fingerprinting of drug-resistant Mycobacterium tuberculosis strains isolated in Germany during 1995.  J Clin Microbiol. 1997;  35 3015-3020
• 78 Caminero J A, Pena M J, Campos-Herrero M I et al.. Epidemiological evidence of the spread of a Mycobacterium tuberculosis strain of the Beijing genotype on Gran Canaria Island.  Am J Respir Crit Care Med. , 2002 164 1165-1170
• 79 Borgdorff M W, de Haas P, Kremer K, van Soolingen D. Mycobacterium tuberculosis Beijing genotype, the Netherlands.  Emerg Infect Dis. 2003;  9 1310-1313
• 80 Richardson M, van Lill S W, van der Spuy G D et al.. Historic and recent events contribute to the disease dynamics of Beijing-like Mycobaterium tuberculosis isolates in a high incidence region.  Int J Tuberc Lung Dis. 2002;  6 1001-1011
• 81 van Crevel R, Nelwan R H, de Lenne W et al.. Mycobacterium tuberculosis Beijing genotype strains associated with febrile response to treatment.  Emerg Infect Dis. 2001;  7 880-883
• 82 Lillebaek T, Andersen A B, Dirksen A et al.. Mycobacterium tuberculosis Beijing genotype.  Emerg Infect Dis. 2003;  9 1553-1557
• 83 Tracevska T, Jansone I, Baumanis V et al.. Prevalence of Beijing genotype in Latvian multidrug-resistant Mycobacterium tuberculosis isolates.  Int J Tuberc Lung Dis. 2003;  7 1097-1103
• 84 Bifani P J, Plikaytis B B, Kapur V et al.. Origin and interstate spread of a New York City multidrug-resistant Mycobacterium tuberculosis clone family.  JAMA. 1996;  275 452-457
• 85 Agerton T B, Valway S E, Blinkhorn R J et al.. Spread of strain W, a highly drug-resistant strain of Mycobacterium tuberculosis, across the United States.  Clin Infect Dis. 1999;  29 85-92
• 86 Glynn J R, Whitley J, Bifani P J et al.. Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review.  Emerg Infect Dis. 2002;  8 843-849
• 87 Munsiff S S, Nivin B, Sacajiu G et al.. Persistence of a highly resistant strain of tuberculosis in New York City during 1990-1999.  J Infect Dis. 2003;  188 356-363
• 88 Bifani P J, Mathema B, Liu Z et al.. Identification of a W variant outbreak of Mycobacterium tuberculosis via population-based molecular epidemiology.  JAMA. 1999;  282 2321-2327
• 89 Bifani P J. Mathema, Kurepina NE, Kreiswirth BN. Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains.  Trends Microbiol. 2002;  10 45-52
• 90 Rad M E, Bifani P, Martin C et al.. Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family.  Emerg Infect Dis. 2003;  9 838-845
• 91 Lopez B, Aguilar D, Orozco H et al.. A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes.  Clin Exp Immunol. 2003;  133 30-37
• 92 Shafi J, Andrew P W, Barer M R. Microarays for public health: genomic epidemiology of tuberculosis.  Comp Funct Genom. 2002;  3 362-365