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February 14, 1996, Vol 275, No. 6 >
ARTICLE | February 14, 1996

Origin and Interstate Spread of a New York City Multidrug-Resistant Mycobacterium tuberculosis Clone Family FREE

Pablo J. Bifani, MS; Bonnie B. Plikaytis, MS; Vivek Kapur, PhD; Kathryn Stockbauer; Xi Pan, MD; Michael L. Lutfey, MS; Soraya L. Moghazeh; William Eisner; Thomas M. Daniel, MD; Mark H. Kaplan, MD; Jack T. Crawford, PhD; James M. Musser, MD, PhD; Barry N. Kreiswirth, PhD
[+] Author Affiliations

This article is one of a series addressing emerging and reemerging global microbial threats.

Reprint requests to Tuberculosis Center, Public Health Research Institute, 455 First Ave, New York, NY 10016 (Dr Kreiswirth).


JAMA. 1996;275(6):452-457. doi:10.1001/jama.1996.03530300036037
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Objective.  —To determine whether isolates of Mycobacterium tuberculosis from New York and elsewhere that are resistant to four or more primary antimicrobial agents and responsible for widespread disease in the 1990s represent a newly emerged clone or a heterogeneous array of unrelated organisms.

Setting.  —New York City area and selected locations in the United States.

Patients.  —M tuberculosis isolates from 1953 patients in New York and multidrug-resistant isolates from six patients from other US communities.

Design.  —Convenience sample of all M tuberculosis strains (M tuberculosis isolates resistant to rifampin, streptomycin, isoniazid, and ethambutol, and sometimes ethionamide, kanamycin, capreomycin, or ciprofloxacin) submitted to the Public Health Research Institute Tuberculosis Center since 1991 and samples submitted to the Centers for Disease Control and Prevention from throughout the United States. The samples submitted were representative of the New York City strains of M tuberculosis.

Main Outcome Measure.  —Characterization of resistant M tuberculosis strains studied by IS61 10 and polymorphic GC-rich repetitive sequence (PGRS) hybridization patterns, multiplex polymerase chain reaction (PCR) analysis, and automated DNA sequencing of genes containing mutations associated with resistance to rifampin (rpoB), isoniazid (katG and inhA locus), and streptomycin (strA and rrs).

Results.  —Multidrung-resistant M tuberculosis isolates were recovered from 253 New York City patients and had the same or closely allied IS6110 and PGRS patterns, multiplex PCR type, and gene mutations associated with resistance to rifampin, isoniazid, and streptomycin. Isolates with these same molecular characteristics were recovered from patients in Florida and Nevada, health care workers in Atlanta, Ga, and Miami, Fla, and an individual who recently moved from New York City to Denver, Colo, and caused disease or skin test conversion in at least 12 people in a nursing home environment.

Conclusions.  —The results document the molecular origin and spread of progeny of a closely related family of multidrug-resistant M tuberculosis strains that have recently shared a common ancestor and undergone clonal expansion. The multidrug-resistant phenotype in these organisms arose by sequential acquisition of resistance-conferring mutations in several genes, most likely as a consequence of antibiotic selection of randomly occurring mutants in concert with inadequately treated infections. Dissemination of these difficult-to-treat bacteria throughout New York City and to at least four additional US cities has adverse implications for tuberculosis control in the 21st century.(JAMA. 1996;275:452-457)

REFERENCES

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Bloom BR, Murray CJL.  Tuberculosis, commentary on a reemergent killer. Science . 1992;;257:1055-1063.
2 +
Brudney K, Dobkin J.  Resurgent tuberculosis in New York City: human immunodeficiency virus, homelessness and the decline of tuberculosis control programs. Am Rev Respir Dis . 1991;;144:745-749.
3 +
Frieden TR, Sterling T, Pablos-Mendez A, et al.  The emergence of drug-resistant tuberculosis in New York City. N Engl J Med . 1993;;328:521-526.
4 +
Sepkowitz KA, Telzak EE, Recalde S, et al.  Trends in the susceptibility of TB in New York City. Clin Infect Dis . 1994;;18:755-759.
5 +
Bloch AB, Cauthen GM, Onorato IM, et al.  Nationwide survey of drug-resistant tuberculosis in the United States. JAMA . 1994;;271:665-671.
6 +
Snider DE, Roper WL.  The new tuberculosis. N Engl J Med . 1992;;326:703-705.
7 +
Small PM, Moss A.  Molecular epidemiology and the new tuberculosis. Infect Agents Dis . 1993;;2:132-138.
8 +
Hopewell PC.  Impact of human immunodeficiency virus infection on the epidemiology, clinical features, management and control of tuberculosis. Clin Infect Dis . 1992;;18:540-546.
9 +
Frieden TR, Fujiwara PI, Washko RM, Hamburg MA.  Tuberculosis in New York City: turning the tide. N Engl J Med . 1995;;333:229-233.
10 +
Centers for Disease Control and Prevention.  Transmission of multidrug-resistant tuberculosis among immunocompromised persons in a correctional system—New York, 1991. MMWR Morbid Mortal Wkly Rep . 1992;;41:507-509.
11 +
Horn DL, Hewlett D, Alfalla C, et al.  Natural history and treatment outcome of 55 patients with rifampin-isoniazid-streptomycin-ethambutol (RISE)-resistant tuberculosis. Infect Dis resistant Pract . In press.
12 +
Coronado VG, Beck-Sague CM, Hutton MD, et al.  Transmission of multidrug-resistant Mycobacterium tuberculosis among persons with human immunodeficiency virus infection in an urban hospital: epidemiologic and restriction fragment length polymorphism analysis. J Infect Dis . 1993;;168:1052-1055.
13 +
Valway SE, Greifinger RB, Papania M, et al.  Multidrug-resistant tuberculosis in the New York State prison system, 1990-1991. J Infect Dis . 1994;; 170:151-156.
14 +
van Embden JDA, Cave MD, Crawford JT, et al.  Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol . 1993;;31:406-409.
15 +
Kapur V, Li LL, Hamrick MR, et al.  Rapid Mycobacterium species assignment and unambiguous identification of mutations associated with antimicrobial resistance in Mycobacterium tuberculosis by automated DNA sequencing. Arch Pathol Lab Med . 1995;;119:131-138.
16 +
Musser JM.  Antimicrobial agent resistance in mycobacteria: molecular genetic insights. Clin Microbiol Rev . 1995;;8:496-514.
17 +
Friedman CR, Stoeckle MY, Kreiswirth BN, et al.  Transmission of multidrug-resistant tuberculosis in a large urban setting. Am J Respir Crit Care Med . 1995;;152:355-359.
18 +
Siddiqi S. BACTEC TB Systems: Product and Procedure Manual . Sparks, Md: Becton Dickinson Co; 1989;.
19 +
Antimycobacterial Susceptibility Testing: Proposed Standards . Villanova, Pa: National Committee for Clinical Laboratory Standards; 1990;. NC-CLS publication M24-P.
20 +
Ross BC, Raios K, Jackson K, et al.  Molecular cloning of a highly repeated DNA element from Mycobacterium tuberculosis and its use as an epidemiological tool. J Clin Microbiol . 1992;;30:942-946.
21 +
Plikaytis BB, Marden JL, Crawford JT, et al.  Multiplex PCR assay specific for the multidrugresistant strain W of Mycobacterium tuberculosis. J Clin Microbiol . 1994;;32:1542-1546.
22 +
Centers for Disease Control.  Nosocomial transmission of multidrug-resistant tuberculosis among HIV-infected persons—Florida and New York, 1988-1991. MMWR Morbid Mortal Wkly Rep . 1991;; 40:585-591.
23 +
van Soolingen D, Hermans PWM, de Haas PEW, et al.  Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J Clin Microbiol . 1991;;29:2578-2586.
24 +
Hewlett D Jr, Horn DL, Franchini D, et al.  A report of 91 health care workers with nosocomial tuberculosis infection following exposure to rifampin-isoniazid-streptomycin-ethambutol (RISE)-resistant and drug susceptible tuberculosis. Infect Dis Clin Pract . 1995;;4:389-396.
25 +
Weis SE, Slocum PC, Blais FX, et al.  The effect of directly observed therapy on the rates of drug resistance and relapse in tuberculosis. N Engl J Med . 1994;;330:1179-1184.
26 +
Longuet P, Pierre J, Lacassin F, et al.  A limited multidrug-resistant Mycobacterium tuberculosis (MDR-TB) outbreak: screening of contact hospitalized patients (pts).  In: Abstracts of the 35th Interscience Conference on Antimicrobial Agents and Chemotherapy ; September 17-20, 1995;; San Francisco, Calif. Abstract J59.

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1 +
Bloom BR, Murray CJL.  Tuberculosis, commentary on a reemergent killer. Science . 1992;;257:1055-1063.
2 +
Brudney K, Dobkin J.  Resurgent tuberculosis in New York City: human immunodeficiency virus, homelessness and the decline of tuberculosis control programs. Am Rev Respir Dis . 1991;;144:745-749.
3 +
Frieden TR, Sterling T, Pablos-Mendez A, et al.  The emergence of drug-resistant tuberculosis in New York City. N Engl J Med . 1993;;328:521-526.
4 +
Sepkowitz KA, Telzak EE, Recalde S, et al.  Trends in the susceptibility of TB in New York City. Clin Infect Dis . 1994;;18:755-759.
5 +
Bloch AB, Cauthen GM, Onorato IM, et al.  Nationwide survey of drug-resistant tuberculosis in the United States. JAMA . 1994;;271:665-671.
6 +
Snider DE, Roper WL.  The new tuberculosis. N Engl J Med . 1992;;326:703-705.
7 +
Small PM, Moss A.  Molecular epidemiology and the new tuberculosis. Infect Agents Dis . 1993;;2:132-138.
8 +
Hopewell PC.  Impact of human immunodeficiency virus infection on the epidemiology, clinical features, management and control of tuberculosis. Clin Infect Dis . 1992;;18:540-546.
9 +
Frieden TR, Fujiwara PI, Washko RM, Hamburg MA.  Tuberculosis in New York City: turning the tide. N Engl J Med . 1995;;333:229-233.
10 +
Centers for Disease Control and Prevention.  Transmission of multidrug-resistant tuberculosis among immunocompromised persons in a correctional system—New York, 1991. MMWR Morbid Mortal Wkly Rep . 1992;;41:507-509.
11 +
Horn DL, Hewlett D, Alfalla C, et al.  Natural history and treatment outcome of 55 patients with rifampin-isoniazid-streptomycin-ethambutol (RISE)-resistant tuberculosis. Infect Dis resistant Pract . In press.
12 +
Coronado VG, Beck-Sague CM, Hutton MD, et al.  Transmission of multidrug-resistant Mycobacterium tuberculosis among persons with human immunodeficiency virus infection in an urban hospital: epidemiologic and restriction fragment length polymorphism analysis. J Infect Dis . 1993;;168:1052-1055.
13 +
Valway SE, Greifinger RB, Papania M, et al.  Multidrug-resistant tuberculosis in the New York State prison system, 1990-1991. J Infect Dis . 1994;; 170:151-156.
14 +
van Embden JDA, Cave MD, Crawford JT, et al.  Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol . 1993;;31:406-409.
15 +
Kapur V, Li LL, Hamrick MR, et al.  Rapid Mycobacterium species assignment and unambiguous identification of mutations associated with antimicrobial resistance in Mycobacterium tuberculosis by automated DNA sequencing. Arch Pathol Lab Med . 1995;;119:131-138.
16 +
Musser JM.  Antimicrobial agent resistance in mycobacteria: molecular genetic insights. Clin Microbiol Rev . 1995;;8:496-514.
17 +
Friedman CR, Stoeckle MY, Kreiswirth BN, et al.  Transmission of multidrug-resistant tuberculosis in a large urban setting. Am J Respir Crit Care Med . 1995;;152:355-359.
18 +
Siddiqi S. BACTEC TB Systems: Product and Procedure Manual . Sparks, Md: Becton Dickinson Co; 1989;.
19 +
Antimycobacterial Susceptibility Testing: Proposed Standards . Villanova, Pa: National Committee for Clinical Laboratory Standards; 1990;. NC-CLS publication M24-P.
20 +
Ross BC, Raios K, Jackson K, et al.  Molecular cloning of a highly repeated DNA element from Mycobacterium tuberculosis and its use as an epidemiological tool. J Clin Microbiol . 1992;;30:942-946.
21 +
Plikaytis BB, Marden JL, Crawford JT, et al.  Multiplex PCR assay specific for the multidrugresistant strain W of Mycobacterium tuberculosis. J Clin Microbiol . 1994;;32:1542-1546.
22 +
Centers for Disease Control.  Nosocomial transmission of multidrug-resistant tuberculosis among HIV-infected persons—Florida and New York, 1988-1991. MMWR Morbid Mortal Wkly Rep . 1991;; 40:585-591.
23 +
van Soolingen D, Hermans PWM, de Haas PEW, et al.  Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J Clin Microbiol . 1991;;29:2578-2586.
24 +
Hewlett D Jr, Horn DL, Franchini D, et al.  A report of 91 health care workers with nosocomial tuberculosis infection following exposure to rifampin-isoniazid-streptomycin-ethambutol (RISE)-resistant and drug susceptible tuberculosis. Infect Dis Clin Pract . 1995;;4:389-396.
25 +
Weis SE, Slocum PC, Blais FX, et al.  The effect of directly observed therapy on the rates of drug resistance and relapse in tuberculosis. N Engl J Med . 1994;;330:1179-1184.
26 +
Longuet P, Pierre J, Lacassin F, et al.  A limited multidrug-resistant Mycobacterium tuberculosis (MDR-TB) outbreak: screening of contact hospitalized patients (pts).  In: Abstracts of the 35th Interscience Conference on Antimicrobial Agents and Chemotherapy ; September 17-20, 1995;; San Francisco, Calif. Abstract J59.

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