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Clinical Investigations: INFECTIONS |

Mycobacterium tuberculosis Disease in Somali Immigrants in Minnesota* FREE TO VIEW

Robert Kempainen, MD; Karin Nelson, MD; David N. Williams, MB, ChB; Linda Hedemark, MD, FCCP
Author and Funding Information

*From the University of Washington, Seattle, WA (Dr. Kempainen); University of California/Los Angeles, Los Angeles, CA (Dr. Nelson); Department of Medicine, Hennepin County Medical Center, and Department of Medicine, University of Minnesota Medical School (Drs. Williams and Hedemark); and Community Health Department, Hennepin County Tuberculosis Control Center (Dr. Hedemark), Minneapolis, MN.

Correspondence to: David N. Williams, MB, ChB, Hennepin County Medical Center, Department of Medicine, 701 Park Ave, Minneapolis, MN 55415; e-mail: david.williams@co.hennepin.mn.us



Chest. 2001;119(1):176-180. doi:10.1378/chest.119.1.176
Text Size: A A A
Published online

Study objective: To characterize pulmonary and extrapulmonary Mycobacterium tuberculosis cases in the Somali community in Minnesota.

Design: Retrospective chart review of active tuberculosis cases in Somalis reported to the Minnesota Department of Health between January 1993 and June 1998.

Patients: Ethnic Somalis in the state of Minnesota with M tuberculosis diagnosed by positive culture or radiographic findings consistent with tuberculosis and clinical improvement when treated with antituberculous drugs.

Results: Eighty-two Somali patients were diagnosed with tuberculosis during the study period. Extrapulmonary disease (typically lymphadenopathy) was present in 46% (n = 38). The 1997 incidence of tuberculosis in Minnesota’s Somali population was estimated at 170 cases per 100,000 population compared with a national incidence of 20.5 per 100,000 among African Americans and 2.5 per 100,000 among whites. Ninety percent of Somali patients were < 40 years of age; 63% were diagnosed within 1 year of immigration, and> 90% had positive results with the purified protein derivative skin test. M tuberculosis was confirmed in 24 of 25 isolates from extrapulmonary cases. Multidrug resistance was present in 3.4%, and only two patients had AIDS.

Conclusions: Somalis have a high incidence of active disease, with frequent extrapulmonary involvement in the absence of AIDS, clinical presentation shortly after immigration, and infrequent infection with resistant organisms. Health-care providers should maintain an increased awareness for tuberculosis when evaluating Somali immigrants.

Despite increased understanding of its pathogenesis and treatment, Mycobacterium tuberculosis infection remains an important cause of morbidity and mortality throughout the world. In 1997, there were an estimated 8 million new cases of tuberculosis (TB), resulting in 1.9 million deaths, with the greatest burden of disease in developing nations.1During the past 30 years, the United States, like other developed nations, has experienced relatively low rates of TB but has seen marked changes in the demographics of the disease. TB has increasingly become concentrated in foreign-born persons and within racial and ethnic minority groups. In 1997, 39% of cases in the United States were among foreign-born persons compared with 27% 5 years earlier,2 and the majority were diagnosed within 5 years of arrival in the United States.3Furthermore, the proportion of all US cases involving extrapulmonary sites has grown steadily since the 1960s.45

Since the early 1990s, more than half of all Somali immigrants, mainly refugees, to the United States have settled in Minnesota, primarily in the Minneapolis metropolitan area. Numerous cases of active TB have been observed in this population, with frequent involvement of extrapulmonary sites and presentation shortly after immigration, but to our knowledge, there has been no report on the characteristics of TB in this population. The purpose of this case series is to characterize cases of pulmonary and extrapulmonary TB occurring in ethnic Somalis in Minnesota.

We identified all cases of TB in ethnic Somalis in Minnesota between January 1, 1993, and June 30, 1998, using data collected by the Minnesota Department of Health. Given the aggressive surveillance program for the identification of new TB cases run by the health department, we are confident that this case series includes all Somalis treated for TB within Minnesota during the study period. Most Somalis in Minnesota live in the metropolitan area in and around Minneapolis and are treated through clinics operated by Hennepin County. Charts for these patients were identified and reviewed. Clinical data from the remaining patients who were not treated by Hennepin County clinics were obtained from case reports available at the Minnesota Department of Health. The charts of an additional eight patients diagnosed with TB outside Minnesota but treated by the clinic in Hennepin County were also reviewed and are included in this series.

Data were abstracted from these sources in a systematic manner using a standardized format that included age at diagnosis, sex, time between immigration and diagnosis, site(s) of disease, duration of symptoms before diagnosis, purified protein derivative (PPD) skin-test status, bacteriology, drug resistance, and exposure history. Cases were screened for the presence of comorbid immunosuppressive conditions, including infection with HIV, end-stage renal disease, diabetes mellitus, and malignancy, as well as the use of immunosuppressive medications; hypoalbuminemia; and other known risk factors for TB, such as pregnancy, residence in nursing home, chemical dependency, history of incarceration, and homelessness.

Cases were defined by the following: (1) radiographic findings consistent with TB and clinical improvement when treated with antituberculous drugs or (2) a positive DNA hybridization test for M tuberculosis complex. DNA hybridization was performed using the Accuprobe system (Genprobe; San Diego, CA).6A liquid Bactec system was used for culture and sensitivity testing.7Isolates showing resistance were further categorized by reference laboratories. Isolates of M tuberculosis complex from a subset of 25 patients with extrapulmonary disease underwent nitrate reduction analysis as previously described8 to confirm the presence of M tuberculosis and to rule out Mycobacterium bovis. To identify specific infecting strains, restriction fragment length polymorphism analysis was performed on 22 isolates from patients with a positive culture for M tuberculosis complex (Michigan Department of Community Health; Lansing, MI). DNA “fingerprinting” was performed by digestion of DNA with PvuII, followed by hybridization to an IS6110 probe in standardized fashion.9 Bivariate analysis was used to determine significant differences between pulmonary and extrapulmonary cases. Three patients (4% of all cases) had both pulmonary and extrapulmonary involvement and, with the exception indicated in Table 2, were designated as extrapulmonary or pulmonary cases based on clinical presentation.

Eighty-two cases of TB in ethnic Somalis were identified in Minnesota between January 1, 1993, and June 30, 1998. In 1997, the incidence of TB in Somalis was 170 per 100,000 population based on an estimated population of 15,000 Somalis in the state.10 Somalis comprised < 0.4% of the state’s population, but accounted for 17% of all Minnesota cases of TB and 23% of the foreign-born cases. Forty-six percent of patients had extrapulmonary involvement, and in 1997, TB in Somalis was more likely to manifest as extrapulmonary disease than in the remainder of the state population with M tuberculosis (relative risk, 1.5; 95% confidence interval, 1.1 to 1.9; p < 0.007).

Table 1 compares the proportion of extrapulmonary cases among Somalis in Minnesota to national data for foreign-born and US-born blacks. Forty-six percent of Somali TB cases in Minnesota had disease in extrapulmonary locations compared with 22% of cases among US-born blacks and 33% among foreign-born blacks5 during the study period (p < 0.001). In addition, the incidence of TB among Somalis in Minnesota in 1997 is estimated to be 170 per 100,000 compared with 20.5/100,000 for all blacks in the United States and 2.5/100,000 for whites.11

Patient characteristics are summarized in Table 2. Ninety-three percent of patients were aged < 40 years, and one quarter were < 20 years of age. There was no statistically significant difference between the number of women and men with extrapulmonary or pulmonary disease manifestations. Both pulmonary and extrapulmonary cases were frequently diagnosed shortly after immigration, and 30% began treatment for TB within 3 months of arrival in the United States. More than half of the patients were diagnosed within 1 year and 83% within 2 years of immigration. Patients with pulmonary manifestations were more likely to be diagnosed within 6 months of immigration when compared with extrapulmonary cases (52% vs 26%; p = 0.03). All 42 (100%) pulmonary cases with known PPD skin-test status had positive results, whereas 32 of 35 (91%) with extrapulmonary disease had positive skin-test results. All three patients with extrapulmonary disease and negative PPD skin test results were anergic and had miliary involvement or concomitant AIDS.

The sites of extrapulmonary disease are summarized in Table 3: more than half (55%) had lymph node involvement, including cervical, mediastinal, axillary, and inguinal lymphadenitis. Five patients had evidence of TB in more than one extrapulmonary site.

The results of acid-fast bacteria (AFB) smears and cultures are summarized in Table 4. Cultures were not obtained in six cases because of young patient age or inaccessibility of the site of infection. Sixty-two (76%) patients had positive culture results; 33 of 38 patients (87%) with extrapulmonary disease and 29 of 44 patients (66%) with pulmonary disease had positive results. Of the cases with positive results, those with extrapulmonary TB were less likely to have had a positive smear for AFB. Twenty-two of 38 patients (58%) with extrapulmonary disease had a negative result on AFB smear but a positive result on culture, compared with 11 of 44 patients (25%) with pulmonary disease (p = 0.008). Of the 38 cases of extrapulmonary TB, M tuberculosis complex isolates from 25 patients (65%) with extrapulmonary disease underwent further laboratory analysis. All but one of these isolates were specifically identified as M tuberculosis, with one designated as indeterminate.

Drug resistance was unusual in this series of patients and similar in both pulmonary and extrapulmonary groups. Drug sensitivity testing was undertaken on isolates from 58 patients, 11 of whom (19%) had some form of resistance. Only 2 of 58 patients (3.4%), both with extrapulmonary involvement, had multidrug-resistant TB (ie, resistant to at least rifampin and isoniazid). In 1997, the national rate of multidrug-resistant TB was 1.3%.2 Drug sensitivity testing results were unavailable in 29% of cases (21% of extrapulmonary and 36% of pulmonary cases).

Only 2 of the 82 patients had AIDS. Other patients with concomitant immunocompromised states included three women who were pregnant at the time of diagnosis, and three patients with diabetes mellitus, one of whom had end-stage renal disease. No patient had a history of immunosuppressive therapy, malignancy, chemical dependency, homelessness, incarceration in a correctional facility, or residence in a nursing home.

TB classification before immigration was unknown in > 85% of patients in this study, and the exposure history was unknown in one third of patients. Nearly one fourth of patients gave a history consistent with prior treatment for TB or household contact with active disease. Twenty-two isolates underwent DNA fingerprinting using restriction fragment length polymorphism analysis. All but three patients (14%) had unique strains identified. There was no known contact between the three patients infected with the same strain.

This series of cases of TB in Somali immigrants in Minnesota reveals a high incidence of active disease and a distinct patient pattern of presentation, namely age < 40 years, recent immigration, frequent extrapulmonary involvement, and drug-sensitive M tuberculosis isolates. As of January 1, 1998, approximately 25,000 ethnic Somalis had immigrated to the United States, of whom an estimated 13,000 to 16,000 had settled in Minnesota.10 Based on these data, the incidence of TB in Somalis in Minnesota in 1997 was between 156/100,000 and 193/100,000, compared with a national incidence of 7.4/100,000 and 20.5/100,000 for all US blacks.11

Minnesota’s Somali population had a significantly greater proportion of extrapulmonary disease (46%) than US-born (22%) and foreign-born (33%) blacks.5 The proportion of cases of TB involving extrapulmonary sites has increased steadily in the United States from 8% in 1964 to 26.6% of cases in 1998 (19.3% exclusively extrapulmonary and an additional 7.3% with both pulmonary and extrapulmonary disease).45 The ability of preimmigration screening to more readily identify pulmonary than extrapulmonary disease may have contributed to the high proportion of extrapulmonary cases observed in the study. High rates of extrapulmonary disease have been previously reported in other immigrant populations from Asia and India.1213

TB in immigrant populations is thought to be primarily related to reactivation of latent disease with initial infection occurring in the country of origin.3,1415 Although restriction fragment length polymorphism analysis was performed on only a minority of our positive culture results, identification of specific M tuberculosis strains in this and previous studies in the United States have found an absence of clustering of cases in foreign-born persons, reinforcing the view that the initial infection is acquired abroad.19 Only gross estimates of the incidence of TB in Somalia can be made, but > 50% of the Somali population is estimated to be infected with M tuberculosis, with about 1% having active disease.22 The estimated per capita incidence rate for TB in Somalia for 1997 was between 100 and 249 per 100,000, which approximates the findings of this study.1

The large TB burden in Somalis in the United States and abroad is likely caused by multiple factors, including poverty, overcrowding, and limited medical resources. In addition, epidemiologic and molecular studies indicate there are also racial differences in resistance to TB.2326 These differences may be a function of the erratic global spread of TB with time and the presence of multiple, concurrent TB epidemics in various stages across the globe.2729 Although there is some evidence TB was present in sub-Saharan Africa long before the arrival of Europeans, historical records indicate the TB epidemic did not begin in this region until after 1900 in the wake of increasing contact with Europeans.2930

High incidence and mortality, greater disease burden in the young, and systemic manifestations of TB are thought to be manifestations of the early phase of an epidemic and are similar to the pattern of presentation we observed in the Somali population. It is unclear, however, whether TB disproportionately causes disease in younger Minnesota Somalis. More than 90% of the 1,075 Somalis who immigrated to Minnesota as primary refugees during the study period were < 40 years old, suggesting the Somali immigrant population as a whole is disproportionately young (M.O. Maliwat, MPH; personal communication; May 1999). The extent to which nutritional and socioeconomic factors contribute to the high rates of TB observed also remains unclear.

In this case series, extrapulmonary cases were more likely to have negative smear results than pulmonary cases, emphasizing the importance of appropriate bacteriologic culture and the early initiation of treatment in this setting. In recent years, extrapulmonary TB has been commonly associated with AIDS,3133 but only two patients in this study were positive for HIV infection, and other risk factors for TB were infrequent. As of 1990, lymph node involvement was the most common site of extrapulmonary disease in the United States, occurring in approximately 30% of cases.4,34 Lymphadenitis was also the most common manifestation in the Somalis, affecting 58% of extrapulmonary cases.

Previous studies have shown that immigrants classified as having inactive disease at the time of screening in their country of origin frequently have active disease when initially evaluated in their destination country.16,35 Minnesota’s aggressive surveillance program for the identification of new TB cases coupled with heightened clinical suspicion for TB among community caregivers when evaluating Somalis likely contributes to the higher incidence observed in the study. Nearly a third of cases were diagnosed with active TB within 3 months of immigration and more than three fourths were diagnosed within 2 years of immigration. Given that the vast majority of Minnesota Somalis are recent immigrants, however, a cohort study is needed to determine definitively whether recent immigrants have higher rates of infection than long-term residents. Nonetheless, the early presentation of such large numbers of cases is striking given that within 1 year of immigration, all refugees and permanent immigrants to the United States undergo chest radiographic screening for TB in their country of origin. Routine preimmigration screening does not identify TB in extrathoracic sites, and AFB smears rather than cultures are used to screen persons with suspicious chest radiographs. TB classification before immigration was unknown in 85% of patients in this series. Our data underscore the fact that many Somalis may have undetected active disease at the time of immigration.

This study of Somali immigrants is one of the first descriptions of TB in immigrants from sub-Saharan Africa to a developed country and demonstrates a high incidence of active disease, frequent extrapulmonary involvement, diagnosis soon after immigration, and infrequent infection with multidrug-resistant organisms. These findings are consistent with previous studies of immigrant populations in developed countries and may reflect the natural history of a population in an early phase of a TB epidemic. Health-care providers should maintain a high level of awareness for TB, including unusual extrapulmonary involvement, when evaluating Somali immigrants.

Abbreviations: AFB = acid-fast bacteria; PPD = purified protein derivative; TB = tuberculosis

Table Graphic Jump Location
Table 1. TB Cases in Somalis Compared With African Americans and Foreign-Born Blacks*
* 

January 1993–January 1996, Centers for Disease Control and Prevention data; January 1993–June 1998, MN data. Extrapulmonary and pulmonary cases for foreign-born and US-born blacks accessed from www.wonder.cdc.gov on March 6, 2000.

 

Percentages given in parentheses.

Table Graphic Jump Location
Table 2. Characteristics of TB in 82 Somali Patients in Minnesota
* 

Includes two cases with concomitant pulmonary and extrapulmonary disease.

 

Includes one case with concomitant pulmonary and extrapulmonary disease.

 

p = 0.03.

Table Graphic Jump Location
Table 3. Site of Disease in 38 Patients With Extrapulmonary TB*
* 

GU = genitourinary; ENT = ear, nose, and throat.

 

Percentages total > 100 because five cases had multiple sites of involvement.

Table Graphic Jump Location
Table 4. AFB Smear and Mycobacterium tuberculosis Culture Results in Minnesota Somali TB Cases*
* 

Percentages given in parentheses. cx = culture; EP = extrapulmonary.

 

Includes two cases with concomitant pulmonary and extrapulmonary disease.

 

Includes one case with concomitant pulmonary and extrapulmonary disease.

§ 

p = 0.008.

Dye, C, Scheele, S, Dolin, P, et al (1999) Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country.JAMA282,677-686. [CrossRef] [PubMed]
 
US Department of Health and Human Services. Tuberculosis Morbidity—United States 1997. MMWR Morb Mortal Wkly Rep 1998; 47:253–257.
 
Zuber, PLF, McKenna, MT, Binkin, NJ, et al Long-term risk of tuberculosis among foreign-born persons in the United States.JAMA1997;278,304-307. [CrossRef] [PubMed]
 
Thornton, GF Extrapulmonary tuberculosis, excluding the central nervous system. Rossman, MD MacGregor, RR eds.Tuberculosis: clinical management and new challenges1995,173-184 McGraw-Hill. New York, NY:
 
CDC WONDER Data Sets. Centers for Disease Control and Prevention Web Site. Tuberculosis Prevention Surveillance Reports. Available at: www.wonder.cdc.gov/DataSets. Accessed March 6, 2000.
 
Lebrun, L, Espinasse, F, Poveda, JD, et al Evaluation of nonradioactive DNA probes for identification of mycobacteria.J Clin Microbiol1992;30,2476-2478. [PubMed]
 
Siddiqui, F. BacTec system product and procedure manual. 1989; Becton Dickenson. Cockeysville, MD:.
 
Kubica, G, Kent, P Public health mycobacteriology: a guide for level III laboratory.1985,125-133 US Department of Health and Human Services and Centers for Disease Control. Atlanta, GA:
 
VanEmbden, JD, Cave, MD, Crawford, JT, et al Strain identification of mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standard methodology.J Clin Microbiol1993;31,406-409. [PubMed]
 
Tillotson K. Somalis are becoming part of the Twin Cities’ landscape. Minneapolis Star Tribune, March 22, 1998; Metro Section: 1A.
 
CDC Division of Tuberculosis Elimination. Centers for Disease Control and Prevention. Table 3: Tuberculosis Case Rates per 100,000 Population by Race/Ethnicity, Sex, and Age: United States, 1997. Available at: www.cdc.gov/nchstp/tb/surv. Accessed March 6, 2000.
 
Cowie, RL, Sharpe, JW Extrapulmonary tuberculosis: a high frequency in the absence of HIV infection.Int J Tuberc Lung Dis1997;1,159-162. [PubMed]
 
Medical Research Council Tuberculosis, and Chest Diseases Unit. National survey of tuberculosis notifications in England and Wales 1978–79. BMJ 1980; 281:895–898.
 
Enarson, D, Ashley, MJ, Grzybowski, S Tuberculosis in immigrants to Canada.Am Rev Respir Dis1979;119,11-18. [PubMed]
 
Enarson, DA, Sjogren, I, Grzybowski, S Incidence of tuberculosis among Scandinavian immigrants in Canada.Eur J Respir Dis1980;61,139-142. [PubMed]
 
DeRiemer, K, Chin, DP, Schecter, GF, et al Tuberculosis among immigrants and refugees.Arch Intern Med1998;158,753-759. [CrossRef] [PubMed]
 
Alland, D, Kalkut, GE, Moss, AR, et al Transmission of tuberculosis in New York City: an analysis by DNA fingerprinting and conventional epidemiologic methods.N Engl J Med1994;330,1710-1716. [CrossRef] [PubMed]
 
Friedman, CR, Stoeckle, MY, Kreiswirth, BN, et al Transmission of multi-drug resistant tuberculosis in a large urban setting.Am J Respir Crit Care Med1995;152,355-359. [PubMed]
 
Small, PM, Hopewell, PC, Singh, SP, et al The epidemiology of tuberculosis in San Francisco: a population-based study using conventional and molecular methods.N Engl J Med1994;330,1703-1709. [CrossRef] [PubMed]
 
Laughlin, LW, Legters, LJ Disease threats in Somalia.Am J Trop Med1993;489,6-10
 
Oldfield, EC, III, Rodier, GR, Gray, GC The endemic infectious diseases in Somalia.Clin Infect Dis1993;16(suppl 3),S132-S157. [PubMed]
 
Powell, KE, Brown, DE, Farer, LS Tuberculosis among Indochinese refugees in the United States.JAMA1983;249,1455-1460. [CrossRef] [PubMed]
 
Comstock, GW Tuberculosis in twins: a re-analysis of the Prophit Survey.Am Rev Respir Dis1978;117,621-624. [PubMed]
 
Stead, WW, Senner, JW, Reddick, WT, et al Racial differences in susceptibility to infection byMycobacterium tuberculosis.N Engl J Med1990;322,422-427. [CrossRef] [PubMed]
 
Skamene, E Genetic control of susceptibility to mycobacterial infections.Rev Infect Dis1989;11(suppl 2),S394-S399. [PubMed]
 
Bellamy, R, Ruwende, C, Corrah, T, et al Variations in theNRAMP1gene and susceptibility to tuberculosis in West Africans.N Engl J Med1998;338,640-644. [CrossRef] [PubMed]
 
Stead, WW Genetics and resistance to tuberculosis: could resistance be enhanced by genetic engineering?Ann Intern Med1992;116,937-941. [PubMed]
 
Grzybowski, S Tuberculosis: a look at the world situation.Chest1983;84,756-761. [CrossRef] [PubMed]
 
Stead, WW Tuberculosis in Africa.Int J Tuberc Lung Dis1998;2,791-792. [PubMed]
 
Daniel, TM The early history of tuberculosis in central East Africa: insights from the clinical records of the first twenty years of Mengo Hospital and review of relevant literature.Int J Tuberc Lung Dis1998;2,784-790. [PubMed]
 
Small, PM, Schecter, GF, Goodman, PH, et al Treatment of tuberculosis in patients with advanced human immunodeficiency virus infection.N Engl J Med1991;324,289-294. [CrossRef] [PubMed]
 
Shafer, RW, Kim, DS, Weiss, JP, et al Extrapulmonary tuberculosis in patients with human immunodeficiency virus infection.Medicine1991;70,384-396. [PubMed]
 
Barnes, PF, Bloch, AB, Davidson, PT, et al Tuberculosis in patients with human immunodeficiency virus.N Engl J Med1991;324,1644-1650. [CrossRef] [PubMed]
 
Rieder, HL, Snider, DE, Jr, Cauthen, GM Extrapulmonary tuberculosis in the United States.Am Rev Respir Dis1990;141,347-351. [PubMed]
 
Wang, JS, Allen, EA, Enarson, DA, et al Tuberculosis in recent Asian immigrants to British Columbia, Canada: 1982–1985.Tubercle1991;72,277-283. [CrossRef] [PubMed]
 

Figures

Tables

Table Graphic Jump Location
Table 1. TB Cases in Somalis Compared With African Americans and Foreign-Born Blacks*
* 

January 1993–January 1996, Centers for Disease Control and Prevention data; January 1993–June 1998, MN data. Extrapulmonary and pulmonary cases for foreign-born and US-born blacks accessed from www.wonder.cdc.gov on March 6, 2000.

 

Percentages given in parentheses.

Table Graphic Jump Location
Table 2. Characteristics of TB in 82 Somali Patients in Minnesota
* 

Includes two cases with concomitant pulmonary and extrapulmonary disease.

 

Includes one case with concomitant pulmonary and extrapulmonary disease.

 

p = 0.03.

Table Graphic Jump Location
Table 3. Site of Disease in 38 Patients With Extrapulmonary TB*
* 

GU = genitourinary; ENT = ear, nose, and throat.

 

Percentages total > 100 because five cases had multiple sites of involvement.

Table Graphic Jump Location
Table 4. AFB Smear and Mycobacterium tuberculosis Culture Results in Minnesota Somali TB Cases*
* 

Percentages given in parentheses. cx = culture; EP = extrapulmonary.

 

Includes two cases with concomitant pulmonary and extrapulmonary disease.

 

Includes one case with concomitant pulmonary and extrapulmonary disease.

§ 

p = 0.008.

References

Dye, C, Scheele, S, Dolin, P, et al (1999) Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country.JAMA282,677-686. [CrossRef] [PubMed]
 
US Department of Health and Human Services. Tuberculosis Morbidity—United States 1997. MMWR Morb Mortal Wkly Rep 1998; 47:253–257.
 
Zuber, PLF, McKenna, MT, Binkin, NJ, et al Long-term risk of tuberculosis among foreign-born persons in the United States.JAMA1997;278,304-307. [CrossRef] [PubMed]
 
Thornton, GF Extrapulmonary tuberculosis, excluding the central nervous system. Rossman, MD MacGregor, RR eds.Tuberculosis: clinical management and new challenges1995,173-184 McGraw-Hill. New York, NY:
 
CDC WONDER Data Sets. Centers for Disease Control and Prevention Web Site. Tuberculosis Prevention Surveillance Reports. Available at: www.wonder.cdc.gov/DataSets. Accessed March 6, 2000.
 
Lebrun, L, Espinasse, F, Poveda, JD, et al Evaluation of nonradioactive DNA probes for identification of mycobacteria.J Clin Microbiol1992;30,2476-2478. [PubMed]
 
Siddiqui, F. BacTec system product and procedure manual. 1989; Becton Dickenson. Cockeysville, MD:.
 
Kubica, G, Kent, P Public health mycobacteriology: a guide for level III laboratory.1985,125-133 US Department of Health and Human Services and Centers for Disease Control. Atlanta, GA:
 
VanEmbden, JD, Cave, MD, Crawford, JT, et al Strain identification of mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standard methodology.J Clin Microbiol1993;31,406-409. [PubMed]
 
Tillotson K. Somalis are becoming part of the Twin Cities’ landscape. Minneapolis Star Tribune, March 22, 1998; Metro Section: 1A.
 
CDC Division of Tuberculosis Elimination. Centers for Disease Control and Prevention. Table 3: Tuberculosis Case Rates per 100,000 Population by Race/Ethnicity, Sex, and Age: United States, 1997. Available at: www.cdc.gov/nchstp/tb/surv. Accessed March 6, 2000.
 
Cowie, RL, Sharpe, JW Extrapulmonary tuberculosis: a high frequency in the absence of HIV infection.Int J Tuberc Lung Dis1997;1,159-162. [PubMed]
 
Medical Research Council Tuberculosis, and Chest Diseases Unit. National survey of tuberculosis notifications in England and Wales 1978–79. BMJ 1980; 281:895–898.
 
Enarson, D, Ashley, MJ, Grzybowski, S Tuberculosis in immigrants to Canada.Am Rev Respir Dis1979;119,11-18. [PubMed]
 
Enarson, DA, Sjogren, I, Grzybowski, S Incidence of tuberculosis among Scandinavian immigrants in Canada.Eur J Respir Dis1980;61,139-142. [PubMed]
 
DeRiemer, K, Chin, DP, Schecter, GF, et al Tuberculosis among immigrants and refugees.Arch Intern Med1998;158,753-759. [CrossRef] [PubMed]
 
Alland, D, Kalkut, GE, Moss, AR, et al Transmission of tuberculosis in New York City: an analysis by DNA fingerprinting and conventional epidemiologic methods.N Engl J Med1994;330,1710-1716. [CrossRef] [PubMed]
 
Friedman, CR, Stoeckle, MY, Kreiswirth, BN, et al Transmission of multi-drug resistant tuberculosis in a large urban setting.Am J Respir Crit Care Med1995;152,355-359. [PubMed]
 
Small, PM, Hopewell, PC, Singh, SP, et al The epidemiology of tuberculosis in San Francisco: a population-based study using conventional and molecular methods.N Engl J Med1994;330,1703-1709. [CrossRef] [PubMed]
 
Laughlin, LW, Legters, LJ Disease threats in Somalia.Am J Trop Med1993;489,6-10
 
Oldfield, EC, III, Rodier, GR, Gray, GC The endemic infectious diseases in Somalia.Clin Infect Dis1993;16(suppl 3),S132-S157. [PubMed]
 
Powell, KE, Brown, DE, Farer, LS Tuberculosis among Indochinese refugees in the United States.JAMA1983;249,1455-1460. [CrossRef] [PubMed]
 
Comstock, GW Tuberculosis in twins: a re-analysis of the Prophit Survey.Am Rev Respir Dis1978;117,621-624. [PubMed]
 
Stead, WW, Senner, JW, Reddick, WT, et al Racial differences in susceptibility to infection byMycobacterium tuberculosis.N Engl J Med1990;322,422-427. [CrossRef] [PubMed]
 
Skamene, E Genetic control of susceptibility to mycobacterial infections.Rev Infect Dis1989;11(suppl 2),S394-S399. [PubMed]
 
Bellamy, R, Ruwende, C, Corrah, T, et al Variations in theNRAMP1gene and susceptibility to tuberculosis in West Africans.N Engl J Med1998;338,640-644. [CrossRef] [PubMed]
 
Stead, WW Genetics and resistance to tuberculosis: could resistance be enhanced by genetic engineering?Ann Intern Med1992;116,937-941. [PubMed]
 
Grzybowski, S Tuberculosis: a look at the world situation.Chest1983;84,756-761. [CrossRef] [PubMed]
 
Stead, WW Tuberculosis in Africa.Int J Tuberc Lung Dis1998;2,791-792. [PubMed]
 
Daniel, TM The early history of tuberculosis in central East Africa: insights from the clinical records of the first twenty years of Mengo Hospital and review of relevant literature.Int J Tuberc Lung Dis1998;2,784-790. [PubMed]
 
Small, PM, Schecter, GF, Goodman, PH, et al Treatment of tuberculosis in patients with advanced human immunodeficiency virus infection.N Engl J Med1991;324,289-294. [CrossRef] [PubMed]
 
Shafer, RW, Kim, DS, Weiss, JP, et al Extrapulmonary tuberculosis in patients with human immunodeficiency virus infection.Medicine1991;70,384-396. [PubMed]
 
Barnes, PF, Bloch, AB, Davidson, PT, et al Tuberculosis in patients with human immunodeficiency virus.N Engl J Med1991;324,1644-1650. [CrossRef] [PubMed]
 
Rieder, HL, Snider, DE, Jr, Cauthen, GM Extrapulmonary tuberculosis in the United States.Am Rev Respir Dis1990;141,347-351. [PubMed]
 
Wang, JS, Allen, EA, Enarson, DA, et al Tuberculosis in recent Asian immigrants to British Columbia, Canada: 1982–1985.Tubercle1991;72,277-283. [CrossRef] [PubMed]
 
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