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Active pulmonary tuberculosis and latent tuberculosis infection among homeless people in Seoul, South Korea: a cross-sectional study
© Lee et al.; licensee BioMed Central Ltd. 2013
Received: 5 August 2012
Accepted: 23 July 2013
Published: 5 August 2013
The aim of this study was to determine the prevalence rate of latent TB infection (LTBI) and active TB among homeless in Seoul metropolitan city, South Korea, and to compare the TB burden among homeless people with that of a control group.
The homeless participants were recruited from five sites between October 30, 2009 and April 12, 2010. LTBI was diagnosed through the QuantiFERON(R) TB Gold In-Tube(QFT-GIT) assay and a tuberculin skin test(TST) and, and active PTB was diagnosed based on chest radiography.
Among 313 participants, the prevalence of LTBI was 75.9% (95% CI, 71.1-80.8%) and 79.8% (95% CI, 74.9-84.7%) based on a QFT-GIT assay and the TST, respectively, and that of active PTB was 5.8% (95% CI, 3.2-8.3%). The prevalence of LTBI among homeless participants was about five times higher than controls. Also, the age-specific prevalence rate ratio of active PTB was as high as 24.86.
The prevalence rate of LTBI as well as active PTB among homeless people was much higher than that of the general population in South Korea. Thus, adequate strategies to reduce the TB burden among homeless people are needed.
Among infectious diseases, tuberculosis (TB) is the leading cause of mortality and morbidity worldwide, with 9.4 million incident cases and 1.7 million deaths in 2009. Most TB cases occur in developing countries . In industrialized countries, TB is decreasing and the majority of TB cases occur in minority groups, including migrants, refugees, and itinerant people .
Homeless people are also at high risk for TB because of poor nutrition, alcohol consumption, and tobacco smoking . Their unsafe housing conditions where TB organisms may be spread through insufficient air exchange also contributes on the occurrence of TB . In many industrialised countries, TB rates among the homeless can be up to 20 times higher than in the general population . TB disease in homeless people is especially problematic because it may be highly contagious and can presents as advanced disease with poor outcomes . Studies suggest that the majority of urban homeless TB cases are attributable to ongoing transmission of TB in developing countries, and recommendations call for tailored programs to address TB in these high-risk groups . However, although several studies [5, 7–10] have reported the prevalence rate of TB among homeless people, prior studies rarely compared the prevalence rates of both active and latent TB infection among homeless people to that of a control group or the general population. Rather, there is a report showing no statistically significant difference in pulmonary TB between homeless people and general population . Additionally, there is no report on the burden and impact of TB in homeless people in South Korea, a middle-income country and a region with an intermediate TB burden .
The aim of this study was to explore the prevalence rate of latent TB infection (LTBI) and active TB among homeless in Seoul metropolitan city, South Korea, and to compare the TB burden among homeless people with that of a control group.
Participants were recruited in Seoul, South Korea, between October 30, 2009 and April 12, 2010 by community outreach or by visits to homeless shelters at two streets adjacent to major railroad stations in Seoul (Seoul Station [site A] and Yeongdeungpo Station [site B]) where homeless people congregate. Three homeless shelters, sites C, D and E, were also randomly selected and visited by us. Monthly average number of homeless was 140–200 in site A, 60–100 in site B, and approximate total of 400 in site C, D and E.
Persons were eligible to participate if they were at least 20 years of age and if they provided written informed consent. Sample size was calculated as 384 by using the following formula : n = (1.96)2p(1-p)/d2, where n = sample size, 1.96 = Z statistic for 95% confidence, p = expected prevalence rate = 0.5, d = precision = 0.05. To facilitate enrollment, vouchers valued at about 10 US dollars were provided on second visits. This research was funded by Korea Centers for Disease Control and Prevention (2009-E31001-00).
After giving informed consent, each participant was interviewed using a questionnaire about demographics, previous history of TB, smoking status, and respiratory symptoms. Height and weight were measured, and the presence of scars from bacille Calmette-Guerin (BCG) vaccination was confirmed. Also, chest radiographs (posterior–anterior) were viewed, and an interferon-γ (IFN-γ release assay (IGRA), QuantiFERON® TB Gold In-Tube (QFT-GIT; Celletis Ltd., Victoria, Australia) and a tuberculin skin test (TST) were conducted. This study was reviewed and approved by the Institutional Review Board of Seoul National University Hospital.
Interferon-γ release assay
The QuantiFERON-TB Gold In-Tube (QFT-GIT) assay was performed according to the manufacturer’s instructions. The plasma concentration of IFN-γ was measured by enzyme-linked immunosorbent assay (ELISA), and the technician who performed the tests was blind to the clinical and radiographic information of the participants. Test results were interpreted as negative, indeterminate, or positive (cutoff, 0.35 IU/mL) using the manufacturer’s software . Participants with indeterminate IGRA results were excluded from further analysis.
Tuberculin skin test
After collection of blood samples for the QFT-GIT assay, the TST was performed on the volar side of the forearm according to the Mantoux method using a 2-TU dose of purified protein derivative RT23 (Statens Serum Institut, Copenhagen, Denmark), and induration was measured in millimetres after 48–72 h using the ballpoint pen method . The investigator who performed the TST was blind to the IGRA results as well as to the clinical and radiographic information of the participants. We defined a positive test as an induration of ≥10 mm .
Interpretation of chest radiographs
Radiographic diagnoses of active pulmonary and old healed TB were made based on previously published criteria  by two independent readers, including one board-certified radiologist. If the results from two were different, the final decision was made by discussion. Lesions including a cavity, a “tree-in-bud” appearance, or multiple noncalcified poorly circumscribed nodules without cavity were classified as active pulmonary TB. Lesions appearing mainly as calcified nodules or fibrotic bands in the upper lobe were classified as old healed TB.
Comparison with general population of the prevalence of active pulmonary TB, and with age, sex, and the presence of old healed lesions on chest radiograph-matched controls of the prevalence of LTBI
The prevalence rate of active pulmonary TB in homeless participants was compared with that of the population included in 2010 Korea National Health and Nutrition Examination Survey (KNHANES) by using an age-adjusted prevalence rate ratio. KNHANES used a stratified, multi-stage, clustered, probability sampling method based on the 2000 Korean Population Census administered by the National Statistical Office of Korea to select a representative sample of Korean people aged 18 years or over . Presence of active pulmonary TB was decided based on chest radiographs. Interpretation of chest radiographs was performed in an identical manner described above.
The expected numbers of active TB individuals were extrapolated from the prevalence rate of each age group in the 2010 Korea National Health and Nutrition Examination Survey.
Meanwhile, positive rates of the QFT-GIT assay and the TST were compared with controls from a Seoul National University cohort. The ‘Seoul National University cohort’ consists of prospectively enrolled 319 (non-homeless) participants with or without radiographic lesions suggesting old-healed TB. The detail of the cohort was described in another article . From this cohort, we randomly selected age, sex, and the presence of old healed TB on chest radiograph, could find 67 pairs matching. QFT-GIT and TST were conducted in a same manner. Conditional logistic regression analyses were performed to calculate the odds ratio (OR) of positive rates of the QFT-GIT assay and the TST in homeless participants compared with those in matched controls.
Demographic and clinical characteristics of participants
Demographic and clinical characteristics of homeless participants
Age (years), median (range)
Body mass index (kg/m 2 ), median (range)
History of previous TB
Current or ex- smoker
Presence of BCG scar
Prevalence rate of active pulmonary TB based on CXR
Prevalence rate of active pulmonary TB and lesions suggesting old healed TB based on CXR
Number of participants
Active pulmonary TB
Old healed TB
Significant pleural thickening
Comparison of prevalence rate of active pulmonary TB between samples from general male and homeless male populations between 2009 and 2010 using age-specific prevalence rate ratio (PR)
Samples from general population
Number of samples
Number of active TB cases
Active TB prevalence rate (/1,000)
Number of samples
Number of active TB cases (observed)
Number of active TB cases (expected)
Risk factors of active pulmonary tuberculosis among homeless participants (multivariable logistic regression analysis)
History of previous TB
Presence of BCG scar
Presence of diabetes
Prevalence rate of latent TB infection among participants without active pulmonary TB
Prevalence rate of TB infection in homeless people
Prevalence rate of TB infection in homeless people stratified by the status of BCG vaccination
BCG scar negative
BCG scar positive
BCG scar unknown*
BCG scar negative
BCG scar positive
We could match 67 pairs from the present study and Seoul National University cohort study as described above. Positive rates of the QFT-GIT assay and the TST were much higher among participants compared with those controls matched for age, sex, and presence of old-healed TB lesions on CXR (QFT-GIT; 91.0% vs. 74.6%, OR, 4.67; 95% CI, 1.34–16.2 and TST; 77.4% vs. 49.1%, OR, 6.0; 95% CI, 1.8–20.4).
Through this cross-sectional study that focuses on homeless people, we determined that the prevalence of radiographic active pulmonary TB was 5.8%. In addition, prevalence of LTBI was 75.9% based on a QFT-GIT assay and 79.8% based on a TST. The age-adjusted prevalence rate ratio of active TB in males was as high as 24.86. Also, the prevalence of LTBI among homeless participants was about five times higher when compared with controls matched for age, gender, and presence of old healed TB lesions on CXR.
The prevalence of active TB as well as LTBI in our study was higher than that reported in New York in the US (31% of LTBI)  and in the Airin district in Japan (1.5% and 50.6% rate of active TB and LTBI, respectively) . The higher rate of active TB and LTBI among homeless people in Seoul reflects the higher prevalence of active TB in South Korea (115 per 100 000 persons) compared with the US (4.7 per 100 000 persons) and Japan (27 per 100 000 persons) in 2009 .
Development of TB disease is a two-step process: infection by transmission and progression to active disease. The risk of infection is dependent on exogenous factors. The intimacy and duration of contact with active TB cases, the degree of infectiousness of the case, and the shared environment in which the contact takes place are important risk factors [19–22]. Most homeless people in our study had resided in shelters or railroad stations, where they slept in crowded environments, conditions that could enhance transmission of tuberculosis bacilli . High prevalence of LTBI among homeless in our study could be understood in this context.
Meanwhile, development of active TB depends largely on endogenous factors including HIV/AIDS , radiographic evidence of old healed TB , diabetes mellitus , chronic renal failure , immunosuppressive treatment such as TNF-α inhibitors  and use of steroids . In our study, being underweight, defined as a body mass index (BMI) <18.5 kg/m2, and a history of TB were independent risk factors for active pulmonary TB. Being underweight, as an indication of malnutrition, is a well-known risk factor for progression from LTBI to active disease . Malnutrition is reported to attenuate human immunity against M. tuberculosis[27–29] Because a history of previous TB is a risk factor in addition to underweight for active pulmonary TB in our study, a considerable proportion of active TB among these homeless people might be reactivated TB; however, molecular comparisons of TB strains could not be performed. Although a majority of TB cases in urban homeless populations has been regarded as attributable to ongoing transmission in shelters , our study underscores the importance of reactivation of previous TB among the homeless population.
This study did have its limitations. First, the prevalence of active TB was not based on a sputum acid-fast bacillus smear and culture but on CXR. The diagnosis of active TB based on CXR could be inaccurate as well as over-sensitive [30–32] Second, the selection of six sites of homeless populations was based on random sampling and may have caused selection bias. Third, the number of participants did not reach the calculated sample size, which could make the estimation underpowered. Fourth, our study used two different control groups (people with active TB and people with latent TB) which might result in a potential bias. Finally, possible risk factors for TB development such as the duration of, HIV/AIDS, alcohol addiction, mental illness, history of imprisonment of the participants were not evaluated thoroughly. This might have biased the estimation of LTBI prevalence rate and the results of comparisons.
In conclusion, the prevalence rate of LTBI as well as active pulmonary TB among homeless people was much higher than that among general population in South Korea. Thus, adequate strategies to reduce the TB burden among homeless people are needed.
Co-authors: Chang-Hoon Lee, Yun-Jeong Jeong, Eun Young Heo, Jong Sun Park, Ji Sun Lee, Byoung Jun Lee, Young Sik Park, Eun Hee Song, Yun Jung Yang, Young Soo Cho, En-hi Cho, Kyoung-in Na, Eun-Jeong Oh, Jin-beom Lee, Soo-Yeon Oh, HeeJin Kim and Chang Min Park.
We thank Hyun-Jeong Lee for her kind advice and written-English support.
- WHO: Global tuberculosis control: epidemiology, strategy, financing: WHO report 2010. 2010, Geneva, Switzerland: World Health Organization 2010Google Scholar
- Figueroa-Munoz JI, Ramon-Pardo P: Tuberculosis control in vulnerable groups. Bull World Health Organ. 2008, 86 (9): 733-735. 10.2471/BLT.06.038737.View ArticlePubMedPubMed CentralGoogle Scholar
- Burki T: Tackling tuberculosis in London’s homeless population. Lancet. 2010, 376 (9758): 2055-2056. 10.1016/S0140-6736(10)62282-9.View ArticlePubMedGoogle Scholar
- Hwang SW, Kiss A, Ho MM, Leung CS, Gundlapalli AV: Infectious disease exposures and contact tracing in homeless shelters. J Health Care Poor Underserved. 2008, 19 (4): 1163-1167. 10.1353/hpu.0.0070.View ArticlePubMedPubMed CentralGoogle Scholar
- Khan K, Rea E, McDermaid C, Stuart R, Chambers C, Wang J, Chan A, Gardam M, Jamieson F, Yang J, et al: Active tuberculosis among homeless persons, Toronto, Ontario, Canada, 1998–2007. Emerg Infect Dis. 2011, 17 (3): 357-365. 10.3201/eid1703.100833.View ArticlePubMedPubMed CentralGoogle Scholar
- Brewer TF, Heymann SJ, Krumplitsch SM, Wilson ME, Colditz GA, Fineberg HV: Strategies to decrease tuberculosis in us homeless populations: a computer simulation model. Jama. 2001, 286 (7): 834-842. 10.1001/jama.286.7.834.View ArticlePubMedGoogle Scholar
- Moss AR, Hahn JA, Tulsky JP, Daley CL, Small PM, Hopewell PC: Tuberculosis in the homeless. A prospective study. Am J Respir Crit Care Med. 2000, 162 (2 Pt 1): 460-464.View ArticlePubMedGoogle Scholar
- Haddad MB, Wilson TW, Ijaz K, Marks SM, Moore M: Tuberculosis and homelessness in the United States, 1994–2003. JAMA. 2005, 293 (22): 2762-2766. 10.1001/jama.293.22.2762.View ArticlePubMedGoogle Scholar
- Tabuchi T, Takatorige T, Hirayama Y, Nakata N, Harihara S, Shimouchi A, Fujita K, Yoshida H, Tamura Y, Nagai T, et al: Tuberculosis infection among homeless persons and caregivers in a high-tuberculosis-prevalence area in Japan: a cross-sectional study. BMC Infect Dis. 2011, 11: 22-10.1186/1471-2334-11-22.View ArticlePubMedPubMed CentralGoogle Scholar
- McAdam JM, Bucher SJ, Brickner PW, Vincent RL, Lascher S: Latent tuberculosis and active tuberculosis disease rates among the homeless, New York, New York, USA, 1992–2006. Emerg Infect Dis. 2009, 15 (7): 1109-1111. 10.3201/eid1507.080410.View ArticlePubMedPubMed CentralGoogle Scholar
- Beijer U, Andreasson S: Physical diseases among homeless people: gender differences and comparisons with the general population. Scand J Public Health. 2009, 37 (1): 93-100.View ArticlePubMedGoogle Scholar
- Daniel WW: Biostatics: a foundation for analysis in the health sciences. 1999, New York: John Wiley & Sons, 7Google Scholar
- Cellestis: QuantiFERON®-TB Gold In-Tube Package Insert. Vol. 2010, 2006. 2006, Cellestis Limited (Australia), Cellestis Inc. (USA) and Cellestis GmbH (Europe), http://www.cellestis.com/IRM/Company/ShowPage.aspx?CPID=1171,Google Scholar
- Sokal JE: Editorial: measurement of delayed skin-test responses. N Engl J Med. 1975, 293 (10): 501-502. 10.1056/NEJM197509042931013.View ArticlePubMedGoogle Scholar
- Ryu S, Park YK, Bai GH, Kim SJ, Park SN, Kang S: 3′UTR polymorphisms in the NRAMP1 gene are associated with susceptibility to tuberculosis in Koreans. Int J Tuberc Lung Dis. 2000, 4 (6): 577-580.PubMedGoogle Scholar
- Graham S, Das GK, Hidvegi RJ, Hanson R, Kosiuk J, Al ZK, Menzies D: Chest radiograph abnormalities associated with tuberculosis: reproducibility and yield of active cases. Int J Tuberc Lung Dis. 2002, 6 (2): 137-142.PubMedGoogle Scholar
- Lee SW, Kim YS, Kim DS, Oh YM, Lee SD: The risk of obstructive lung disease by previous pulmonary tuberculosis in a country with intermediate burden of tuberculosis. J Korean Med Sci. 2011, 26 (2): 268-273. 10.3346/jkms.2011.26.2.268.View ArticlePubMedPubMed CentralGoogle Scholar
- Jeong YJ, Yoon S, Koo HK, Lim HJ, Lee JS, Lee SM, Yang SC, Yoo CG, Kim YW, Han SK, et al: Positive tuberculin skin test or interferon-gamma release assay in patients with radiographic lesion suggesting old healed tuberculosis. J Korean Med Sci. 2012, 27 (7): 761-766. 10.3346/jkms.2012.27.7.761.View ArticlePubMedPubMed CentralGoogle Scholar
- Shaw JB, Wynn-Williams N: Infectivity of pulmonary tuberculosis in relation to sputum status. Am Rev Tuberc. 1954, 69 (5): 724-732.PubMedGoogle Scholar
- Ferebee SH: Controlled chemoprophylaxis trials in tuberculosis. A general review. Bibl Tuberc. 1970, 26: 28-106.PubMedGoogle Scholar
- Rouillon A, Perdrizet S, Parrot R: Transmission of tubercle bacilli: the effects of chemotherapy. Tubercle. 1976, 57 (4): 275-299. 10.1016/S0041-3879(76)80006-2.View ArticlePubMedGoogle Scholar
- Grzybowski S, Barnett GD, Styblo K: Contacts of cases of active pulmonary tuberculosis. Bull Int Union Tuberc. 1975, 50 (1): 90-106.PubMedGoogle Scholar
- Pablos-Mendez A, Blustein J, Knirsch CA: The role of diabetes mellitus in the higher prevalence of tuberculosis among Hispanics. Am J Public Health. 1997, 87 (4): 574-579. 10.2105/AJPH.87.4.574.View ArticlePubMedPubMed CentralGoogle Scholar
- Askling J, Fored CM, Brandt L, Baecklund E, Bertilsson L, Coster L, Geborek P, Jacobsson LT, Lindblad S, Lysholm J, et al: Risk and case characteristics of tuberculosis in rheumatoid arthritis associated with tumor necrosis factor antagonists in Sweden. Arthritis Rheum. 2005, 52 (7): 1986-1992. 10.1002/art.21137.View ArticlePubMedGoogle Scholar
- Jick SS, Lieberman ES, Rahman MU, Choi HK: Glucocorticoid use, other associated factors, and the risk of tuberculosis. Arthritis Rheum. 2006, 55 (1): 19-26. 10.1002/art.21705.View ArticlePubMedGoogle Scholar
- Palmer CE, Jablon S, Edwards PQ: Tuberculosis morbidity of young men in relation to tuberculin sensitivity and body build. Am Rev Tuberc. 1957, 76 (4): 517-539.PubMedGoogle Scholar
- Cegielski JP, McMurray DN: The relationship between malnutrition and tuberculosis: evidence from studies in humans and experimental animals. Int J Tuberc Lung Dis. 2004, 8 (3): 286-298.PubMedGoogle Scholar
- Kim HJ, Lee CH, Shin S, Lee JH, Kim YW, Chung HS, Han SK, Shim YS, Kim DK: The impact of nutritional deficit on mortality of in-patients with pulmonary tuberculosis. Int J Tuberc Lung Dis. 2010, 14 (1): 79-85.PubMedGoogle Scholar
- Kim DK, Kim HJ, Kwon SY, Yoon HI, Lee CT, Kim YW, Chung HS, Han SK, Shim YS, Lee JH: Nutritional deficit as a negative prognostic factor in patients with miliary tuberculosis. Eur Respir J. 2008, 32 (4): 1031-1036. 10.1183/09031936.00174907.View ArticlePubMedGoogle Scholar
- Balabanova Y, Coker R, Fedorin I, Zakharova S, Plavinskij S, Krukov N, Atun R, Drobniewski F: Variability in interpretation of chest radiographs among Russian clinicians and implications for screening programmes: observational study. BMJ. 2005, 331 (7513): 379-382. 10.1136/bmj.331.7513.379.View ArticlePubMedPubMed CentralGoogle Scholar
- Schlossberg D: Acute tuberculosis. Infect Dis Clin North Am. 2010, 24 (1): 139-146. 10.1016/j.idc.2009.10.009.View ArticlePubMedGoogle Scholar
- Jeon K, Koh WJ, Kwon OJ, Suh GY, Chung MP, Kim H, Lee NY, Park YK, Bai GH: Recovery rate of NTM from AFB smear-positive sputum specimens at a medical centre in South Korea. Int J Tuberc Lung Dis. 2005, 9 (9): 1046-1051.PubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://0-www.biomedcentral.com.brum.beds.ac.uk/1471-2458/13/720/prepub
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