Original Article

Pulmonary Tuberculosis Increases the
Risk of Lung Cancer
A Population-Based Cohort Study

Chen-Yi Wu, MD1,2; Hsiao-Yun Hu, PhD3; Cheng-Yun Pu, PhD2; Nicole Huang, PhD4; Hsi-Che Shen, MD, PhD5;
Chung-Pin Li, MD, PhD6,7; and Yiing-Jeng Chou, MD, MPH, PhD2

BACKGROUND: The possible effect of pulmonary tuberculosis (TB) on subsequent lung cancer development has
been suspected, but the evidence remains inconsistent. The purpose of this study was to perform a nationwide popu-
lation-based cohort study to investigate the risk of lung cancer after pulmonary TB infection. METHODS: This nation-
wide population-based cohort study was based on data obtained from the Taiwan National Health Insurance
Database. In total, 5657 TB patients and 23,984 controls matched for age and sex were recruited for the study from
1997 to 2008. RESULTS: The incidence rate of lung cancer (269 of 100,000 person-years) was significantly higher in
the pulmonary TB patients than that in controls (153 of 100,000 person-years) (incidence rate ratio [IRR], 1.76; 95%
confidence interval [CI], 1.33-2.32; P < .001). Compared with the controls, the IRRs of lung cancer in the TB cohort
were 1.98 at 2 to 4 years, 1.42 at 5 to 7 years, and 1.59 at 8 to 12 years after TB infections. The multivariate Cox pro-
portional hazards model revealed pulmonary TB infections (hazard ratio [HR], 1.64; 95% CI, 1.24-2.15; P < .001) and
chronic obstructive pulmonary disease (HR, 1.09; 95% CI, 1.03-1.14; P ¼ .002) to be independent risk factors for lung
cancer. CONCLUSIONS: Pulmonary infection with TB is associated with an increased risk of lung cancer. Cancer
2011;117:618–24. V
C 2010 American Cancer Society.

KEYWORDS: tuberculosis, lung cancer, cohort study, population-based..

Tuberculosis (TB) poses a global public health threat and remains 1 of the major causes of death among infectious dis-
eases. It is estimated that 1=3 of the human population harbors TB in its latent form.1,2 With aging or a deteriorated immune
system, the causative microorganism, Mycobacterium tuberculosis, can reactivate and cause severe and prolonged pneumonia,
pulmonary scarring, and wasting. Pulmonary TB comprises about 85% of clinical TB cases and exists as a chronic inflamma-
tion process that may lead to carcinogenesis of the lung tissue.3 Lung cancer is also a major cause of morbidity and mortality; it
comprises approximately 12.4% of all new cancer cases, and accounts for 29% of all cancer deaths.4
The possible relationship between pulmonary TB and subsequent lung cancer development has attracted attention
for several decades. However, the evidence is inconsistent, with some reporting a positive association, whereas others have
reported an insignificant association.5-11 The temporal relationship between TB and lung cancer is also not clear. TB and
lung cancer have a large public health impact, and therefore the association between these 2 diseases deserves detailed
investigation.
A meta-analysis performed by Liang et al revealed a positive association between pulmonary TB and subsequent
lung cancer.12 However, the cited reports were mostly case-control studies. Recall bias of exposure assessment, selection
bias of the control group, and the validity of the reported TB diagnosis are all possible limitations in this type of study. In
addition, this approach makes it difficult to confirm a temporal relationship between TB and subsequent lung cancer.
Some cohort studies have reported a positive association between TB and lung cancer.10,11 However, these studies might

Corresponding authors: Yiing-Jeng Chou, MD, MPH, PhD, Institute of Public Health, National Yang-Ming University, No. 155, Sec. 2, Li-Nong Street, Taipei 112,
Taiwan; Fax: (011) 886-2-2826-1002; yjchou@ym.edu.tw and Chung-Pin Li, MD, PhD, Division of Gastroenterology, Department of Medicine, Taipei Veterans
General Hospital, No. 201, Sec. 2, Shih-Pai Road, Taipei 112, Taiwan; Fax: (011) 886-2-2873-9318; cpli@vghtpe.gov.tw
1
Division of Dermatology, Taipei County Hospital, Taipei County, Taiwan; 2Institute of Public Health, National Yang-Ming University, Taipei, Taiwan; 3Department
of Senior Citizen Service Management, Ching-Kuo Institute of Management of Health, Keelung, Taiwan; 4Institute of Hospital and Health Care Administration,
National Yang-Ming University, Taipei, Taiwan; 5Division of Surgery, Taipei County Hospital, Taipei County, Taiwan; 6Division of Gastroenterology, Department of
Medicine, Taipei Veterans General Hospital, Taipei, Taiwan; 7National Yang-Ming University School of Medicine, Taipei, Taiwan
DOI: 10.1002/cncr.25616, Received: May 19, 2010; Revised: July 24, 2010; Accepted: August 3, 2010, Published online September 30, 2010 in Wiley Online
Library (wileyonlinelibrary.com)

618 Cancer February 1, 2011

Those indi. vision. death.000 NHI beneficiaries. representing approximately strophic Illness Patient Database. the NHI program since 1996. apply for a Catastrophic Illness Card in Taiwan. code 585 or A code A350). A total of incidence rates and IRRs. consist of comprehensive utilization and enroll. and chronic based cohort study that included a large number of TB obstructive pulmonary disease (ICD-9-CM code 490- cases to investigate the association between pulmonary 492. 2008. chronic renal failure (ICD-9-CM with a high indoor exposure to coal smoke. A325). and the registry the NHI program.000 person-years). The incidence rate of lung cancer was for drug prescriptions. incidence rate ratios (IRRs). We included diabetes mellitus (ICD-9-CM code heavy smokers. or the end of the year 2008. con- structed and managed by the National Health Research Incidence of Lung Cancer Institute. Histological confirmation is stratified systematic sampling design was used. Pulmonary TB was defined by a compatible ICD. 1997 to December 31. Comprehen. Control Group Subjects with no TB records were used as the control group. because they Comorbidities were defined based on the claims were usually conducted in high-risk populations. We chose all the active was followed up for a minimum of 1 year and a maximum pulmonary TB patients during this period as the study of 12 years. such as data. Lung Cancer After Pulmonary Tuberculosis/Wu et al not be able to yield generalizable results. and the Cancer February 1. Those who were diagnosed with cancer can between the sample group and all enrollees. cohort. A431). This study has been The 2 cohorts were followed up until the development of approved by the National Health Research Institutes. The confiden- tiality of the data abides by the data regulations of the Lung Cancer Risk Analysis Bureau of National Health Insurance. the Catastrophic Illness files.13 A multistage part of the NHI Database. A total of 23. based on ambulatory care year of the index pulmonary TB infection. Because lung cancer developing in the first year of the index pul- monary TB infection is difficult to differentiate from lung Study Population cancer mimicking pulmonary TB. those with lung cancer diag- universal health insurance program. The National Health Insurance (NHI) is a mandatory Similar to the TB patients. were performed by the Kaplan-Meier method. The incidences of lung cancer were compared between viduals who had lung cancer diagnosed before or within pulmonary TB patients and controls by calculating the the first year of TB infection were excluded. Four control subjects were selected to match each MATERIALS AND METHODS TB patient by random sampling stratified for age and sex Data Sources from the database within the same observational period. autoimmune diseases (ICD-9- We therefore conducted a nationwide population. we excluded patients We conducted a retrospective cohort study from January with a diagnosis of lung cancer registered within the first 1. Each subject and inpatient discharge records. calculated as the number of lung cancer patients divided All information that allows a specific individual by the observed person-years. Lung cancer was defined by a compatible ICD-9-CM ment information for a randomly selected sample of code (162) or A code (A101) from the Registry for Cata- 1000. 496 or A code A323. lung cancer. CM code 710. plus the prescriptions of at least 2 Statistical Analysis antituberculosis medications for >28 days.984 subjects served as a to 96% of the residents in Taiwan have been enrolled in comparison group. asbestos-exposed workers. ninth re. Cumulative incidence analyses 5657 pulmonary TB patients were included in this study. patient to be identified has been encrypted. A021). 2011 619 . lung cancer were analyzed. the holders are exempted from cost sharing required under claims data. Up were excluded. 714 or A code A430. TB and subsequent risk of lung cancer as well as the temporal relationship between these 2 diseases. nosed before or within the first year of the observation sive medical care coverage to all Taiwanese residents. offering comprehen. There needed by the NHI to apply for this Catastrophic Illness were no statistically significant differences in sex or age Registry. The NHI sample files. clinical modification) code (010-012. and hazard ratios (HRs) of 9-CM (International Classification of Diseases. or populations 250 or A code A181). Card- sive healthcare data include the enrollment files. 018) or A code (A020. which is a separate sub- 5% of all enrollees in Taiwan in 2000. Incidence rates (per 100.

y (first-third quartiles) 58 (41-72) 58 (42-72) <60 2910 51.4 12.4 1071 4.33-2.6 11. noted for female sex and comorbidity with autoimmune chronic renal failure.76 (95% CI.3 . including diabetes mellitus. Table 2).22. at 2 to 4 years. cohorts were 5. College was significantly higher compared with the 153 per Station. Higher lung controls by age and sex.001 Follow-up years (95% CI) 5.86 and 6. and 1.53).3 <.8%.8 7512 31. chronic renal failure.000 person-years in the control group.22 (6. 12 years of observation. 2011 . 23.86 (5.51 Male 3856 68. 1.744 49 Sex Female 1796 31. and 8 to 12 years.7 5817 24. The incidence rate of lung cancer 1 year after Cox model. TB infection.2 16. The aver- age interval from pulmonary TB infection to diagnosis of RESULTS lung cancer was 3.2 .240 51 .94) 6.5 . differences between the curves were tested with the log. % Median age.18-6.001).75-3. which to link the data. Variables in this compared with the controls.6 4686 19.105 person-years for conditions were taken as time-varying covariates in the the controls. Baseline Characteristics of Pulmonary TB Patients and Age.26) TB indicates tuberculosis.984 No. 3.001.58 ‡60 2747 48.and sex-matched controls were recruited.42 (95% CI.59 (95% CI.472 68. as well as comorbidity with dia- determine whether pulmonary TB is an independent risk betes mellitus and chronic obstructive pulmonary disease. autoimmune diseases.11). matching resulted in comparable distributions of cases and 5 to 7 years.59). On Cox multivariate proportional hazards 620 Cancer February 1. NC) pulmonary TB was 269 per 100.37-2.5 3170 13.32. chronic renal failure. Demographic Data Table 3 showed the temporal relationship of lung Between 1997 and 2008. Other comorbidity demographic cancer incidence was noted in the TB cohort in the entire data.7 Comorbidity Diabetes mellitus 1334 23. 5657 pulmonary TB patients and cancer incidence among pulmonary TB and controls.95 years (95% CI.and Sex-Matched Controls Characteristics TB Patients. autoimmune diseases.83).479 person-years obstructive pulmonary disease. and chronic diseases.1 (SAS Institute. Tex) to perform the statistical analyses. Cary.31-4. sex. . respectively.76-2. Risks of Lung Cancer and chronic obstructive pulmonary disease.Original Article Table 1. Pulmonary TB patients had a Cumulative Incidences and Relative higher prevalence of diabetes mellitus. confidence interval. The individual 0. and Stata 10 (Stata Corporation. Higher IRR trends were also model included age. P < .98 (95% CI. The cumulative incidence of lung cancer in the TB The TB cohort was associated with a higher risk of lung patients was significantly higher than that in the controls cancer compared with the controls (1.000 person-years. rank test. 1. The Cox proportional hazards model was used there were higher risks of lung cancer associated with all to calculate the HRs and 95% confidence interval (CI) to age groups and male sex.001 Chronic renal failure 305 5.3% vs 0. We used SAS 9. % No. The cases of comorbid for the pulmonary TB cases and 125. factor for lung cancer development. are shown in Table 1.78-5. Kaplan-Meier estimates of the cumulative incidences of lung cancer for TB patients and controls are shown in Fig- Incidence Rates of Lung Cancer ure 1. P < (P < . in the TB cohort. P n 5 5657 n 5 23. and chronic obstructive pulmonary disease.0001). The crude IRR was 1. 1. On stratified analysis. 0.984 age. The Compared with the control group. 100. Controls.22 Chronic obstructive pulmonary disease 2753 48. the IRRs of the TB mean years of follow-up for pulmonary TB and control cohort were 1. diabetes mellitus. CI.5 <. respectively. The observation period was 27.005 Autoimmune diseases 708 12.

Controls.000 person-years 269 153 1. 1.04. 95% CI. P < .001 TB indicates tuberculosis. TB infection (HR.225 8-12 years 12 4893 245 37 23. followed by chest x-rays.93-3.001 Median age (first-third quartiles).147 Male 64 1. With the relative low Disease Control mandates that all patients diagnosed with incidence of pulmonary TB. incidence rate ratio. The incidence of notified pulmonary TB ple size to obtain a sufficient statistical power. 1.000 person-year). we need to have a large sam. TB is a notifi- to investigate the associations between lung cancer and able disease in Taiwan by law.59) Observation person-times 27. We identified the TB cases based on their ICD- DISCUSSION 9-CM codes or A codes. 2.90 (1.1 165 0. plus the prescription of at least 2 This is the first nationwide population-based cohort study antituberculosis medications for >28 days. incidence rate ratio.000 previous reports were hospital-based studies with limited person-years according to the report from the Taiwan numbers of observation and possible selection bias.06 0.177 TB indicates tuberculosis.75-3.33-2.31-4.10) . Person-Years IR No.0 170 0. % LC. general population in our study.98) <. which allowed us to observe the < . which is quite close to vious studies.47 (1.75-3.75 (0.95-3.and sex-matched control TB incidence rate of 55 of 100.42 (0. 1.53) . sputum smear and culture.98 (0.09. 95% CI. we used the NHI claims data to the reported TB cases in Centers for Disease Control data.80) <.77 (1.78 (0. Combination treatment for TB is used.11) . which is in accordance with the international standard. IRR (95% CI) P n55657 n523.30-2. 95% CI.62-3.3 41 0. y (95% CI) 3.76 (1.923 155 1.37) <.73 (1.7 1. infection and lung cancer. n 5 191 IRR (95% CI) P No. male sex (HR. y 69 (60-74) 72 (63-76) <60 16 0.001). 1. lung cancer.001 Comorbidity Diabetes mellitus 23 0.981 329 102 61.001). In addition. CI.69-6.4 55 0.24) .374 166 1. LC. IR.1 1.13-2. temporal relationship between active pulmonary TB 1.013 Chronic renal failure 3 0. Risk of Lung Cancer for Pulmonary TB Patients and Controls Characteristics TB Patients. IRR.8 1. Most of the cases during 2002 to 2008 in Taiwan was 58 of 100.1 100 0.32) <.37-2.12-3. % Total 74 1.28.479 125. IR.30.05 14 0. incidence rate (per 100.001 ‡60 58 1. Cancer February 1.2 1.76-2.06. 1. P create a cohort study.98 (1. and comorbidity with chronic obstructive pul.33-2. CI.75) . being 1 year older (HR.32) <. IRR. analysis. incidence rate.76 (1.4 2. P < .15) . 95% CI.59 (0. Table 3.50) 1. Pulmonary TB in Taiwan is diagnosed by clinical monary disease (HR.2 1.05. The Centers for Disease Control.3 191 0.14 We found a pulmonary population-based data with age. No.001 Interval from TB to cancer.005 Sex Female 10 0. Person-Years IR 2-4 years 46 13.2 26 0. The Taiwan Centers for previous pulmonary TB infection.09 3. 1.061 Chronic obstructive pulmonary disease 60 1.002) suspicion. confidence interval.7 1.55 (1. Temporal Association of Lung Cancer Incidences Among Pulmonary TB Patients and Controls Variables TB Patients. and confirmation by were independent risk factors of lung cancer.18-3. 2011 621 . No.105 IR of lung cancer per 100.001 5-7 years 16 8606 186 52 39.809 131 1.984 LC. 1. n 5 74 Controls.001).64.15.000 person-years in the group permits us a better external validation than the pre.95 (3.83) <. confidence interval.14.019 Autoimmune diseases 16 0.3 21 0.03-1. Lung Cancer After Pulmonary Tuberculosis/Wu et al Table 2. P ¼ .24-2. TB be reported.

as occult lung cancer than 60 years and for those older than 60 years. The activation of innate immunity previous pulmonary TB cases compared with controls. After excluding lung cancer that sis.05 Chronic renal failure 1. this would magnify the lung cancer risk dur. for a Catastrophic Illness Card. which reported a positive association between pulmonary TB and subsequent lung cancer.55.05 1.3 Chronic inflammation orchestrates a likely. 95% CI. when reverse causality is not so extended periods. compared with the con- tion is latently infected with TB. it is groups.00-1.09 1.64. occult lung cancer may trols. studies.Original Article Table 4.07 .12 . 1. These results were consistent with many previous vated leukocytes that participate in the inflammatory 622 Cancer February 1. The respiratory symp- infection was excluded to lessen the possibility of reverse toms of TB may persist several months before TB diagno- causality and coexistence.64 1. Cumulative incidences of lung cancer for the pulmo- nary tuberculosis (TB) and control cohorts are shown. and inflammation results in the production of cytokines with the crude IRR of 1.5-7 After adjusting for possible confounders. CI.17.19-21 When there smoked significantly more cigarettes per day (18 vs 11).8%) and the observation that men diagnosis and treatment of both diseases.03-1.001 Diabetes mellitus 1. we used both diagnostic sis also revealed pulmonary TB infection to be a signifi- codes and the Catastrophic Illness Registry. and therefore the TB and The risk of lung cancer subsequent to pulmonary lung cancer data should be valid.22 is occult lung cancer or the coexistence of TB and Smoking is an important risk factor for lung cancer that lung cancer.01 0.06 <. This suggests that pulmonary TB plays an important provoke reactivation of latent TB by weakening the local role in the formation of subsequent lung cancer in all age immunity. and poses significant challenges for the being 9.54 Autoimmune diseases 1.62-3.14 . TB. especially in the younger patients.15 <. P < that can stimulate tumor growth and progression. Multivariate Analysis for Prediction of Lung Cancer Development Variables Cox P Regression Model HR 95% CI TB infection 1. 2011 . and thereafter treatment typically entails 6 to 9 occurred during the first year of pulmonary TB infection.001 Sex (male/female) 2. of 3.95-1.15. 1. respectively.28 <.28.24- confirmation is needed under the NHI program to apply 2.75 Chronic obstructive pulmonary disease 1. Previous studies among males in our study (HR.03 0. with the smoking rate ratio of males/females for decades.94-1. Because almost 1=3 of the popula.76 (95% CI. the and women were reported in a 2004 cross-sectional survey coexistence of TB and lung cancer has been observed in Taiwan. The TB infection may we were still able to detect an increased IRR for lung can.002 HR indicates hazard ratio. the multivariate analy- As for lung cancer diagnosis.11 .23 Acti- . tumor-supporting microenvironment that is indispensa- We observed elevated rates of lung cancer among ble to carcinogenesis. P < . Figure 1. lung The association between pulmonary TB and lung cancer diagnosis before or within the first year of TB cancer has biological plausibility. 2.16 If occult lung cancer really exists. TB was significantly higher both for patients younger Reverse causality is possible. months of multidrug medication. We also observed a higher lung cancer incidence datory 6 to 9 months of TB treatment. have reported an average of 4 to 11 months delay in lung P < . 1.32.001). 95% CI.33-2. more likely to be diagnosed during the intensive and man.04-1. tuberculosis. 1.18 In addition. To focus specifically on incidence in our study.7% vs 4. Differences in the smoking behavior of men cancer diagnosis among TB patients. with IRRs may cause TB infection.001 Age.05 1.001.24-2.5 (45. induce substantial pulmonary inflammation during these cer in the TB cohort. confidence interval. Table 4). the risk of lung cancer after pulmonary TB infection.001).30. Histological cant risk factor for lung cancer (HR.30 1.15. y 1. could account for the sex discrepancy of the lung cancer ing the first year of TB infection.47 and 1.62-3.

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