ERJ
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Published online before print December 20, 2006, 10.1183/09031936.00134706
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
29/4/745    most recent
09031936.00134706v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Permissions
Right arrowRequest Permissions
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Web of Science (3)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Leung, C. C.
Right arrow Articles by Fu, F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Leung, C. C.
Right arrow Articles by Fu, F.
Eur Respir J 2007; 29:745-750
Copyright ©ERS Journals Ltd 2007

Smoking and tuberculosis among silicotic patients

C. C. Leung1, W. W. Yew2, W. S. Law1, C. M. Tam1, M. Leung1, Y. W. Chung1, K. W. Cheung1, K. W. Chan2 and F. Fu1

1 Tuberculosis and Chest Service, Centre for Health Protection, Department of Health, and 2 Tuberculosis and Chest Unit, Grantham Hospital, Hong Kong, China.

CORRESPONDENCE: C. C. Leung, Pneumoconiosis Clinic, 4/F 8 Chai Wan Road, Shaukeiwan, Hong Kong, China. Fax: 852 29775940. E-mail: cc_leung{at}dh.gov.hk

Keywords: Cohort study, smoking, tuberculosis

Received: October 16, 2006
Accepted December 4, 2006


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
The aim of the present study was to investigate the relationship between smoking and tuberculosis (TB) among high-risk silicotic patients in Hong Kong.

A cohort of 435 silicotic patients tuberculin tested from 1995–2002 was prospectively followed-up until the end of 2005. Baseline characteristics were analysed with respect to positive tuberculin reaction (≥10 mm) at baseline and subsequent development of TB.

Smoking, alcohol use and body mass index were independent predictors of positive tuberculin reaction at baseline in multiple logistic regression analysis. Total cigarette pack-yrs did not demonstrate any significant effect. The annual incidences of TB were 1,841, 2,294 and 4,181 per 100,000 for never-, ex- and current smokers, respectively. On Cox proportional hazard analysis, current smokers have a significantly higher risk of TB than other silicotic patients (adjusted hazard ratio (95% confidence interval (CI)): 1.96 (1.14–3.35)) after controlling for age, alcohol use, tuberculin status, treatment for latent TB infection and other relevant background/disease factors. A significant dose-response relationship was also observed with the daily number of cigarettes currently smoked. Smoking cessation may reduce 32.4% (95% CI: 6.5–54.0) of the risk.

Smoking increases the risk of both tuberculosis infection and subsequent development of the disease among silicotic patients.

In recent years, there has been increasing evidence on the relationship between smoking and tuberculosis (TB). Smoking has been associated with latent TB infection (LTBI) 1–3, active TB disease 4–8 and TB-related death 9–12. However, the underlying mechanisms of such associations remain largely elusive. As both conditions are strongly related to a multitude of socioeconomic factors, increased risk of exposure could explain, fully or in part, all the associations observed 13, 14. The long latent period and relatively low incidence of active disease among immunocompetent subjects renders it rather difficult to dissect the complex relationships.

In Hong Kong, both smoking and TB are common conditions 15. Silicosis is also the second most common statutorily notifiable occupational disease. Silicotic patients are regularly referred to the Pneumoconiosis Medical Board in the Tuberculosis and Chest Service of the Department of Health (Hong Kong, China) for compensation assessment. Confirmed silicotic patients are reassessed every 2 yrs for delineation of additional disability and also at death for contribution of the disease. During compensation assessment, detailed occupational and smoking histories are available. A very high risk of TB has been reported among these silicotic patients 5, 16. Since 1995, tuberculin tests are also regularly offered to newly confirmed cases without previous history of TB. The availability of detailed assessment and tuberculin testing records in the present high-risk cohort allowed examination of the effect of smoking on TB prospectively and in greater detail.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
Study subjects
All silicotic patients without previous history of TB, tuberculin skin testing or treatment for LTBI were offered a Mantoux test with purified protein derivative RT23 (1 unit from August 1, 1995 to June 30, 2000; 2 units from July 1, 2000 to December 31, 2002) as part of the regular service. Due to their existing small numbers, female subjects were excluded from the present study. The study was approved by the ethics committee of the Department of Health of Hong Kong.

Study design
A prospective cohort analysis was performed on the development of TB.

Methods
The following baseline information was collected at the time of tuberculin testing: date of tuberculin testing; name; age; identity card number; ethnicity; smoking history; alcohol use; bacilli Calmette–Guérin (BCG) scar; coexisting medical conditions; occupation; duration of dust exposure; and disease indices according to the International Labour Organisation classification (profusion/size/shape of lung nodules, progressive massive fibrosis). A never-smoker was defined as an individual who had never smoked as many as 1 cigarette·day–1 or equivalent for the duration of 1 yr. An ever-smoker was defined as an individual who had smoked ≥1 cigarette·day–1 for ≥1 yr. An ex-smoker was defined as an ever-smoker who had stopped smoking for ≥1 yr prior to study commencement. A current smoker was defined as an ever-smoker who was still smoking within the previous 1 yr. A regular drinker was defined as an individual who drank alcohol regularly (≥4 days·week–1) at the time of tuberculin testing. The cohort was followed-up prospectively in the Pneumoconiosis Clinic (Hong Kong) or other chest clinics of the Tuberculosis and Chest Service until December 31, 2005. The cohort was also cross-matched with the statutory TB notification registry and death registry of Hong Kong for further case finding and ascertainment of vital status. The period of follow-up was defined as the period from enrolment to the date of notification of TB, death or December 31, 2005, whichever was earlier. Date of TB notification, bacteriological status, form of TB and previous TB history were retrieved from the notification registry. The diagnosis and clinical information of all identified TB cases were verified with the medical records retrieved from the Pneumoconiosis Clinic and other relevant sources. An active case of TB was defined as disease proven by isolation of Mycobacterium tuberculosis or, in the absence of bacteriological confirmation, disease diagnosed on clinical, radiological and/or histological grounds together with an appropriate response to treatment.

Analysis
The effect of background and disease characteristics on LTBI (defined as a tuberculin reaction ≥10 mm) on the baseline was first analysed in a cross-sectional analysis, followed by a prospective analysis with respect to the development of active TB disease and culture-proven TB. For univariate analysis, Chi-squared or Fisher exact tests were used for categorical variables and ANOVA for numerical variables as appropriate. Multiple logistic regression analysis and Cox proportional hazards analysis were then employed in the cross-sectional and prospective analysis, respectively, to control for all the confounding background/disease variables. A two-tailed p-value <0.05 was taken as statistically significant. The risk of TB attributable to smoking was derived by applying the adjusted hazard ratio to the Levin formula 17:

Attributable risk = px(r-1)/[px(r-1)+1] (1)

where p is the proportion of the population exposed and r is the relative risk of disease for the exposed group.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGEMENTS
 REFERENCES
 
A total of 441 silicotic patients were tuberculin tested from August 1, 1995 to December 31, 2002. Six female patients were excluded, leaving 435 male silicotic patients for analysis. All recruited subjects were ethnically Chinese.

Table 1Go summarises the baseline characteristics of all recruited subjects as stratified by tuberculin status. Smoking was significantly associated with a positive tuberculin reaction (≥10 mm). Among the ex-smokers in the cohort, there was no significant difference in the tuberculin-positive rates (66.2 versus 70.5%, p = 0.554) between those 65 patients having given up smoking for ≥10 yrs and the other 105 patients having given up for <10 yrs. Variables associated with a positive tuberculin response (≥10 mm) at a p-value <0.1 were entered into multiple logistic regression and the results are summarised in table 2Go. Only smoking status, alcohol use and body mass index (BMI) remained independent predictors of a positive tuberculin reaction at baseline. Profusion of nodules failed to reach statistical significance. Of the 317 patients with positive tuberculin reaction ≥10 mm, only 101 (31.9%) accepted treatment for LTBI; 61 were administered 6 months of daily isoniazid and 40 were administered 2 months of daily rifampicin and pyrazinamide.


View this table:
[in this window]
[in a new window]

  		Table 1— Background/clinical characteristics of silicotic patients at tuberculin testing

 

View this table:
[in this window]
[in a new window]

  		Table 2— Predictors of positive tuberculin reaction(≥10 mm) in multiple logistic regression analysis

 
The mean duration of follow-up from the day of enrolment to development of TB, death or December 31, 2005 was 1,908±847 days. A total of 78 new TB cases were identified during the period of follow-up, with 75 cases from the regular clinical follow-up and three further cases from the TB notification registry. Two cases were found to have nontuberculous mycobacterial infection and three other bacteriologically negative cases were excluded due to absence of appropriate response after anti-TB treatment. The remaining 73 cases meeting the case definition for active TB were diagnosed at a mean duration of 1,273±874 days from the time of tuberculin testing. In total, 49 (67.1%) of them were confirmed by successful isolation of M. tuberculosis in culture. A total of 63 cases (86.3%) had pulmonary involvement alone, two cases (2.7%) presented extrapulmonary involvement alone and 8 cases (11.0%) had both. None of the 66 TB patients consenting to voluntary HIV testing was found to be HIV-infected. A total of 54 deaths (12.4%) occurred among the cohort, at a mean duration of 1,201±843 days from the time of tuberculin testing. A total of 14 patients died from bronchogenic carcinomas, 11 from other malignancies, 16 from other respiratory diseases or complications, nine from cardiovascular diseases and four from miscellaneous conditions. Nine of the deaths occurred at varying intervals after the development of TB, but none of them died directly as a result of the disease.

The annual incidences of active TB and culture-confirmed TB among different smoking categories are summarised in table 3Go. For ex-smokers, there was no significant difference between individuals who had given up for ≥10 yrs and those who had given up more recently in risk of active TB (2,515 per 100,000 versus 1,927 per 100,000; p = 0.588) and culture-confirmed TB (1,605 per 100,000 versus 1,548 per 100,000; p = 0.949). Current smokers were at a significantly higher risk of both active TB and culture-confirmed TB than those not currently smoking (never- and ex-smokers combined) and the differences persisted after all regular alcohol drinkers were excluded or after stratification by tuberculin status and treatment for LTBI (table 4Go).


View this table:
[in this window]
[in a new window]

  		Table 3— Annual rates of active tuberculosis(TB) and culture-confirmed TB by smoking status among the whole cohort

 

View this table:
[in this window]
[in a new window]

  		Table 4— Relative risks of active tuberculosis(TB) and culture-confirmed TB between current smokers and other silicotic patients

 
The effects of different smoking-related variables on the risk of active TB disease and culture-confirmed TB in Cox proportional hazard analysis are summarised in table 5Go. Current smokers were at an increased risk for development of TB after adjustment by age, alcohol use, tuberculin status, treatment for LTBI and other relevant background/disease factors. Figures 1Go and 2Go demonstrate the higher risks of active TB and culture-confirmed TB with increasing number of cigarettes smoked per day at the baseline, respectively. By applying the Levin formula, smoking at the time of tuberculin testing accounted for 32.4% (95% confidence interval 6.5–54.0) and 36.0% (5.6–60.4) of the risks of active TB and culture-confirmed TB among the cohort, respectively.


View this table:
[in this window]
[in a new window]

  		Table 5— Adjusted hazard ratios(HR) of active tuberculosis (TB) and culture-confirmed TB with respect to smoking-related variables

 

Figure 1
View larger version (8K):
[in this window]
[in a new window]

  		Fig. 1— Risk of active tuberculosis among silicotic patients by number of cigarettes currently smoked per day after adjustment of other confounding variables, as listed in table 5Go. ——: <10 cigarettes·day–1; -----: 10–19 cigarettes·day–1;·······: ≥20 cigarettes·day–1. Overall model: -2log likelihood 770.0, Chi-squared 44.74; p<0.001.

 

Figure 2
View larger version (7K):
[in this window]
[in a new window]

  		Fig. 2— Risk of culture-confirmed tuberculosis among silicotic patients by number of cigarettes currently smoked per day after adjustment of other confounding variables, as listed in table 5Go. ——: <10 cigarettes·day–1; -----: 10–19 cigarettes·day–1; ·······: ≥20 cigarettes·day–1. Overall model: -2log likelihood 520.1, Chi-squared 41.02; p = 0.001.

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGEMENTS
 REFERENCES
 
With the potential ethical concerns in conducting a randomised controlled experiment on human subjects, a prospective cohort analysis is probably the best option to address the relationship between smoking and TB. Even in high incidence areas, the annual rate of TB among immunocompetent individuals is usually just in the order of one in 1,000. Therefore, it is necessary to follow-up a very large cohort to get sufficient cases for analysis, and with this, critical details about potential confounders are often incomplete or missing. The present cohort involved a relatively homogeneous group of male silicotic patients of Chinese ethnicity who were at a very high risk for developing TB (3% per annum, as shown in table 3Go), and for whom detailed smoking history, tuberculin testing results and other clinical information were available under regular two-yearly compensation assessment. Therefore, it offers a relatively unique opportunity to examine the relationships between smoking, LTBI and TB.

In the present study, there was a high prevalence of LTBI as measured by a tuberculin reaction ≥10 mm (table 1Go), similar to what was previously reported among the silicotic patients in Hong Kong 5, 16, 18. Both current and ex-smokers were associated with LTBI (table 1Go) and such association was independent of alcohol intake, BMI and other background variables (table 2Go). Never-smokers, ex-smokers and current smokers were at different risks of TB (table 3Go). Current smoking was consistently associated with higher rates of both active TB and culture-confirmed TB, even after exclusion of regular alcohol use or stratification by tuberculin status/treatment of LTBI (table 4Go) and controlling for all relevant confounding variables (table 5Go). The time elapsed after giving up did not appear to affect the TB risk. A clear dose-response effect was also observed in active TB and culture-confirmed TB with the number of cigarettes smoked per day, again after controlling for all relevant confounders (table 5Go, fig. 1Go). Past cigarette pack-yrs showed only a suggestive but insignificant effect on the development of TB (table 5Go). The independent and dose-response relationship between current smoking and the subsequent development of TB disease is consistent with the authors’ previous observations in another prospective cohort study 8. In contrast with that study, none of the subjects had past history of TB and much more information was available regarding cigarette pack-yrs, time of giving up, tuberculin status and treatment history for LTBI.

With the closer examination allowed in the present study, there is further support of a causal link between smoking and TB. There is an increased vulnerability of developing disease, in addition to an increased risk of acquiring infection. For many years smoking has been associated with changes in pulmonary macrophages 19 and lymphocytes 20. Pulmonary and upper zone predominance of TB lesions in smokers has been reported in a previous study 7. More recent studies suggest that nicotine 21, similar to vagus efferent discharge 22, inhibits the release of tumour necrosis factor, which plays a key role in the cellular defence against TB 23. The overall evidences are therefore in line with a direct airborne insult promoting the risk of disease development.

Tuberculin test was used to measure the LTBI because the specific interferon-release assays were not available locally at the time of the study 24. As BCG vaccination was only introduced into Hong Kong in the 1950s 25 and the vast majority of the present cohort was born well before that time, BCG vaccination is unlikely to affect the interpretation of the test excessively. Indeed, only 3.2% of the present cohort showed a BCG vaccination scar and there was no significant association between a BCG scar and a positive tuberculin reaction.

The present study focused on a homogenous group of ethnically Chinese male patients with silicosis. It would be ideal if it were indeed possible to examine a cohort involving all age groups in the general population. However, tuberculin test data are seldom available among other groups and their relatively low disease incidences pose a genuine difficulty in showing a difference between different smoking categories using active disease as an end-point. Therefore, the current cohort provides a possible window to examine the intricate relationship between smoking, LTBI and active TB. While there might be genuine concern that the findings might not necessarily be transferable to a general population, the higher risk of active TB in current smokers, as observed, is consistent with the findings in a similar study among a larger cohort of elderly subjects within the general community 8.

Incomplete case ascertainment is a major concern for prospective cohort analysis. As the cohort was under regular follow-up for compensation purposes and attempts have also been made to screen for missed cases through the territory-wide TB notification registry, the number of such cases should be low. In any case, incomplete case ascertainment, unless highly selective, is unlikely to significantly affect the internal comparison among different smoking categories. The vital status of patients missing follow-up was also ascertained through cross-matching with the territory-wide death registry. A relatively long period of cessation for 1 yr was employed to distinguish between current and ex-smokers and this would have minimised the short-term fluctuations associated with abortive smoking cessation attempts. The diagnosis of TB could have been complicated by the progression of the underlying silicotic process. As current smokers were more likely to experience symptoms, this might increase the possibility of over-diagnosis of bacteriologically negative TB. However, the association persisted even if only culture-proven cases were considered.

Although alcohol use is a well-known confounder 26, 27, its prevalence was relatively low in the present cohort. Smoking showed independent effect on LTBI and development of TB, even after controlling for the effect of alcohol (tables 2Go, 4Go and 5Go). In the absence of detailed local data on dust exposure levels for various jobs, only job type and duration of exposure were used as proxy measures of dust exposure and disease indices were also taken into account in the analysis. The prevalence of LTBI was not associated with specific job types (table 1Go) and the increased risk of current smokers persisted after adjustment of all relevant background variables and disease indices (table 5Go).

In the present study, one-third of the risk of tuberculosis disease was attributable to current smoking, partly reflecting the high smoking prevalence in the current cohort. Tuberculosis is an important cause of morbidity and mortality among silicotic patients 5 and both smoking and tuberculosis are independently associated with lung function impairment 28. Smoking cessation is, therefore, expected to have major impact on the quality of life for patients suffering from this largely irreversible disease. Ageing of the population is also increasingly observed in developing countries, many of which still have a very high tuberculosis burden. In Hong Kong, ~40% of tuberculosis patients are ≥65 yr of age and males of >80 yrs of age have an eight-fold higher tuberculosis risk than the population average 15. The interaction of smoking with the huge latently infected pool in an ageing population is therefore a serious concern. As endogenous reactivation accounted for >70% of the tuberculosis risk in Hong Kong 29, the use of directly observed treatment, short course alone, is unlikely to be able to bring down the disease incidence rapidly. With the high male and rising female smoking prevalence in many parts of Asia, it would appear rational to include smoking cessation as one of the armaments for tuberculosis control.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
REFERENCES
 
The authors would like to express their sincere thanks to the medical and nursing staff of the Pneumoconiosis Clinic (Hong Kong, China) for assistance in data collection.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 REFERENCES
 

  1. Anderson RH, Sy FS, Thompson S, Addy C. Cigarette smoking and tuberculin skin test conversion among incarcerated adults. Am J Prev Med 1997;13:175–181.[Web of Science][Medline] [Order article via Infotrieve]
  2. Solsona J, Cayla JA, Nadal J, et al. Screening for tuberculosis upon admission to shelters and free-meal services. Eur J Epidemiol 2001;17:123–128.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  3. Plant AJ, Watkins RE, Gushulak B, et al. Predictors of tuberculin reactivity among prospective Vietnamese migrants: the effect of smoking. Epidemiol Infect 2002;128:37–45.[Medline] [Order article via Infotrieve]
  4. Yu GP, Hsieh CC, Peng J. Risk factors associated with the prevalence of pulmonary tuberculosis among sanitary workers in Shanghai. Tubercle 1988;69:105–112.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  5. Chang KC, Leung CC, Tam CM. Tuberculosis risk factors in a silicotic cohort in Hong Kong. Int J Tuberc Lung Dis 2001;5:177–184.[Web of Science][Medline] [Order article via Infotrieve]
  6. Kolappan C, Gopi PG. Tobacco smoking and pulmonary tuberculosis. Thorax 2002;57:964–966.[Abstract/Free Full Text]
  7. Leung CC, Yew WW, Chan CK, et al. Smoking and tuberculosis in Hong Kong. Int J Tuberc Lung Dis 2003;7:980–986.[Web of Science][Medline] [Order article via Infotrieve]
  8. Leung CC, Li T, Lam TH, et al. Smoking and tuberculosis among the elderly in Hong Kong. Am J Respir Crit Care Med 2004;170:1027–1033.[Abstract/Free Full Text]
  9. Doll R, Peto R, Wheatley K, Gray R, Sutherland I. Mortality in relation to smoking: 40 years' observations on male British doctors. BMJ 1994;309:901–911.[Abstract/Free Full Text]
  10. Liu BQ, Peto R, Chen ZM, et al. Emerging tobacco hazards in China: 1. Retrospective proportional mortality study of one million deaths. BMJ 1998;317:1411–1422.[Abstract/Free Full Text]
  11. Lam TH, Ho SY, Hedley AJ, Mak KH, Peto R. Mortality and smoking in Hong Kong: case–control study of all adult deaths in 1998. BMJ 2001;323:361[Abstract/Free Full Text]
  12. Gajalakshmi V, Peto R, Kanaka TS, Jha P. Smoking and mortality from tuberculosis and other diseases in India: retrospective study of 43000 adult male deaths and 35000 controls. Lancet 2003;362:507–515.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  13. Doll R, Hill AB. Lung cancer and other causes of mortality in relation to smoking; a second report on the mortality of British doctors. BMJ 1956;12:1071–1081.
  14. Bothamley GH. Smoking and tuberculosis: a chance or causal association? Thorax 2005;60:527–528.[Free Full Text]
  15. Tuberculosis and Chest Service. Annual report of Tuberculosis and Chest service (2004). Department of Health, Hong Kong, 2006
  16. Hong Kong Chest Service/Tuberculosis Research Centre, Madras/British Medical Research Council. A double-blind placebo-controlled clinical trial of three antituberculosis chemoprophylaxis regimens in patients with silicosis in Hong Kong. Am Rev Respir Dis 1992;145:36–41.[Web of Science][Medline] [Order article via Infotrieve]
  17. Levin ML. The occurrence of cancer in man. Acta Unio Int Contra Cancrum 1953;19:531
  18. Leung CC, Law WS, Chang KC, et al. Initial experience on rifampin and pyrazinamide versus isoniazid in the treatment of latent tuberculosis infection among patients with silicosis in Hong Kong. Chest 2003;124:2112–2118.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  19. Hocking WG, Golde DW. The pulmonary-alveolar macrophage (first of two parts). N Engl J Med 1979;301:580–587.[Web of Science][Medline] [Order article via Infotrieve]
  20. Daniele RP, Dauber JH, Altose MD, Rowlands DT Jr, Gorenberg DJ. Lymphocyte studies in asymptomatic cigarette smokers. A comparison between lung and peripheral blood. Am Rev Respir Dis 1977;116:997–1005.[Web of Science][Medline] [Order article via Infotrieve]
  21. Wang H, Yu M, Ochani M, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003;421:384–388.[CrossRef][Medline] [Order article via Infotrieve]
  22. Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000;405:458–462.[CrossRef][Medline] [Order article via Infotrieve]
  23. Keane J, Gershon S, Wise RP, et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 2001;345:1098–1104.[Abstract/Free Full Text]
  24. Lalvani A, Pathan AA, Durkan H, et al. Enhanced contact tracing and spatial tracking of Mycobacterium tuberculosis infection by enumeration of antigen-specific T cells. Lancet 2001;357:2017–2021.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  25. Tuberculosis and Chest Service. Annual report of Tuberculosis and Chest service (1952). Department of Health, Hong Kong, 1953
  26. Brown KE, Campbell AH. Tobacco, alcohol and tuberculosis. Br J Dis Chest 1961;55:150–158.[CrossRef][Web of Science]
  27. Lewis JG, Chamberlain DA. Alcohol consumption and smoking habits in male patients with pulmonary tuberculosis. Br J Prev Soc Med 1963;17:149–152.[Web of Science][Medline] [Order article via Infotrieve]
  28. Leung CC, Chang KC, Law WS, et al. Determinants of spirometric abnormalities among silicotic patients in Hong Kong. Occup Med (Lond) 2005;55:490–493.[CrossRef][Medline] [Order article via Infotrieve]
  29. Chan-Yeung M, Tam CM, Wong H, et al. Molecular and conventional epidemiology of tuberculosis in Hong Kong: a population-based prospective study. J Clin Microbiol 2003;41:2706–2708.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Am. J. Respir. Crit. Care Med.Home page
H.-H. Lin, M. Ezzati, H.-Y. Chang, and M. Murray
Association between Tobacco Smoking and Active Tuberculosis in Taiwan: Prospective Cohort Study
Am. J. Respir. Crit. Care Med., September 1, 2009; 180(5): 475 - 480.
[Abstract] [Full Text] [PDF]

Home page
 ACCP Pulmonary Med Brd RevHome page
D. W. Kamp
Pneumoconiosis
ACCP Pulmonary Med Brd Rev, January 1, 2009; 25(0): 369 - 390.
[Full Text] [PDF]

Home page
 Am. J. Respir. Crit. Care Med.Home page
C. C. Leung, W. C. Bailey, and W. W. Yew
Screening Contacts of Tuberculosis: Overcoming Obstacles with an Old Tool
Am. J. Respir. Crit. Care Med., May 1, 2008; 177(9): 939 - 940.
[Full Text] [PDF]

Home page
 Am. J. Respir. Crit. Care Med.Home page
K. Aissa, F. Madhi, N. Ronsin, F. Delarocque, A. Lecuyer, B. Decludt, N. Remus, L. Abel, C. Poirier, C. Delacourt, et al.
Evaluation of a Model for Efficient Screening of Tuberculosis Contact Subjects
Am. J. Respir. Crit. Care Med., May 1, 2008; 177(9): 1041 - 1047.
[Abstract] [Full Text] [PDF]

Home page
 Eur Respir JHome page
C. C. Leung, W. C. Yam, W. W. Yew, P. L. Ho, C. M. Tam, W. S. Law, M. Y. Wong, M. Leung, and D. Tsui
Comparison of T-Spot.TB and tuberculin skin test among silicotic patients
Eur. Respir. J., February 1, 2008; 31(2): 266 - 272.
[Abstract] [Full Text] [PDF]

Home page
 Arch Intern MedHome page
C. C. Leung, T. H. Lam, and W. W. Yew
Smoking and Tuberculosis: Infection, Disease, and Mortality
Arch Intern Med, October 8, 2007; 167(18): 2008 - 2009.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
29/4/745    most recent
09031936.00134706v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Permissions
Right arrowRequest Permissions
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Web of Science (3)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Leung, C. C.
Right arrow Articles by Fu, F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Leung, C. C.
Right arrow Articles by Fu, F.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS