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Pulmonary Impairment After Tuberculosis^*

^* From the Department of Medicine (Drs. Pasipanodya, Miller, Vecino, Munguia, and Weis), and the School of Public Health (Dr. Bae), University of North Texas Health Science Center at Fort Worth, Fort Worth, TX; the Tarrant County Health Department (Mr. Drewyer), Fort Worth, TX; and private practice (Dr. Garmon), Weatherford, TX.

Correspondence to: Stephen E. Weis, DO, FCCP, University of North Texas Health Science Center at Fort Worth, 3500 Camp Bowie Blvd, Fort Worth, TX 76107; e-mail: sweis{at}hsc.unt.edu

Abstract

Background: Pulmonary impairment subsequent to a cure of pulmonary tuberculosis has been described only in selected populations.

Methods: We compared pulmonary function in a case-control study of 107 prospectively identified patients with pulmonary tuberculosis who had completed at least 20 weeks of therapy and 210 patients with latent tuberculosis infection (LTBI).

Results: Both groups had similar risk factors for pulmonary impairment. Impairment was present in 59% of tuberculosis subjects and 20% of LTBI control subjects. FVC, FEV₁, FEV₁/FVC ratio, and the midexpiratory phase of forced expiratory flow were significantly lower in the treated pulmonary tuberculosis patients than in the comparison group. Ten patients with a history of pulmonary tuberculosis (9.4%) had less than half of their expected vital capacity vs one patient (0.53%) in the LTBI group. Another 42 patients (39%) with tuberculosis had between 20% and 50% of the expected vital capacity vs 36 patients with LTBI (17%). After adjusting for risk, survivors of tuberculosis were 5.4 times more likely to have abnormal pulmonary function test results than were LTBI patients (p > 0.001; 95% confidence interval, 2.98 to 9.68). Birth in the United States (odds ratio [OR], 2.64; p = 0.003) and age (OR, 1.03; p = 0.005) increased the odds of impairment. Pulmonary impairment was more common in cigarette smokers; however, after adjusting for demographic and other risk factors, the difference did not reach statistical significance (p = 0.074).

Conclusions: These findings indicate that pulmonary impairment after tuberculosis is associated with disability worldwide and support more aggressive case prevention strategies and posttreatment evaluation. For many persons with tuberculosis, a microbiological cure is the beginning not the end of their illness.

Key Words: disability • impairment • pulmonary function • tuberculosis

Tuberculosis is common, with an estimated 8.9 million new cases and 1.6 million deaths worldwide in 2004.¹ It is unknown how many survivors of tuberculosis are living today; however, when the incidence of tuberculosis and the success of therapy are considered, the numbers of living tuberculosis survivors are substantial and increasing.¹

Histopathologic findings resulting from tuberculosis include the formation of caseating granuloma, tissue liquefaction, and cavity formation.² When these occur in the lung, many survivors experience permanent anatomic changes. These result in pulmonary sequelae that are characterized by bronchial and parenchymal structural changes, including bronchovascular distortion, bronchiectasis, emphysematous changes, and fibrotic bands. While these changes remain after a microbiological cure, the further evaluation of persons after tuberculosis is not recommended.³ Current tuberculosis treatment guidelines suggest that performing a chest radiograph at the completion of therapy may be useful but is not essential.³ Additional evaluation for patients after tuberculosis has been cured is currently recommended only for those patients who have suggestions of disease recurrence.³

Studies of pulmonary function in individuals with pulmonary tuberculosis demonstrated variable patterns and severity of impairment.⁴⁵⁶⁷⁸⁹ Pulmonary function studies⁴⁵⁶⁷⁸⁹ can show restrictive, obstructive, or mixed patterns and range from normal to severe impairment. These findings are currently incompletely characterized. The studies performed to date⁴⁵⁶⁷⁸⁹ have been of highly selected populations, as follows: patients receiving only inpatient tuberculosis treatment; patients who have been referred for symptom or preoperative evaluation; patients with an absence of other lung disease; and persons sufficiently well to be currently employed in mining.⁴⁵⁶⁷⁸⁹ These patients do not completely represent the populations affected by tuberculosis. Accurate estimates of the frequency and extent of pulmonary impairment from tuberculosis are important to patients and clinicians as well as to those weighing the potential benefits of the treatment of latent tuberculosis infection (LTBI).

Pulmonary function tests (PFTs) objectively quantify lung function and impairment, and are used to evaluate persons with chronic lung disease.¹⁰ To determine the pattern and extent of pulmonary function abnormalities that are attributable to tuberculosis, we conducted a prospective case-control study using a PFT of patients with culture-confirmed pulmonary tuberculosis and a comparison group with LTBI.

Materials and Methods

A case-control study was conducted at Tarrant County Public Health Department (TCPHD) in Tarrant County, TX. The TCPHD serves approximately 1.5 million residents in north central Texas.¹¹

Eligible case patients were all persons with culture-confirmed pulmonary tuberculosis or pulmonary tuberculosis with extrapulmonary tuberculosis who had completed at least 20 weeks of therapy between July 7, 2005, and November 7, 2006. It is uncertain when lung function stabilizes after tuberculosis, but one serial study⁴ showed no statistically significant change in lung mechanics and attenuation between the onset of therapy and after 5 weeks of therapy; another study⁹ suggested that a peak function loss occurs within 6 months after diagnosis. We therefore assumed, by enrolling persons after 20 weeks of directly observed therapy, that subjects would be microbiologically cured and that such timing would allow data collection to be convenient for a maximal number of subjects.

Comparison subjects were persons who were at least 18 years of age who had LTBI. Comparison subjects were prospectively selected by requesting participation from every fifth person presenting to the clinic for the evaluation of LTBI. All persons with HIV-LTBI coinfection who had been referred to the TCPHD were eligible for inclusion in the comparison group.

By state statute, all tuberculosis-positive cultures are reported to the local health authority; by state policy, all persons with tuberculosis are treated with directly observed therapy.¹²¹³ In Tarrant County, all patients with confirmed tuberculosis are treated by the TCPHD. LTBI is not a reportable condition in Texas; however, the TCPHD offers the evaluation and treatment of persons with LTBI.¹⁴

Study evaluations were incorporated into clinical care visits. Evaluations included PFTs and the completion of a standardized questionnaire of demographic and occupational information, and smoking, medical, and other histories. Occupational information was used to ascertain pulmonary risk, which was defined by us as exposure to particulates or asbestos for > 2 years. Other studies¹⁵¹⁶ have defined the term high-risk occupation as exposure to asbestos for at least 5 years, or exposure to dust for at least 6 years. The evaluation of comparison subjects was performed during their initial clinic visit. Patients with pulmonary tuberculosis were evaluated after at least 20 weeks of treatment. PFTs were conducted according to the American Thoracic Society recommendations¹⁵¹⁶ for subject maneuver, techniques, and quality control using a device (Spirotouch Spirometry System 086578; Spacelabs Burdick; Deerfield, WI) that was calibrated daily before use. PFTs were performed by trained technicians in the patient’s preferred posture with the support of a translator when needed. Three tests with values within 5% were defined as being acceptable, and the best of three values was used for comparisons. When the variation was > 5%, the best three results from eight tests were selected. The FVC maneuver was performed without a nose clip. FEV₁, FVC, FEV₁/FVC ratio and their respective percent predicted values were outcomes. Persons with a history of intermittent bronchodilator use received albuterol nebulization 30 min prior to testing.

FVC, FEV1, and FEV₁/FVC ratio values for case patients were compared with gender-specific and race-specific adult predicted normative population values and the control group.¹⁰ Airway obstruction was defined as an FEV₁/FVC ratio of < 70% and an FVC of > 80% predicted, restrictive defects as an FEV₁/FVC ratio of > 70% with an FVC of < 80% predicted, and combined defects were FVC of < 80% predicted and an FEV₁/FVC ratio of < 70%.¹⁷ Interpretive algorithms were used in determining restrictive or obstructive patterns.¹⁷¹⁸

Data were double entered using a computer spreadsheet program (Microsoft Office 2003 ACCESS; Microsoft Corporation; Redmond, WA). Discrepancies were queried and corrected. Data analysis was performed using a statistical software package (SPSS, version 12 for Windows; SPSS Inc; Chicago, IL). Significant differences between groups were determined with the Student t test and the ² test. Logistic regressions were used to identify predictors for outcomes after controlling for patient variables. The Institutional Review Board of the University of North Texas Health Science Center at Fort Worth approved the study, and written informed consent was obtained from all participants.

Results

Between July 7, 2005, and November 7, 2006, 121 persons who were potentially eligible for the case cohort were reported to the TCPHD. Of these, 14 patients did not meet the study eligibility criteria; all eligible case patients consented to participate (Fig 1 ). Ninety-two of the remaining 107 subjects (86%) had pulmonary tuberculosis and 15 subjects (14%) had pulmonary tuberculosis plus extrapulmonary tuberculosis. Patients with pulmonary and pulmonary plus extrapulmonary disease were considered to be a single group. Two hundred eighteen LTBI patients were selected as control subjects, and 210 of them agreed to participate in the study. All persons with known HIV infection who had been referred to the TCPHD with LTBI agreed to participate. The mean values for FVC, FEV₁, and the midexpiratory phase of forced expiratory flow (FEF_25–75) for patients with a history of pulmonary tuberculosis, for comparison subjects with LTBI, and the predicted values for the general population are shown in Figure 2 .

View larger version (11K): [in this window] [in a new window] [Download PPT slide]   Figure 1.. Study enrollment. TB = tuberculosis; PTB = pulmonary tuberculosis; EPTB = extrapulmonary tuberculosis.

View larger version (4K): [in this window] [in a new window] [Download PPT slide]   Figure 2.. Interquartile ranges for FVC (left, A), FEV1 (middle, B), and FEF25–75 (right, C) for patients with pulmonary tuberculosis (PTB) and LTBI, and for the expected healthy population.

Ninety-nine percent of subjects (316 of 317 subjects) had reproducible spirometry results, and 100% of subjects (317 of 317 subjects) had acceptable spirometry results. Values for FVC, FEV₁, FEV₁/FVC, and FEF_25–75 were significantly lower in patients who had been treated for pulmonary tuberculosis than in the comparison group (Table 1). After adjusting for age, BMI, country of birth, gender, and smoking, survivors of pulmonary tuberculosis were 5.4 times more likely to have abnormal PFT results than patients with LTBI (95% confidence interval [CI], 2.98 to 9.68) [Table 4 ]. Except for a history of pulmonary tuberculosis, only birth in the United States and age significantly increased the odds of pulmonary impairment (odds ratio [OR], 2.64 [p = 0.003] vs 1.03, respectively; p = 0.005) [Table 4].

Fifty-seven percent of case patients and 51% of subjects in the comparison group had a history of ever smoking (Table 1). Smoking volume was significantly higher in the case group (12.01 vs 7.24 pack-years in the comparison group; p = 0.011) [Table 1]. Smoking volume (in pack-years) had a significant correlation with the decline in lung function, and FEV₁/FVC ratio was significantly lower in smokers than in nonsmokers (mean, 79% vs 84% predicted, respectively; p < 0.001 [data not shown]). Even though pulmonary impairment was more common in cigarette smokers, it was not statistically significant (p = 0.074) after adjusting for demographics and other risk factors (Tables 3, 4).

Discussion

Over half of all recently treated pulmonary tuberculosis patients in Tarrant County had significantly impaired pulmonary function (Tables 1, 2). Patients receiving directly observed treatment for tuberculosis were more than five times more likely than LTBI patients to have pulmonary impairment (OR, 5.37; 95% CI, 2.98 to 9.68). The degree of impairment was variable, ranging from mild to severe, and was not uniformly distributed among patient groups; subjects born in the United States and older subjects were more likely to have impairment than were younger or foreign-born subjects (Table 4). Pulmonary restriction and obstruction with low vital capacity were the predominant patterns observed. This study is the first in which data have been collected from a nonselected population and then controlled for background risk that was not related to tuberculosis. These data suggest that pulmonary impairment after tuberculosis is an important, mostly unrecognized, cause of chronic lung disease worldwide.

Our findings differ from those of earlier studies, which have occurred within highly selected populations. In a study⁶ of impairment performed prior to the adoption of short-course therapy, 60% of hospitalized tuberculosis patients had an FEV₁ of < 80% predicted. Fifteen percent of patients had a severe reduction in FEV₁ (< 50% predicted).⁶ The authors found evenly distributed patterns of dysfunction among impaired patients, as follows: restrictive dysfunction, 24%; obstructive dysfunction, 23%; and mixed dysfunction, 19%.⁶ Studies of patients who have been treated with short-course regimens found variable levels of impairment.⁴⁷⁹¹⁹ Two studies from South Africa showed abnormal lung function after the completion of antituberculosis therapy. One of these studies,⁹ which was limited to hospitalized patients, found that 53% had pulmonary function abnormalities. The second study⁹ evaluated current miners with a history of tuberculosis who had been identified through screening up to 31 years prior to their evaluation. The investigators found that the proportion of impaired subjects increased with episodes of tuberculosis; impairment was identified in 18%, 27%, and 35% of subjects, respectively, after one, two, or three episodes.⁹ A study from Canada⁴ found that 36% of patients with pulmonary tuberculosis had abnormal pulmonary function. This study employed stringent entry criteria and enrolled 25 of 84 subjects over 17 months.⁴ Of the 15 patients with cavitary disease, progressive obstruction developed in 1 patient with a final FEV₁ of 0.73 L; 7 of 11 patients (64%) had bronchiectasis.⁴ These studies each demonstrated pulmonary impairment after tuberculosisis, but none measured the full spectrum of impairment, and subjects were drawn from selected populations not controlled for pulmonary risks extant in populations of subjects who were predisposed to tuberculosis.

Previous studies⁴⁵⁶⁷⁸⁹ of pulmonary impairment resulting from tuberculosis all used adult normative population pulmonary function values for comparison. Normative pulmonary function data may not be representative of the population of persons in whom tuberculosis is destined to develop and is not an ideal comparator (Fig 2). LTBI and tuberculosis are not distributed homogeneously throughout society. Both are more likely to occur in persons with unstable housing, foreign birth, low socioeconomic status, HIV coinfection, substance abuse, and other risk factors.²⁰ There are no data on the effects of LTBI on lung function. In this study, the control group of persons in whom LTBI was diagnosed was chosen to identify the contribution to pulmonary impairment from pulmonary tuberculosis independent of these factors. To avoid case-selection bias, the study population was derived from a geographic area rather than from select groups that may not fully represent the population with tuberculosis.⁴⁵⁶⁷⁸⁹ We believe that these methodologies give the most representative estimate currently available for pulmonary impairment due to pulmonary tuberculosis.

Symptoms of pulmonary impairment generally do not occur in persons with chronic lung disease until FEV₁ has fallen to 50% of normal values.²¹ Symptom screens alone are unlikely to detect pulmonary impairment after tuberculosisis. The routine identification of persons with pulmonary impairment after tuberculosisis will require the revision of recommendations for performing PFTs for tuberculosis patients.²² Patients with pulmonary impairment after tuberculosisis may benefit from the methods used to ameliorate other respiratory illness, such as immunizations against respiratory illness and advice on preventing further impairment. Moderate-to-severe lung disease has also been associated with increased mortality.²³ Persons with impairment from chronic obstructive lung disease similar to that associated with lung disease after tuberculosis benefit from pulmonary rehabilitation.²⁴²⁵ The improved exercise capacity and quality of life, and reduced use of medical resources associated with rehabilitation may warrant rehabilitation in select patients after treatment for pulmonary tuberculosis.²⁴²⁵ The identification of impairment after tuberculosisis may therefore be an important strategy to limit tuberculosis morbidity and its attendant costs.

A relationship between tobacco smoking and pulmonary tuberculosis is suspected, but has not been well defined.²⁶ Tobacco smoking serves as a marker of risk for pulmonary tuberculosis; many physical and social factors associated with cigarette smoking are shared with tuberculosis.²⁶ Tobacco smoking causes pulmonary impairment, and smoking would be expected to increase the risk of pulmonary impairment from tuberculosis.²⁷ FEV₁/FVC ratio was significantly lower in smokers than in nonsmokers (mean FEV₁/FVC ratio difference, 79% vs 84% predicted, respectively; p < 0.001 [data not shown]). A larger sample size would allow a more powerful analysis of the interaction between smoking and tuberculosis and its effect on pulmonary function. However, we did not find that persons with a history of smoking had an increased risk of pulmonary impairment when pulmonary tuberculosis developed, and 7 of 11 subjects (64%) with < 50% of expected FVC had no history of tobacco use (data not shown).

This study has limitations. The design did not allow the determination of causality, as the sequence of exposure to the outcome cannot be proved. Our population had other risks for chronic lung impairment. Nearly half of the study participants were current smokers, and lifetime smoking histories of 7.24 and 12.01 pack-years, respectively, were reported in comparison subjects and case patients. Chronic exposure to smoke from cooking fires or other sources is another contributing risk for both tuberculosis and other lung disease in immigrant participants.^28293031 A history of such biomass smoke exposure may be an important risk factor for pulmonary tuberculosis and abnormal pulmonary function following its microbiological cure, but we found that subjects born in the United States who are unlikely to have biomass smoke exposure were more likely to have pulmonary impairment than were foreign-born subjects. We estimated the odds of impairment with and without pulmonary tuberculosis using a comparison group with similar pulmonary and other risk factors from a single geographic area. Our data reflect the epidemiologic mix of Tarrant County, which may be different from other areas. Spirometry using FVC and FEV₁/FVC ratio values has a very low positive predictive value but a high negative predictive value for restrictive pulmonary dysfunction. Although spirometry can exclude 97% of those persons without a restrictive pattern, a more positive prediction of restriction can be obtained from total lung capacity.³² All case patients and control subjects were not given bronchodilators, and it is possible that bronchospasm may not be equally distributed between the case and control groups. The natural history of pulmonary impairment after tuberculosis is unknown, and it is possible that the impairment identified may worsen or improve. Finally, we used prediction equations for the interpretation of the PFT results that included adjustments for race but did not include the full range of races in our population.⁷ Despite these limitations, pulmonary tuberculosis remains the most likely etiology for the identified pulmonary impairment.

Pulmonary tuberculosis is associated with frequent pulmonary damage despite microbiological cure. Impairment is variable, ranging from none to severe. Pulmonary impairment contributes important, previously unmeasured burdens of tuberculosis in microbiologically cured patients that may include chronic impairment and excess mortality.^33343536 PFTs and other measures may need consideration after a cure. When earlier data are considered with our findings, it is apparent that a microbiological cure is not protective against substantial pulmonary sequelae of pulmonary tuberculosis. These findings support the aggressive treatment of LTBI or other case preventing strategies worldwide, and indicate that, for many persons with tuberculosis, microbiological cure is the beginning, not the end, of their illness.

Acknowledgements

This study could not have been completed without the TCPHD supplying study resources. We are indebted to the study participants whose participation made this study possible, and to Francesca Sanchez, MD, who provided a critical review. We also are indebted to the Tuberculosis Epidemiologic Studies Consortium (TBESC) at the Centers for Disease Control and Prevention and to the Tuberculosis Trials Consortium (TBTC), which provided salary support for Drs. Bae, Pasipanodya, Munguia, Vecino, Weis, Miller, and Ms. Drewyer, although neither consortium directly funded this study, nor had any role in study design, data collection, data analysis, data interpretation, or writing of the report.

Footnotes

Abbreviations: BMI = body mass index; CI = confidence interval; FEF_25–75 = midexpiratory phase of forced expiratory flow; LTBI = latent tuberculosis infection; OR = odds ratio; PFT = pulmonary function test; TCPHD = Tarrant County Public Health Department

This work was performed at the University of North Texas Health Science Center at Fort Worth, and was made possible by the cooperation of both the Centers for Disease Control and Prevention’s Tuberculosis Epidemiologic Studies Consortium and the Tuberculosis Trials Consortium (which provided salary support for Drs. Bae, Pasipanodya, Munguia, Vecino, Weis, Miller, and Ms. Drewyer), as well as the Tarrant County Public Health Department and the University of North Texas Health Science Center at Fort Worth. The study did not receive direct funding from these or other sources, however. The authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Received for publication December 7, 2006. Accepted for publication February 12, 2007.

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This Article Abstract Full Text (PDF) Free All Versions of this Article: chest.06-2949v1 131/6/1817    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Article Archive Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (2) Citing Articles via Google Scholar Google Scholar Articles by Pasipanodya, J. G. Articles by Weis, S. E. Search for Related Content PubMed PubMed Citation Articles by Pasipanodya, J. G. Articles by Weis, S. E.