Increasing Prevalence of Chronic Lung Disease in Veterans of the Wars in Iraq and Afghanistan

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1 MILITARY MEDICINE, 181, 5:476, 2016 Increasing Prevalence of Chronic Lung Disease in Veterans of the Wars in Iraq and Afghanistan Mary Jo Pugh, PhD* ; Carlos A. Jaramillo, MD, PhD* ; Kar-wei Leung, BS ; Paola Faverio, MD ; Nicholas Fleming, MD ; Eric Mortensen, MD ; Megan E. Amuan, MPH ; Chen-Pin Wang, PhD ; Blessen Eapen, MD* ; Marcos Restrepo, MD* ; Michael J. Morris, MD, FACP, FCCP ABSTRACT Research from the wars in Afghanistan and Iraq have focused on traumatic brain injury (TBI) and mental health conditions; however, it is becoming clear that other health concerns, such as respiratory illnesses, warrant further scientific inquiry. Early reports from theater and postdeployment health assessments suggested an association with deployment-related exposures (e.g., sand, burn pits, chemical, etc.) and new-onset respiratory symptoms. We used data from Veterans Affairs medical encounters between fiscal years 2003 and 2011 to identify trends in chronic obstructive pulmonary disease, asthma, and interstitial lung disease in veterans. We used data from Veterans Affairs and Department of Defense sources to identify sociodemographic (age, sex, race), military (e.g., service branch, multiple deployments) and clinical characteristics (TBI, smoking) of individuals with and without chronic lung diseases. Generalized estimating equations found significant increases over time for chronic obstructive pulmonary disease and asthma in both unadjusted and adjusted analyses. Trends for interstitial lung disease were significant only in adjusted analyses. Age, smoking, and TBI were also significantly associated with chronic lung diseases; however, multiple deployments were not associated. Research is needed to identify which characteristics of deployment-related exposures are linked with chronic lung disease. *South Texas Veterans Health Care System, 7400 Merton Minter Boulevard, San Antonio, TX University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, TX Department of Health Science, Clinica Pneumologica, AO San Gerardo, University of Milan Bicocca, Via Pergolesi 22, Monza, Italy. North Texas Veterans Health Care System, 4500 South Lancaster Road, Dallas, TX Edith Nourse Rogers VA Medical Center, 200 Springs Road, Bedford, MA Uniformed Services University, Brooke Army Medical Center, 3551 Roger Brooke Drive, Fort Sam Houston, TX The opinions or assertions contained herein are the private views of the author and are not to be construed as official or as reflecting the views of the Department of the Army or the Department of Defense. doi: /MILMED-D INTRODUCTION Development of respiratory symptoms is an increasing concern among U.S. military personnel deployed in support of combat operations in Iraq and Afghanistan. This concern has been raised based on reports of environmental exposures such as burn pits, and dust and smoke inhalation, which may lead to the development of chronic lung disease in deployed personnel. 1 3 Blast exposures from improvised explosive devices (IEDs) have occurred in higher numbers during these conflicts aretypicallyassociatedwithtraumaticbraininjury(tbi),butare also known to have injurious effects on the pulmonary system because of barotrauma from blast waves. Despite these occupational risks for pulmonary injury and disease in service members deployed to Iraq and Afghanistan, there is a lack of understanding of the extent of respiratory conditions in this population. Recent data from the Millennium Cohort Study suggest that, despite being generally healthy given the requirements for military service, deployers had a higher rate of selfreported respiratory symptoms compared to nondeployers. 2 Furthermore, service members deployed to Iraq and Afghanistan showed an increase in respiratory symptoms compared to the predeployment period. 4 Findings from recent studies examining chronic lung disease in this population of veterans are mixed. Barth et al 5 foundnodifferencebetween those deployed and nondeployed with regards to increased risk of asthma and bronchitis, but deployers were more likely to report sinusitis. Most of the studies, however, are based on self-report questionnaires and did not report physicians examination or medical records. 4,6 A recent report by Szema et al, 7 based on clinical diagnosis, found that deployed Iraq and Afghanistan veterans (IAVs) were more likely to be diagnosed with asthma. However, this was a cross-sectional study at a single Veterans Affairs (VA) hospital. Population-based studies examining medical diagnoses in the IAV population are rare. The purpose of this study was to examine the prevalence of chronic lung diseases such as chronic obstructive pulmonary disease (COPD), asthma, and interstitial lung disease (ILD) among IAVs over time. We also sought to describe the characteristics of those with and without diagnoses of chronic lung disease and to determine if the prevalence of chronic lung disease increased significantly from fiscal year 2003 (FY03) to fiscal year 2011 (FY11) after controlling for characteristics previously/potentially associated with chronic lung disease including demographic characteristics, multiple deployments, TBI diagnosis, and tobacco use. METHODS Sample and Data Sources We conducted a retrospective analysis of health care system data from veterans deployed in support of combat operations in Iraq and Afghanistan, and who received care from the Department of VA between FY03 and FY11 (October 1, MILITARY MEDICINE, Vol. 181, May 2016

2 to September 30, 2011). We obtained all national VA inpatient and outpatient data for these individuals, and linked those data sources for each individual using an encrypted identifier. Inpatient and outpatient data included demographic characteristics and diagnosis codes (International Classification of Diseases, Clinical Modification [ICD-9-CM] codes) for each clinic visit; ancillary and telephone clinic data were excluded from analysis. MEASURES Respiratory Conditions The study team reviewed the ICD-9-CM codes of diseases of the respiratory system and identified chronic lung diseases relevant to IAV to include in these analyses. These conditions were classified as COPD, asthma, and ILD. Table I shows the conditions included in each group and the ICD-9-CM codes to identify individuals with each condition between FY03 and FY11. Demographic Characteristics We obtained demographic characteristics from VA inpatient and outpatient data during the first year of VA care. Because of a skewed age distribution, for the multivariable analyses, age was categorized as 30 years and younger, 31 to 40, 41 to 50, and 51 years and older. We included race/ethnicity in our adjusted models based on findings of variation in prevalence of asthma by race/ethnicity in prior studies. Race/ethnicity was classified as White, African American, Hispanic, Other, and unknown based on veteran self-report. Finally, we identified branch of service (Army, Navy/Coast Guard, Air Force, Marines). TABLE I. Chronic Lung Disease Chronic Obstructive Pulmonary Disease Chronic Lung Disease Categories and Associated ICD-9-CM Codes Specific Diagnosis (ICD-9-CM) Bronchiectasis (494) Chronic Bronchitis (491) Emphysema (492) Chronic Obstructive Pulmonary Disease (496) Asthma Asthma (493) ILD Pneumoconiosis ( ) Postinflammatory Pulmonary Fibrosis (515) Sarcoidosis (517.8, 135) Pulmonary Eosinophilia (518.3) Pulmonary Insufficiency Following Trauma and Surgery (518.5) Pulmonary Interstitial/Infiltrative Disorders (518.89) ICD-9-CM, International Classification of Disease-9th Revision-Clinical Modification. Tobacco Use We identified a proxy for smoking status using several different types of data as per prior studies. 8 First, we used ICD-9-CM codes for tobacco use/nicotine dependence (305.1, V15.82). We also identified individuals who received VA care in a smoking cessation clinic and those who used medications for the treatment of nicotine dependence (Zyban, nicotine replacement, or varenicline). Individuals having one or more indicator were identified as having tobacco use. TBI Classification Exposure to IED blasts has been clearly linked with TBI and is associated with pulmonary injury from barotrauma. 9,10 Therefore, we used TBI diagnosis as a proxy for blast exposure and used the algorithm from the Armed Forces Health Surveillance Center to identify TBI with ICD-9-CM codes (310.2,800,801,803,804,850,851,852,853,854,907.0, 950.1, 950.2, 950.3, , V15.52) diagnosed before FY11. Multiple Deployments Because of concern about increasing risk of environmental exposures during deployments, we identified individuals with two or more deployment based on dates of deployment included in the roster file of IAV derived from the Defense Manpower Data Center. Individuals for whom the first dates of first and last dates of deployment were different were identified as having multiple deployments (yes/no). 11 Analyses We calculated the prevalence of each condition (and the overall category of chronic lung disease) each year, using the number of unique IAV who received VA care that year as the denominator. We then conducted generalized estimating equations (GEE) analysis to determine if the log-odds of having a diagnosis of any of the chronic lung diseases increased from FY03 to FY11, where the random effect is used to account for the correlation among repeated diagnoses over time. Finally, we controlled for demographic characteristics, multiple deployments, tobacco use, and TBI to determine if log-odds of diagnosis increased from 2003 to 2011, controlling for these potentially contributing factors. The Proc Genmod procedure in SAS 9.1 was used for the GEE analyses. A 2-sided p value <0.05 (calculated based on the sandwich estimate of the covariance) was considered statistically significant. RESULTS Between FY03 and FY11, 760,621 IAV received care in the VA. Among those, 4.5% had at least one diagnosis of the respiratory conditions listed in Table I. The descriptive characteristics of the patients with pulmonary condition diagnoses are shown in Table II. Over the entire study period (FY03 FY11), 0.8% were diagnosed with COPD, 3.4% with asthma, and 0.3% with ILD. Examination of demographics using the chi-square test showed that whites were more likely to experience COPD than either African Americans or Hispanics. African Americans were more likely to experience asthma and ILD. With regards to service branch, Marines were less likely to experience COPD, whereas Army veterans were the most likely to experience COPD and ILD. Those with tobacco use were significantly more likely to be diagnosed MILITARY MEDICINE, Vol. 181, May

3 TABLE II. Characteristics of Individuals With and Without Respiratory Conditions Chronic Obstructive Pulmonary Disease (N = 5,998) Asthma (N = 25,592) Interstitial Lung Disease (N = 2,372) No Respiratory (N = 726,659) Age (Mean [SD]) 42.2 (11.1) 34.6 (9.1) 40.0 (10.4) 34.3 (9.5) Sex Female 660 (11.0) 5,370 (20.98) 243 (10.24) 86,027(11.84) Race/Ethnicity White 4,215 (70.3) 14,350 (56.1) 1,363 (57.5) 443,533 (61.0) African American 919 (15.3) 5,560 (21.7) 616 (26.0) 101,865 (14.0) Hispanic 442 (7.4) 3,232 (12.6) 228 (9.6) 80,544 (11.1) Other 155 (2.6) 1,145 (4.5) 60 (2.5) 29,172 (4.0) Unknown 267 (4.5) 1,305 (5.1) 105 (4.4) 71,545 (9.85) Service Branch Marines 374 (6.2) 2,820 (11.0) 174 (7.3) 98,511 (13.6) Army 4,346 (72.5) 16,842 (65.8) 1,661 (70.0) 441,357 (60.7) Air Force 632 (10.5) 2,568 (10.0) 261 (11.0) 91,089 (12.5) Navy/Coast Guard 646 (10.8) 3,362 (13.1) 276 (11.6) 95,702 (13.2) Rank Officer/Warrant Officer 378 (6.30) 1,783 (7.0) 254 (10.7) 66,190 (9.1) Enlisted 5,620 (93.7) 23,809 (93.0) 2,118 (89.3) 660,469 (90.9) Clinical Characteristics Smoking 3,415 (56.9) 6,790 (26.5) 860 (36.3) 152,840 (21.0) Traumatic Brain Injury 974 (16.2) 3,731 (14.6) 373 (15.7) 63,904 (8.8) with COPD, asthma, or ILD compared to those without. Additionally, those with TBI were more likely to be diagnosed with any of the chronic lung diseases (all p <0.01). Figure 1 shows the change in the unadjusted prevalence in chronic lung diseases examined in our study. The prevalence of COPD was 0.31% in 2003 and 0.55% in 2011, whereas the prevalence of asthma was 1.1% in 2003 and 3.1% in Prevalence of the smallest group (ILD) was 0.13% in 2003 and 0.28% in GEE analyses found that these increases (on the log-odds scale) over time were significant in all three categories of chronic lung disease. The average increase in the log-odds per year was 0.06 (95% confidence interval [CI] ) for COPD, 0.07 (95% CI ) for asthma, and 0.03 (95% CI ; p < 0.001) for ILD. Table III shows the results of the GEE analysis examining prevalence over time controlling for demographic/military characteristics, tobacco use, TBI, and multiple deployments. FIGURE 1. Prevalence of chronic lung disease in VA care from 2003 to Even after controlling for these variables the odds of having a diagnosis of COPD was significantly higher in 2011 than in each earlier year in the observation period. Similarly the odds of diagnosis of asthma were significantly higher in 2011 than in other earlier years of the study. For both of these conditions, the odds increased gradually each year. For ILD, the likelihood of diagnosis did not change significantly over the course of the study; the only significant difference was found between 2003 and Table III also shows the relationship of demographic and clinical characteristics to chronic lung diseases in this cohort. Older age was associated with higher prevalence of COPD and ILD. Women were significantly less likely than men to have COPD and more likely to have asthma. African Americans and Hispanics were less likely to be diagnosed with COPD and more likely to be diagnosed with asthma than Whites. African Americans were also more likely to be diagnosed with ILD than Whites. Military characteristics were also associated with chronic lung diseases. Air Force and Marine veterans were less likely to be diagnosed with COPD than Army veterans, and Marines were also less likely to be diagnosed with asthma and ILD than Army veterans.airforceveteransweremorelikelytobediagnosed with asthma than Army veterans. Those with multiple deployments were less likely than individuals with a single deployment to have diagnoses of any of the chronic lung diseases in this study. With regard to clinical conditions, individuals with tobacco use were significantly more likely to have all of the chronic lung disease in this study, with the effect size being greatest for COPD (adjusted odds ratio [AOR] 4.45; 95% CI vs. ILD AOR 1.85; 95% CI and asthma AOR 1.17; 95% CI ). The association of 478 MILITARY MEDICINE, Vol. 181, May 2016

4 TABLE III. Generalized Estimating Equations Analysis of Temporal Trends Controlling for Demographic and Clinical Characteristics Category Chronic Obstructive Pulmonary Disease OR CI Asthma OR CI Interstitial Lung Disease OR CI Year (vs. 2011) ( ) ( ) 0.70 ( ) ( ) 0.44 ( ) 0.80 ( ) ( ) 0.60 ( ) 1.00 ( ) ( ) 0.66 ( ) 0.91 ( ) ( ) 0.72 ( ) 0.91 ( ) ( ) 0.77 ( ) 0.92 ( ) ( ) 0.84 ( ) 0.92 ( ) ( ) 0.93 ( ) 0.90 ( ) Age (vs. Under 30) ( ) 1.14 ( ) 3.11 ( ) ( ) 1.15 ( ) 5.33 ( ) ( ) 1.05 ( ) ( ) Race (vs. White) African American 0.73 ( ) 1.54 ( ) 1.18 ( ) Hispanic 0.56 ( ) 1.23 ( ) 0.91 ( ) Other 0.65 ( ) 1.20 ( ) 0.88 ( ) Unknown 0.60 ( ) 0.74 ( ) 0.44 ( ) Sex Female vs. Male 22.3 ( ) 1.54 ( ) 1.18 ( ) Service (vs. Army) Air Force 0.73 ( ) 1.20 ( ) 0.88 ( ) Marines 0.56 ( ) 0.74 ( ) 0.44 ( ) Navy/Coast Guard 0.91 ( ) 0.96 ( ) 0.92 ( ) Multiple Deployments 0.92 ( ) 0.93 ( ) 0.98 ( ) Other TBI 1.51 ( ) 1.47 ( ) 1.88 ( ) Smoking 4.45 ( ) 1.17 ( ) 1.83 ( ) TBI was also significant across all conditions, with similar effect sizes across COPD, asthma, and ILD. DISCUSSION This longitudinal cohort study identified increasing prevalence of chronic lung disease in IAV between 2003 and Findings were consistent for COPD, asthma, and ILD. The increasing prevalence of COPD and asthma was statistically significant even after controlling for demographic characteristics, tobacco use, and TBI. This data may suggest a link between deployment exposures and increased diagnoses of chronic lung disease in IAV. Our results add to findings of prior studies examining postdeployment respiratory symptoms among active military personnel. A number of studies found increases in postdeployment respiratory symptoms and medical encounters for obstructive pulmonary disease (predominantly asthma and bronchitis) relative to predeployment rates in a population of active duty U.S. military. 12 However, Smith et al 2 found that deployers had a higher rate of newly reported persistent or recurrent cough and shortness of breath than nondeployers (14% vs. 10%) yet similar rates of chronic bronchitis or emphysema as well as asthma. In general, however, findings from studies using rigorous clinical testing (pulmonary function tests, radiographs, screening spirometry, etc.) and diagnosis revealed little difference between active duty personnel who did and did not deploy to Afghanistan/ Iraq. Matthews et al 13 conducted a retrospective chart review of 371 individuals clinically diagnosed with COPD and found similar proportions of deployed and nondeployed individuals. Evaluation of pulmonary function tests indicated no difference in pulmonary function between those who were and were not deployed. Similarly, DelVecchio et al 14 examined medical records of 400 consecutive individuals undergoing a medical evaluation board for asthma and found that about half were deployed and half were not deployed. Evaluation of spirometry revealed no significant differences between deployers and nondeployers. Although our study was not able to compare prevalence of chronic lung diseases in deployers and nondeployers, our study demonstrates that over the course of the wars, the percent of IAV who sought care for chronic respiratory conditions has increased over time. Our study also adds to the literature on rare ILDs thought secondary to deployment exposures as existing studies are limited. 15 These case series studies found rare cases of bronchiolitis among soldiers with inhalational exposures during service in Iraq and Afghanistan, 16 and cases of acute eosinophilic pneumonia a rare disease involving eosinophilic infiltration of the lung. 17,18 Our data indicate that, while rare cases such as these are treated in the VA setting, after controlling for demographic and clinical characteristics, the percent of IAV with ILD remained relatively stable. MILITARY MEDICINE, Vol. 181, May

5 Since much of the recent literature sampled active duty personnel and did not follow individuals for extended time periods, it is logical that data for chronic respiratory disorders are limited. Barth et al 5 examined a population-based sample of Iraq/Afghanistan era veterans using a representative sample of IAV who served between 2001 and 2008 and found no difference between deployers and nondeployers on self-reported asthma and bronchitis, but did not examine change over time. Our study identified similar proportions of individuals with asthma (3.4%) compared to Barth et al 5 (3.3%), which is remarkable given the methodological differences and sample characteristics. Although we found much lower prevalence of chronic bronchitis (included in our COPD group 0.8%) our definition of bronchitis included only chronic bronchitis, a condition much less common in younger individuals. Our finding of higher prevalence of COPD and ILD with increasing age is consistent with the literature, which finds increasing prevalence of COPD with age. For instance, Green et al 19 found that among Canadians in primary care, the prevalence of COPD was 0.3% for those 30 to 39 years of age, 1.4% for those 40 to 49 years of age, and 7.4% for those 50 years and older. Although it is possible that older individuals may be at higher risk for subsequent COPD or ILD after deployment-related exposures, preliminary data reported by Skabeland and Morris 20 suggest that preexisting abnormalities found with spirometry and exposures (e.g., smoking) may account for respiratory symptoms reported postdeployment. Additional research is required to examine these possibilities. Of interest, we also found that African Americans and Hispanics had higher likelihood of being treated for asthma than did whites. This is consistent with the broad literature on asthma risk factors for African Americans, which found higher prevalence of asthma among African Americans than whites in national data sets since ; however, national data do not support a significant difference between whites and Hispanics. The finding of specific genetic susceptibility loci for African Americans and Latinos in a genome-wide metaanalysis provides some insight into this finding. 22 Because there were also different genetic susceptibility loci specific to European Americans, it is not clear, if our finding of increased asthma prevalence is because of genetic, early childhood environmental exposures, military exposures or complex interactions of environment with known genetic susceptibility loci. 22 Consistent with prior literature including studies of IAV there was a significant association between the chronic lung disease examined in this study and our proxy for tobacco use. 5,17 While we assume that individuals with our proxy for tobacco use had smoking exposure, our data did not allow us to determine the extent to which this association is caused by deployment exposure or smoking. Since study of the Millennium Cohort found that deployment to combat theater was associated with smoking more, smoking initiation, and smoking recidivism, either or both likely play a role. 23 Although a comparison of other war cohorts, especially those who received cigarettes in their C-rations, would be compelling, comparable longitudinal data from World War II and Vietnam are not available. Our data also revealed an association between TBI and diagnoses of chronic lung disease. One explanation for this association is that those deployed in forward combat areas may be more likely to be exposed to TBI-inducing incidents such as IEDs. Explosive blasts have caused a significant portion of the combat-related injuries among U.S. service members and blast exposure is associated with injury to multiple organ systems including the respiratory system. 16,24 26 Acute injury to the lungs or blast lung injury (BLI) is primarily attributed to overpressurization from the blast wave, which results in pulmonary damage. 25,26 BLI occurs frequently with blast exposure, may necessitate emergent care, and can be fatal. 25,26 Asystematic review by the Institute of Medicine found that the existing studies of respiratory outcomes after blast exposure were inadequate to determine the long-term consequences of blast exposure on respiratory function. 27 Again, analyses of prior war cohorts would help elucidate the impact of deployment exposures, but data from those cohorts are not available. Those at forward operating areas may also have higher risk of inhalational exposure from burn pits since these may be the only facilities for waste disposal. Open-air waste burning in burn pits has been the main solid-waste management solution in Afghanistan and Iraq from the beginning of the conflicts. 27 However, prolonged exposure to burned materials, including plastic and electronics, may represent a risk for health. Possible effects of exposure to burn pit smoke ranges from eye and respiratory irritation to cardiopulmonary involvement. 27 Therefore, we would hypothesize that the accrual of these types of environmental exposures would increase the risk of respiratory disease. Surprisingly, there was not a significant association between multiple deployments and chronic respiratory disease. Our findings are consistent with those of Abraham and Baird, 12 in which obstructive lung disease was not significantly associated with multiple deployments compared to a single deployment. However, our data did not include information on location or duration of deployments or exposures during deployment. The heterogeneity in multiple deployment conditions could bias the findings toward the null. Our study has several additional limitations. First our data were assessed retrospectively and based on VA clinical data, therefore any care not received in the VA is not included in our analysis, and diagnoses may not be supported by pulmonary function testing. This may bias our results to the null. Furthermore, information on smoking is not comprehensive as it is based on diagnoses for nicotine dependence, etc. In addition, we have no information on deployment exposures (e.g., burn pits, airborne particulates, solid fuel vapors, etc.), number of deployments, total duration of deployment and location of deployment. Further, timing of chronic lung disease onset is not clear since many individuals may have been diagnosed while still on active duty. Finally, we did not have pulmonary function test data available to assess the accuracy of the clinical diagnoses. 480 MILITARY MEDICINE, Vol. 181, May 2016

6 CONCLUSION Our study found a consistent and significant pattern of increasing prevalence of COPD and asthma in IAVs between 2003 and Personal characteristics such as smoking were associated with chronic lung disease. However, variables that may be associated with exposures such as TBI/blast were also significant predictors of chronic lung disease. These epidemiological data may be used in conjunction with clinical studies to develop more comprehensive research that will allow policy makers to better understand deployment-related conditions, and provide clinicians with information that will inform their decisions to conduct screening of individuals with persistent respiratory symptoms. ACKNOWLEDGMENTS Data were obtained with the assistance of the VA Office of Environmental Epidemiology for the Operation Enduring Freedom/Operation Iraqi Freedom Roster file. This study was funded by the VA Health Services Research and Development Service (DHI ). The content of this article is solely the responsibility of the authors and does not necessarily reflect the official views of the Veterans Health Administration or the Department of Defense. The funding organizations had no role in the design and conduct of the study; the collection, management, analysis, and interpretation of the data; or the preparation, review, or approval of the manuscript. This retrospective data study received approval including a waiver of informed consent and Health Insurance Portability and Accountability Act authorization by the institutional review boards of the University of Texas Health Science Center San Antonio and the Edith Nourse Rogers Memorial VA Hospital. REFERENCES 1. Abraham JH, DeBakey SF, Reid L, Zhou J, Baird CP: Does deployment to Iraq and Afghanistan affect respiratory health of US military personnel? 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