Szema, Anthony M. MD, FCCP; Salihi, Walid DO; Savary, Khalil AB; Chen, John J. PhD
* Outline previous findings on asthma and lung function abnormalities among soldiers returning from Iraq and Afghanistan.
* Summarize the new data on respiratory symptoms and spirometric variables in troops deployed to Iraq/Afghanistan, compared to those posted elsewhere.
* Review the hazardous exposures possibly associated with lung injury in soldiers serving in Iraq or Afghanistan, and the authors' recommendations for mitigating those hazards.
We earlier reported that among 6233 Long Island–based active-duty soldiers from 2004 to 2007, those returning from Iraq and Afghanistan were being diagnosed with new-onset asthma by Veterans Affairs (VA) physicians with higher frequency than stateside-based troops (6.6% of 920 vs 4.3% of 5313, respectively, P < 0.05). Despite taking asthma medications, mean forced expired volume in 1 second (FEV1)/forced vital capacity (FVC ratios were 74 ± 5% and similar to that of the National Health and Nutrition Examination Survey asthma population but lower than values for healthy subjects.1 Only 7 of the 45 patients with available VA spirometry had reversibility of airway obstruction with an additional β-2 receptor agonist superimposed on current asthma medications. Air pollution indices (PM10 or 10 μm–sized particles per cubic meter of air measured in 24 hours) in the Balad, Iraq, region where all soldiers passed during this time frame, were markedly elevated in the thousands. Threshold levels for PM10 in the United States have historically been around 150. These findings suggest that the clinical syndrome tends to lead to fixed airway obstruction as a result of lung injury. We have utilized the moniker “Iraq/Afghanistan war lung injury” (IAW-LI) to encompass pulmonary complaints related to exposures in this geographic region during the time frame of the ongoing wars.2,3 Other authors have noted that not only those suffering from asthma but also those not suffering from asthma had increased respiratory symptoms—wheezing, cough, sputum production, chest pain/tightness, and allergy symptoms—during deployment compared with predeployment.4
Etiologic mechanisms for new-onset IAW-LI may be manifold: (1) Dust from these regions is toxic (Lyles M, International Seminar on Nuclear War and Planetary Emergencies 42nd session Erice, Italy, August 2009); (2) “burn pits,” which entail burning trash ignited by jet fuel, cause inhalational lung injury3; (3) aeroallergens predispose to sensitization to plants, molds, and, in certain cases, dust mite antigens3,5,6; and (4) improvised explosive devices cause blast overpressure or shock waves to the lung, leading to lung injury.7
Endogenous dust grains may be physically coarse and sharp and porous. This porosity lends itself to contain silicates of metals such as aluminum, zinc, copper, nickel, iron, and lead. The dust also contains fungi and bacteria, which, with the metals, can get into soldiers' eyes, food, and skin. In hot temperatures and dry humidity, most people breathe through their mouth.8,9 The protectants of the nose, such as nasal hairs, are bypassed and the particles have a direct entry into the lung and mouth. These metals and viruses may potentially have an effect not just on the respiratory system, but on the nervous system as well (Lyles M, International Seminar on Nuclear War and Planetary Emergencies 42nd session Erice, Italy, August 2009).
Burn pits are trash piles in the absence of incinerators, where the military throws waste such as plastics10; other garbage; and even medical waste, such as body parts.11 The materials are soaked in jet fuel and ignited. The burned fuel and garbage release toxins that nearby soldiers breathe. Any burning can also lead to generation of particulate matter such as PM10, which is associated with respiratory illness.2
Aeroallergens are a concern because serum IgE levels are higher in those suffering from asthma in Tikrit, Iraq, compared with healthy citizens (554 vs 69, respectively) reported in the Journal of Asthma in 2008.5 Also, 61% of asthmatics in Iraq reportedly have allergic rhinitis compared with only 6% of control Iraqis.12 Our group reported that 9.9% of Iraq-deployed veterans compared with 5.1% of stateside ones were diagnosed with rhinitis at the Veterans Affairs Medical Center, Northport, New York (Szema et al, American Academy of Allergy, Asthma, and Immunology Annual Meeting, Philadelphia, 2008). The US Army has reported multiple cases of allergic contact dermatitis with the TRUE test, which does favor the atopic state.13 The successful use of subcutaneous allergen immunotherapy indicates that patients do get sensitized in an IgE-mediated fashion to allergens and that they may benefit from immunotherapy, which skews from a Th2-proallergic to Th1-nonallergic cytokine profile and increases immune tolerant regulatory T cells.14
Blast overpressure is the result of shock waves to the lung from the sheer force of exploding bombs, called improvised explosive devices. Not only do these explosions cause traumatic brain injury (TBI) and possible posttraumatic distress syndrome, but the physics of explosions on the delicate alveolar air sacs leads to lung injury—necessitating low tidal volume, low pressure mechanical ventilation to prevent barotraumas.15,16
The confluence of sharp, toxic dust, burn pit inhalation, aeroallergen exposure in the susceptible patient, and blast overpressure can lead to IAW-LI.
Our clinical data now show that this is a common problem associated with morbidity, which is not transient. The significance of this problem is that it is likely even underdiagnosed in light of (1) absence of routine spirometry for recently returned soldiers (only symptomatic soldiers get spirometry) and (2) Dr Robert Miller's findings from Vanderbilt University showing bronchiolitis and vascular remodeling even among seemingly healthy soldiers with normal physical examinations, chest radiographs, spirometry, and chest computed tomographic scans.17 Sick troops cannot maximize human performance on the battlefield and cannot return to society in a productive manner. Further studies have potential to guide policy regarding exposure to hazards in Iraq and Afghanistan and subsequent medical consequences.
We hypothesized that US military personnel returning home from a tour of duty in Iraq and Afghanistan will have higher rates of respiratory symptoms leading to spirometry when compared with soldiers who did not serve in these regions.
This study was approved by the Northport VAMC Research & Development Committee. We retrospectively analyzed anonymous age- and gender-matched data from the Northport VAMC and compared Iraq/Afghanistan war veterans to veterans deployed stateside. We retrospectively reviewed Northport VAMC data from all soldiers deployed and discharged from military service during March 1, 2004, to December 1, 2010. Data included age, gender, smoking history, deployment location, discharge date, whether they received spirometry, branch of service, diagnoses of TBI, and posttraumatic stress disorder (PTSD). We studied soldiers who attended the VA Operation Enduring Freedom (OEF) clinic, which comprises soldiers who have served in Iraq/Afghanistan, and the Operation Iraqi Freedom (OIF) clinic, comprising Iraq war veterans. In comparison to our prior study, the computer database was now able to separate OEF versus OIF patients versus neither. In 2004, there were 17,900 US troops in Afghanistan; there were 130,000 forces in Iraq.
Diagnoses and Measurements
All patients were examined by VAMC physicians. All primary care internal medicine staff are licensed teaching faculty at SUNY Stony Brook School of Medicine. Patients who enroll at the VAMC Northport do not get routine screening spirometry since it is not institution policy and human resource capacity to conduct tests on all troops is limited. All asthma International Classification of Disease codes are recorded. The clinical guidelines at the VAMC clinic for a diagnosis of asthma include recurrent episodes of respiratory symptoms (cough, wheeze, dyspnea, exercise-induced shortness of breath) with spirometric evidence of airway obstruction based on the FEV1/FVC or FEF25-75 at rest, with improvement of symptoms after bronchodilators. Patients who get spirometry must have symptoms and a diagnosis entered into the computerized request form by the requesting physician. The Northport VA Information Resource Management Department was able to cull a list extracted onto an excel spreadsheet of active-duty soldiers from 2004 to 2010 registered and seen in Northport. Associated variables included name, age, gender, dates and locations of deployment, smoking status, branch of service, diagnosis of PTSD or TBI, and whether they received spirometry.
Individuals were classified according to deployment status (deployed to Iraq or Afghanistan vs stationed elsewhere). The standard deployment time frame to Iraq is 1 year. Categorical variables were summarized by frequencies and percentages. These included whether the veteran had visited OIF/OEF clinics (yes/no), gender (male/female), and whether they received spirometry (yes/no). Age of the veteran was grouped into the following five categories: 18 to 25 years, 26 to 30 years, 31 to 35 years, 36 to 40 years, and 41 years or more. Contingency tables for categorical values were generated and associations were evaluated using Fisher exact test.
Demographic and clinical characteristics of veterans were compared using two-sample t tests for continuous variables and Fisher exact tests for categorical variables, first between those with versus without deployment in Iraq/Afghanistan, then between those with versus without a spirometry. The subgroups of veterans who had a spirometry were then compared between those with versus without deployment in Iraq/Afghanistan. Two-tailed P value of less than 0.05 was regarded as statistically significant.
In Table 1, mean age of stateside and Iraq/Afghanistan troops was 33.85 years and 35.38 years, respectively. There were more smokers in the Iraq/Afghanistan deployed group (16.1% vs 3.3%) and provider diagnoses of new-onset asthma were six times higher (6.2% vs 0.7%). Symptomatic soldiers requiring spirometry were more frequent in the Iraq/Afghanistan group compared with the elsewhere group, with rates of 14.5% and 1.8%, respectively. Twice as many women were in the elsewhere group, 17.2%, compared with 8.7%. TBI rates and PTSD diagnoses were also more frequent among Iraq/Afghanistan deployed forces, though it appears that the elsewhere group nonetheless had measurable, though lower, rates (Iraq/Afghanistan, 27.5%, vs elsewhere, 4.1%, for TBI; and Iraq/Afghanistan, 33.6%, vs elsewhere, 3.7%, for PTSD).
Table 2 shows that 34.9% of those who received spirometry were smokers, whereas only 5.1% of those who did not get spirometry were smokers. Seventy-two percent of those who received spirometry (and clinical symptoms warranting a diagnosis) were deployed to Iraq/Afghanistan. The percentages of women who either did or did not get spirometry was the same (14 vs 15.2%, P = 0.16). Although only 5.7% of those who did not get spirometry had a diagnosis of TBI, among those who did get spirometry, 92.5% were diagnosed with TBI. Rates of PTSD were lower but still comprised 42.4% of those who had respiratory symptoms/spirometry, while 9.6% of those without spirometry had PTSD.
Table 3 indicates that soldiers were matched for age, height, and weight. Although mean FEV1 and FVC rates were higher for Iraq/Afghanistan veterans—FEV1/FVC = 3.43/4.44 elsewhere and FEV1/FVC = 3.68/4.73 for Iraq/Afghanistan—mean FEV1/FVC ratios were statistically similar (77.53% and 77.97% for elsewhere and Iraq/Afghanistan, respectively).
SIGNIFICANCE OF STUDY
This study provides the first indication that the scope of respiratory symptoms among US military personnel deployed to Iraq and Afghanistan from 2004 to 2010 is widespread. Soldiers deployed to Iraq and Afghanistan were more often symptomatic and received spirometry more than soldiers stationed elsewhere. At issue is whether this is a form of lung injury rather than classic extrinsic IgE versus intrinsic non-IgE asthma. Lung injury and bronchiolitis are plausible because infections, irritants, and toxin exposure may be occurring on the battlefield.
Air pollution (PM10) may explain these findings. A prospective study utilizing more sensitive objective measures pre- and postdeployment, with a control group (nondeployed), will help illuminate possible ramifications of current environmental air exposure in Iraq.
Uncontrolled burning of trash in Balad burn pits without use of incinerators prior to November 2009 is concerning because plastic water bottles doused in jet fuel were lit on fire. Products of combustion from polyethylene terphthalate plastic water bottles leads to release of phthalates, a source of occupational asthma. Furthermore, carcinogens benzene and formaldehyde and aliphatic hydrocarbons are emitted as byproducts of combustion.3,18
Suggested prevention and control measures include cessation of uncontrolled burning of garbage, installation of incinerators, recycling plastic, and use of respiratory protection devices. Surveillance may be accomplished by obtaining spirometry and 2-mile run times for soldiers pre- and postdeployment, with documentation of their duty station location. Personal PM2.5 monitors may better quantify exposure risk.19 The practice of using jet fuel (JP-8) as an accelerant to burn trash is not recommended, since burned jet fuel releases benzene and n-hexane, a neurotoxin, when burned.
Limitations of this study entail the absence of a denominator since we believe that all returning soldiers from Iraq/Afghanistan should receive screening spirometry. We also lack predeployment spirometry. Indeed, the literature suggests that being in the military is a risk factor for asthma, so that even the stateside-based soldiers, who theoretically come from a select, young, healthy fit-for-duty group, are at risk for asthma. Therefore, we advocate that both elsewhere and Iraq/Afghanistan-deployed troops should have pre- and postdeployment spirometry and 2-mile run times. Previously healthy soldiers may have been 100% or greater predicted in terms of exercise capacity, so that returning with 85% predicted capacity may actually suggest disease. More sensitive measures such as methacholine challenge, cardiopulmonary exercise testing, impulse oscillometry to assess small airways, and exhaled breath condensate nitric oxide levels, as well as skin prick testing for aeroallergens may be helpful. Quantitation of indoor aeroallergens from bulk dust in trailers may separate the indoor versus outdoor component. Sampling of burn pit pile dust itself will enable geochemical characterization of the source. Geological characterization of endogenous dust for geometry, mineral content, porosity, bacteriology may also be helpful, as is use of animal models with spontaneous asthma such as the vasoactive intestinal peptide knockout mouse—challenged with burn pit or endogenous dust—with and without allergic sensitization to dust mite antigen.
Similar data are available from Operation Desert Storm and the first deployment to Kuwait and Iraq. The PM size was defined in a study by Korenyi,20,21 who identified the chemical content of the sand.
SIGNIFICANCE OF STUDY/DISCUSSION
Soldiers deployed to Iraq and Afghanistan are at greater risk of having new-onset respiratory symptoms compared with elsewhere-stationed troops. Considering that upwards of 100,000 per year were deployed to Iraq since 2003, and a troop surge is in progress in Afghanistan, the potential ramifications of increased new-onset lung disease and disability in the previously healthy deployed population are substantial. Asthma is a disqualification for enlistment in the Army in the absence of a medical waiver. Recall that soldiers undergo basic training, which entails physical exercise and exposure to tear gas, factors that may elicit symptoms prior to deployment. In addition, soldiers are screened at Fort Hood, Texas, to verify battalion readiness before embarking on combat missions. As a self-selected group of young individuals engaged in outdoor activities, the rate of respiratory symptoms at baseline is expected to be low among recently returned soldiers. Statistical differences in the rates of symptoms associated with ordering spirometry by physicians—who are not compelled to do so—suggest that geography of deployment may influence the development of new-onset respiratory illness. Our data have spanned zip codes in the Long Island and greater New York City region and all branches of service in the military (Army, Navy, Air Force, Marines, and Coast Guard).
Data from our laboratory now indicate that in the absence of a policy of system-wide screening spirometry, only 1.8% of non–Iraq/Afghanistan-based soldiers were symptomatic with shortness of breath or dyspnea and received spirometry, versus 14.5% of Iraq-Afghanistan based soldiers had respiratory symptoms warranting spirometry. Other investigators have provided supporting data. After examining soldiers with normal physical examinations, normal spirometry, normal chest radiographs, and normal chest computed tomographic scans, Dr Robert Miller's team from Vanderbilt University, Nashville, Tennessee, consecutively biopsied 49 dyspneic soldiers from Fort Campbell, Kentucky, who returned from Iraq. Thirty-eight of 49 had bronchiolitis and vascular remodeling, whereas two had hypersensitivity pneumonitis.17 If Miller's data apply to our population in New York, then we are at risk of underdiagnosing lung disease, particularly constrictive bronchiolitis and vascular remodeling, among the veteran population returning from Iraq and Afghanistan. We have one biopsy to date on a soldier with an abnormal chest radiograph and abnormal computed tomography of the chest. Nevertheless, no troops with clear chest radiographs, clear computed tomographic scans, and associated normal spirometry have been biopsied. Indeed, the soldier we biopsied with a tissue diagnosis of nonspecific interstitial pneumonitis and lung fibrosis only had mild reduction in the diffusion capacity, and all lung volumes were normal. This would mean that we are missing cases, since this patient was not counted in our study; and, we have potentially missed cases of constrictive bronchiolitis and vascular remodeling as seen in 78% of cases in Miller's study (all biopsies were abnormal).
The populations (deployed vs not deployed) are similar in all ways, except one. There are far more smokers in the deployed population than the not deployed population. The possibility that this difference accounts, at least, in part, for the difference in symptoms and pulmonary function test results should be considered. Nevertheless, smoking rates cannot fully account for the differences in spirometry rates. Is the interaction between the environmental exposures and smoking synergistic? Should smoking cessation be encouraged before deployment? Is there a genetic susceptibility component? Prospective studies done with baseline pulmonary function studies may be able to address these concerns.
Although active-duty soldiers and veterans often register and visit the OIF/OEF clinic, some, particularly active-duty soldiers with TRICARE insurance, go directly to a primary medical care provider and subsequently get referred to subspecialists. The OIF/OEF clinic is a specialized clinic with plausibly high levels of aggressive care. All patients entering this clinic get mandatory chest x-rays, mandatory thyroid function tests, and mandatory celiac sprue tests. Spirometry is not mandatory in the OIF/OEF clinic, although we, as part of the Denver Working Group on Post-Deployment Health Issues, recommend pre- and postdeployment spirometry and 2-mile run times. Patients who are diagnosed with disease in the OIF/OEF clinic may qualify for disability benefits. So, it is possible that patients may be more aware of symptoms, health care providers may be more sympathetic or biased, or that administrative pressure, either perceived or real, may influence the ordering of tests. An alternative explanation is that these tests have been infrequently ordered in the past based on lack of awareness of respiratory issues regarding Iraq/Afghanistan deployment. Spirometry screening days are twice a month at the Northport VA, so making an appointment is critical. Diagnosing asthma, in particular, by at-rest spirometry alone, is a crude and relatively insensitive test, compared with a systems approach employing (1) impulse oscillometry, a more sensitive and specific test of peripheral airways resistance and airway hyperresponsiveness; (2) methacholine challenge; (3) cardiopulmonary exercise testing with pre- and postexercise spirometry; (4) aeroallergen skin prick testing to outdoor and indoor aeroallergens from the United States and Iraq/Afghanistan; and (5) echocardiography and right heart catheterization to exclude pulmonary arterial hypertension from vascular remodeling. What is even more critical in a previously healthy population, which may be supranormal prior to deployment is the assessment of predeployment 2-mile run times and spirometry with bronchodilator-compared longitudinal, serial measurements postdeployment, especially in those nonsmokers who have maintained ideal body weight. The Northport VA does not have impulse oscillometry or on-site methacholine challenge as a measure of airways hyper-responsiveness, a sine qua non of asthma. In addition, cardiopulmonary exercise testing, a test for exercise-induced asthma, is not on-site and is approached by a so-called “fee-basis” mechanism to pay for services at an outside provider. This may be administratively limiting. In addition, exhaustive aeroallergen testing, including those antigens present regionally in Iraq and Afghanistan, is not readily available, thereby potentially missing those with allergic asthma. There is no obligation to direct a patient to the allergy clinic, so that in the absence of serum IgE testing or skin testing, allergic asthma may be missed and a soldier's complaints dismissed.
If recent trends in asthma prevalence indicate that rates of asthma and allergy and increasing worldwide as well as locally, then a longer and more severe pollen season (high pollen counts over a prolonged period of time) may be due to a combination of factors, including the possibility of climate change. The dictum that for every 1° increase in temperature, more ragweed pollen air pollution is dispersed is noteworthy from the point of view that the physicochemical properties of ragweed—even in the absence of allergic sensitization or positive skin tests—may cause symptoms and clinical disease, since the ragweed pollen resembles a “spiked ball.” Another possibility is that misdiagnosed nonallergic rhinitis with eosinophilia syndrome can lead to cough, and some investigators indicate this may be mild form of aspirin-exacerbated respiratory disease, formerly known as Samter's Triad. Soldiers with pain from injuries and wounds may be more likely to take aspirin and nonsteroidal ant-inflammatory drugs, thereby raising the exposure to these medications in this population and potentially increasing the risk of aspirin-exacerbated respiratory disease. High rates of TBI and PTSD (92.5 and 42.4%, respectively), among all persons who received spirometry (regardless of duty station, both non-Iraq/non-Afghanistan, and Iraq/Afghanistan) is concerning, in part, because blast overpressure from shock waves because of explosions, if significant enough to warrant a diagnosis of TBI, may have also caused lung injury from shock waves to the delicate alveoli or air sacs tethered in the lung.22 Indeed, this is a different pathology from asthma. What complicates the picture even further is that PTSD is associated with higher rates of asthma in monozygotic (identical) twins.23 So, if one twin has PTSD and another does not, then the risk of asthma is greater in the former.
If the distribution of spirometric data is non-Gaussian, then similar FEV1 and FVC values are important, versus strict reliance on percent predicted values. The age, weight, and height values means were not statistically different in this cohort. Smith et al24 reported that among 46,077 active-duty soldiers in the Millennium Cohort Study, deployers to Iraq and Afghanistan had a higher rate of newly reported respiratory symptoms (persistent cough, shortness of breath) than nondeployers (14% vs 10%), suggesting that our rates among Iraq/Afghanistan-deployed Long Island troops are identical to their study, and indicating that rates among nondeployed troops based in Long Island are lower. In the analogous World Trade Center disaster on September 11, 2001, firefighters exposed to the fires, fumes, and smoke, who had high levels of exposure, were more likely to have respiratory symptoms, reduction in lung volume by 500 mL at 5 years, and positive methacholine challenge tests which were persistent.25,26 Rates of sarcodiosis spiked in the year after the disaster at the time on the ongoing fires, which burned for months, then they subsided and have remained at pre-9/11 levels since then.27 If burning of trash in Iraq is of an even longer duration, with many troops undergoing multiple deployments at 12 months each, then we should have heightened concern for these types of illnesses.
The study has the potential to inform recommendations regarding force health protection guidance with respect to trash disposal, occupational health regulations, decisions regarding applications for disability because of lung disease, and medical follow-up and screening of veterans deployed to Iraq.
The authors thank Ellen Berberich, Karen Dorwin, and Christy Zelo from the Office of Information & Technology, VAMC, Northport, New York for computer database mining assistance. SUNY Stony undergraduate student Kun Pan assisted in literature searches.
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