Cross sectional analysis of respiratory symptoms in an injection drug user cohort: the impact of obstructive lung disease and HIV
© Drummond et al; licensee BioMed Central Ltd. 2010
Received: 5 January 2010
Accepted: 11 May 2010
Published: 11 May 2010
Injection drug use is associated with an increased risk of human immunodeficiency virus (HIV) infection and with obstructive lung diseases (OLD). Understanding how HIV and OLD may impact respiratory symptoms among injection drug users (IDUs) is important to adequately care for this high-risk population. We characterized the independent and joint effects of HIV and OLD on respiratory symptoms of a cohort of inner-city IDUs.
Demographics, risk behavior and spirometric measurements were collected from a cross-sectional analysis of the Acquired Immunodeficiency Syndrome Link to the IntraVenous Experience study, an observational cohort of IDUs followed in Baltimore, MD since 1988. Participants completed a modified American Thoracic Society respiratory questionnaire and the Medical Research Council (MRC) dyspnea score to assess respiratory symptoms of cough, phlegm, wheezing and dyspnea.
Of 974 participants, 835 (86%) were current smokers and 288 (29.6%) were HIV-infected. The prevalence of OLD (FEV1/FVC ≤ 0.70) was 15.5%, and did not differ by HIV status. OLD, but not HIV, was associated with increased frequency of reported respiratory symptoms. There was a combined effect of OLD and HIV on worsening of MRC scores. OLD and HIV were independently associated with an increased odds of reporting an MRC ≥ 2 (OR 1.83 [95%CI 1.23-2.73] and 1.50 [95%CI 1.08-2.09], respectively). COPD, but not HIV, was independently associated with reporting an MRC ≥ 3 (OR 2.25 [95%CI 1.43-3.54] and 1.29 [95%CI 0.87-1.91], respectively).
While HIV does not worsen cough, phlegm or wheezing, HIV significantly increases moderate but not severe dyspnea in individuals of similar OLD status. Incorporating the MRC score into routine evaluation of IDUs at risk for OLD and HIV provides better assessment than cough, phlegm and wheezing alone.
Injection drug use (IDU) is a prevalent social behavior in urban centers that is associated with many acute and chronic medical illnesses [1–4]. Due to similar underlying risk factors in injection drug users (IDUs), unique chronic medical conditions frequently co-exist in the same individual [5–10]. IDU is a risk factor for the development of two prevalent diseases: obstructive lung diseases (OLD), specifically chronic obstructive pulmonary disease (COPD) [11–13]. and human immunodeficiency virus (HIV) infection[3, 14, 15]. In 2006, nearly 140,000 deaths were attributed to either COPD or HIV in the States[16, 17].
Risk factors for the development of OLD, such as tobacco use and low socio-economic status, overlap in those with HIV. Prior studies have described the frequent coexistence of HIV and OLD in at-risk populations[11, 19, 20]. Because IDUs are particularly vulnerable to both OLD and HIV, it is important to explore how these two diseases may impact respiratory status. To date, no data exist on the impact of OLD and HIV on respiratory symptoms and functional status among and IDU population. The Acquired Immunodeficiency Syndrome (AIDS) Link to IntraVenous Experience (ALIVE) study. has prospectively observed a cohort of both HIV-infected and at risk IDUs in inner-city Baltimore, Maryland, since 1988, providing an ideal dataset to examine the independent and joint effects of HIV and OLD on manifestation of respiratory disease.
Setting and Participants
The methods for recruitment and data collection in the ALIVE study have been previously described. Subjects were recruited through community outreach programs outside of treatment using distribution of flyers and word of mouth. Briefly, participants were required to be ≥ 18 yrs of age and have a history of injecting drugs. ALIVE participants that underwent spirometry testing as part of the lung sub-study were included in the current analysis. This study was approved by Institutional Review Boards of the Johns Hopkins Bloomberg School of Public Health and the National Cancer Institute. All enrolled participants provided written informed consent.
In this cross-sectional analysis, exposure and outcome data were obtained from the ALIVE study visit where spirometry was first obtained; participants also underwent clinical examination, collection of blood specimens, behavior and respiratory questionnaires. Smoking status and duration, recent injection drug use and anti-retroviral or bronchodilator therapy were determined by self-report. Medical conditions such as respiratory infections or clinical AIDS events were identified through self-report and confirmed through standardized medical record abstraction. Spirometry was performed using a KOKO® (Pulmonary Data Services, Inc., Louisville, CO) pneumotach in accordance with American Thoracic Society guidelines. Percent predicted values were calculated using standard formulas. OLD was defined as a pre-bronchodilator ratio of the forced expiratory volume in one second (FEV1) to forced vital capacity (FVC) of ≤ 70%. Participants completed a modified version of the American Thoracic Society respiratory questionnaire. Our questionnaire captured information regarding presence, frequency and timing of respiratory symptoms (cough, phlegm and wheezing). Dyspnea was assessed using the modified Medical Research Council (MRC) questionnaire with a validated 0-4 scale, with a higher score indicating worse dyspnea[26, 27]. The MRC score has been shown to correlate with lung function and long-term mortality in COPD patients and thus is employed as a tool for assessment of disease impact [27–29].
We compared the prevalence of respiratory symptoms in individuals with and without OLD (defined by FEV1/FVC ≤ 70%) grouped by HIV status. Clinical and demographic characteristics between groups were compared using t-test for continuous variables. Categorical variables were compared with Pearson's chi square and Fisher's exact tests. Analysis of variance was performed to test the effects of HIV and OLD on clinical and spirometric measurements. Because of multiple comparisons, a Bonferroni corrected p-value was used to assess for statistical significance in the two-way comparison. Differences in the distribution of MRC scores were assessed with Pearson's chi squared test. Multivariable logistic regression models were generated to explore combinations of variables associated with different MRC thresholds. Covariates were evaluated based upon known relevance from clinical literature review and/or inspection of exploratory data analysis. Odds ratios were adjusted for age, gender, body-mass index (BMI), lifetime pack-years smoking, number of lifetime pneumonias, presence of severe anemia (hemoglobin<8 mg/dL) and injection drug use status. Hemoglobin samples were not collected on HIV-uninfected participants prior to October 2007, thus these values were missing on 469 (48.2%) of the cohort. Results with and without this covariate in logistic regression modeling did not affect the overall results. Additional multivariable models restricted to HIV-infected individuals compared thresholds of viral load and CD4 levels. All data are presented as mean (standard deviation) for normally distributed data and median (interquartile range [IQR]) for non-normally distributed data. Stata version 10.0 (Stata Corp, College Station, TX), was used for statistical analysis.
Of the 1052 participants evaluated in the lung sub-study, 78 participants lacked complete spirometric data and were excluded. Therefore, analysis presented includes demographic, anthropometric, spirometric and respiratory questionnaire data from 974 individuals. Overall, participants were a median age of 48.7 years old (IQR, 43.6-53.5 years), 65.9% were males, 89.8% were black. Overall, 85.7% were current smokers, 9.3% were former smokers and 4.9% had never smoked. A total of 288 (29.6%) individuals were HIV-infected. Of HIV-infected participants, 155 (54.6%) reported highly active anti-retroviral therapy (HAART) use in the last 6 months. HIV-infected HAART users had a median CD4 count was 322 cells/mm3 (IQR, 177-503) and 109 (70.3%) had an undetectable viral load. Of the 133 HIV-infected individuals not reporting HAART use in the last 6 months, the median CD4 count was 321 cells/mm3 (IQR, 178-497) and 22 (16.5%) had an undetectable viral load. The prevalence of HIV infection among the 78 excluded participants (30.8%) was similar to those included in analysis (29.6%).
Clinical and demographic characteristics of study participants.
Smoking status, n(%)
Current IDU, n(%)
6 mo income, n(%)
High school education, n(%)
Bronchodilator use, n(%)
CD4 cell count
HIV viral load
>400 copies, n(%)
X 100K, mean(SD)±
HAART use, n(%)
Spirometry characteristics of study participants.
Prevalence of respiratory symptoms stratified by OLD and HIV status.
≥ 4 days/week
≥ 3 months
≥ 4 days/week
≥ 3 months
Most days and nights
History of wheezing attack
Adjusted odds ratio (95%CI) of MRC thresholds*.
MRC ≥ 2
MRC ≥ 3
BMI (per kg/m2)
Smoking (per 10-pk yrs)
In this report, we have characterized the respiratory symptoms of a large cohort of IDUs at-risk for HIV and OLD. This analysis has yielded several important findings. First, in this population with almost ubiquitous cigarette smoking, we identified a high prevalence of respiratory symptoms even in the absence of OLD and HIV. While there was not an increased prevalence of reported cough, phlegm and wheezing associated with HIV, we did find that when HIV infection and OLD coexisted, dyspnea was worse than when either disease was present alone. Furthermore, HIV was independently associated with moderate dyspnea after controlling for the presence of OLD and other confounders.
Within this IDU cohort, a high prevalence of respiratory symptoms was present even in those participants without OLD or HIV. Despite the mean age of 48.7 years in our study cohort, the rates of respiratory symptoms observed in those without OLD and HIV are similar to rates reported in a population of elderly Medicare smokers. A prior report of 234 HIV-infected individuals, of whom 6.8% had spirometry-defined COPD, described a similar frequency of respiratory symptoms. Our report highlights the significant symptom burden experienced by the IDU population with heavy tobacco habits. We extend prior publications by stratifying respiratory symptoms and functional status in a population of injection drug users by OLD and HIV status. Prior publications have been limited to descriptions of respiratory symptoms in either OLD or HIV, but not in both disease states[34, 35].
While HIV status was not associated with increasing cough, phlegm and wheezing, there was a combined effect of HIV and OLD on dyspnea assessed by the MRC scale. To our knowledge, no prior study has evaluated the effect of HIV on MRC scores in individuals with and without OLD. Our analysis has shown that the presence of HIV is associated with a detrimental shift in the distribution of MRC scores when OLD is present, and this effect was independent of HIV severity. Moreover, patients who had both OLD and HIV had the highest proportion of MRC scores ≥ 2 and ≥ 3. Female gender was associated with increased odds of reporting an MRC ≥ 2 and ≥ 3 after adjusting for other characteristics. These findings add information to prior publications examining respiratory symptoms in HIV-infected populations, which have not included female participants. We observed a >50% increase in the risk of reporting an MRC ≥ 2 in the presence of HIV, highlighting the impact of HIV infection on dyspnea of individuals without substantially altering cough, phlegm and wheezing. Interestingly, OLD, but not HIV, remained an important predictor of reporting an MRC ≥ 3, suggesting that HIV may increase mild impairment independent of OLD, but advanced dyspnea is largely driven by OLD.
Several potential mechanisms exist by which HIV infection may increase the susceptibility to respiratory symptoms and diseases. HIV-infected individuals demonstrate elevated systemic inflammatory cytokines, including those implicated in the pathogenesis of OLD [36–38]. Moreover, elevated inflammatory cytokines are observed in the bronchoalveolar lavage fluid of asymptomatic HIV-infected individuals. In lung autopsy specimens of HIV-infected individuals, areas of histological emphysema had many HIV-1 infected cells, whereas rare HIV-1 infected cells were evident in normal lung, suggesting that direct HIV infection may drive emphysema formation. These observations suggest that infection with HIV leads to systemic and local abnormalities that may promote the development of OLD. Additionally, HIV infection is associated with an increase in the development of pulmonary arterial hypertension, which may be independently associated with increased respiratory symptoms.
Our study has several implications for health care providers caring for IDU patients at risk for OLD and HIV. The high prevalence of smoking and respiratory symptoms identifies IDUs as patients who would benefit from aggressive smoking cessation and spirometry screening initiatives. Second, when assessing respiratory symptoms in HIV+ patients at-risk for OLD, providers should be hesitant to attribute reported respiratory symptoms solely to HIV infection. Rather, healthcare providers should be vigilant to screen for undiagnosed OLD in this population. Third, clinicians should consider incorporating dyspnea as well as cough, phlegm and wheezing into routine assessments. Given that MRC scores have been shown to correlate with morbidity and mortality in longitudinal studies of OLD patients,[28, 31] incorporation of the MRC scale into routine clinical assessments of IDUs may provide further risk stratification of populations with the combined co-morbidities of OLD and HIV.
Our study has some limitations. First, the cross-sectional nature of this analysis prevents conclusions regarding longitudinal outcomes such as rate of FEV1 decline and mortality. Although analyses incorporating markers of advance HIV did not attenuate the effect of OLD on respiratory symptoms, the high background prevalence of smoking and respiratory symptoms in our population may be obscuring any effect of advanced HIV on respiratory illness. IDUs participating in longitudinal observational studies may differ from the general IDU population, impacting generalizability. Moreover, the inner-city characteristics of this cohort may further limit the generalizability of our findings to other IDU population or different populations with OLD and HIV. The absence of pre- and post-bronchodilator testing in this cohort does not allow us to make conclusions regarding the different symptom profile of asthma and COPD. While we accounted for number of pneumonias in our analysis, prior studies have reported that IDUs have an increased risk of bacterial pneumonia and tuberculosis when compared to other HIV risk groups, a confounder that could impact functional status[42, 43]. We also did not evaluate for underlying cardiac disease as a contributor to dyspnea. Despite these limitations, the large size of our cohort, the systematic administration of validated questionnaires and the use of standardized measures of lung function allow us to provide a novel and comprehensive study of respiratory symptoms and functional status in an inner-city IDU population at risk for HIV and OLD.
We show that HIV significantly worsens dyspnea, but has limited effect on the reported burden of cough, wheezing and phlegm in individuals of similar OLD status. Moreover, we found that OLD and HIV have an additive detrimental effect on dyspnea. HIV is independently associated with moderate but not severe dyspnea after controlling for OLD status. The results of this analysis provide new information which can assist providers managing a population particularly susceptible to the two important diseases of OLD and HIV.
Acquired Immunodeficiency Syndrome
AIDS Linked to IntraVenous Experience
CD4+ T-helper cells
Chronic obstructive pulmonary disease
Forced expiratory volume in one second
Forced vital capacity
Highly active anti-retroviral therapy
Human immunodeficiency virus
Injection drug use
Injection drug users
Medical research council
Obstructive lung disease
This study was funded in part by grants from the NIH (RO1s HL090483, DA04334 and DA12568). MBD is supported by an Institute for Clinical and Translational Research (KL2) Mentored Career Development Award from the National Institutes of Health. EAE is supported by the Intramural Research Program of the National Cancer Institute.
- Schoener EP, Hopper JA, Pierre JD: Injection drug use in North America. Infect Dis Clin North Am. 2002, 16: 535-551. 10.1016/S0891-5520(02)00010-7. vii.View ArticlePubMedGoogle Scholar
- Alcabes P, Friedland G: Injection drug use and human immunodeficiency virus infection. Clin Infect Dis. 1995, 20: 1467-1479.View ArticlePubMedGoogle Scholar
- Kral AH, Bluthenthal RN, Booth RE, Watters JK: HIV seroprevalence among street-recruited injection drug and crack cocaine users in 16 US municipalities. Am J Public Health. 1998, 88: 108-113. 10.2105/AJPH.88.1.108.View ArticlePubMedPubMed CentralGoogle Scholar
- Ebright JR, Pieper B: Skin and soft tissue infections in injection drug users. Infect Dis Clin North Am. 2002, 16: 697-712. 10.1016/S0891-5520(02)00017-X.View ArticlePubMedGoogle Scholar
- Gachupin-Garcia A, Selwyn PA, Budner NS: Population-based study of malignancies and HIV infection among injecting drug users in a New York City methadone treatment program, 1985-1991. AIDS. 1992, 6: 843-848. 10.1097/00002030-199208000-00013.View ArticlePubMedGoogle Scholar
- Sulkowski MS, Mast EE, Seeff LB, Thomas DL: Hepatitis C virus infection as an opportunistic disease in persons infected with human immunodeficiency virus. Clin Infect Dis. 2000, 30 (Suppl 1): S77-84. 10.1086/313842.View ArticlePubMedGoogle Scholar
- Johnson ME, Fisher DG, Fenaughty A, Theno SA: Hepatitis C virus and depression in drug users. Am J Gastroenterol. 1998, 93: 785-789. 10.1111/j.1572-0241.1998.225_a.x.View ArticlePubMedGoogle Scholar
- Lucas GM, Mehta SH, Atta MG, Kirk GD, Galai N, Vlahov D, Moore RD: End-stage renal disease and chronic kidney disease in a cohort of African-American HIV-infected and at-risk HIV-seronegative participants followed between 1988 and 2004. AIDS. 2007, 21: 2435-2443. 10.1097/QAD.0b013e32827038ad.View ArticlePubMedGoogle Scholar
- Chaturvedi AK, Pfeiffer RM, Chang L, Goedert JJ, Biggar RJ, Engels EA: Elevated risk of lung cancer among people with AIDS. AIDS. 2007, 21: 207-213. 10.1097/QAD.0b013e3280118fca.View ArticlePubMedGoogle Scholar
- Kirk GD, Merlo C, P OD, Mehta SH, Galai N, Vlahov D, Samet J, Engels EA: HIV infection is associated with an increased risk for lung cancer, independent of smoking. Clin Infect Dis. 2007, 45: 103-110. 10.1086/518606.View ArticlePubMedPubMed CentralGoogle Scholar
- Crothers K, Butt AA, Gibert CL, Rodriguez-Barradas MC, Crystal S, Justice AC: Increased COPD among HIV-positive compared to HIV-negative veterans. Chest. 2006, 130: 1326-1333. 10.1378/chest.130.5.1326.View ArticlePubMedGoogle Scholar
- Overland ES, Nolan AJ, Hopewell PC: Alteration of pulmonary function in intravenous drug abusers. Prevalence, severity, and characterization of gas exchange abnormalities. Am J Med. 1980, 68: 231-237. 10.1016/0002-9343(80)90359-9.View ArticlePubMedGoogle Scholar
- Sherman CB, Hudson LD, Pierson DJ: Severe precocious emphysema in intravenous methylphenidate (Ritalin) abusers. Chest. 1987, 92: 1085-1087. 10.1378/chest.92.6.1085.View ArticlePubMedGoogle Scholar
- Holmberg SD: The estimated prevalence and incidence of HIV in 96 large US metropolitan areas. Am J Public Health. 1996, 86: 642-654. 10.2105/AJPH.86.5.642.View ArticlePubMedPubMed CentralGoogle Scholar
- Des Jarlais DC, Friedman SR: HIV infection among intravenous drug users: epidemiology and risk reduction. AIDS. 1987, 1: 67-76.PubMedGoogle Scholar
- Heron M, Hoyert DL, Murphy SL, Xu J, Kochanek KD, Tejada-Vera B: Deaths: final data for 2006. Natl Vital Stat Rep. 2009, 57: 1-134.PubMedGoogle Scholar
- CDC: HIV/AIDS Surveillance Report, 2006. Vol. 18. Book HIV/AIDS Surveillance Report, 2006, (Editor ed.^ds.). 2008, City: CDC, 18:Google Scholar
- Burns DN, Hillman D, Neaton JD, Sherer R, Mitchell T, Capps L, Vallier WG, Thurnherr MD, Gordin FM: Cigarette smoking, bacterial pneumonia, and other clinical outcomes in HIV-1 infection. Terry Beirn Community Programs for Clinical Research on AIDS. J Acquir Immune Defic Syndr Hum Retrovirol. 1996, 13: 374-383.View ArticlePubMedGoogle Scholar
- Diaz PT, Clanton TL, Pacht ER: Emphysema-like pulmonary disease associated with human immunodeficiency virus infection. Ann Intern Med. 1992, 116: 124-128.View ArticlePubMedGoogle Scholar
- Diaz PT, King MA, Pacht ER, Wewers MD, Gadek JE, Nagaraja HN, Drake J, Clanton TL: Increased susceptibility to pulmonary emphysema among HIV-seropositive smokers. Ann Intern Med. 2000, 132: 369-372.View ArticlePubMedGoogle Scholar
- Vlahov D, Anthony JC, Munoz A, Margolick J, Nelson KE, Celentano DD, Solomon L, Polk BF: The ALIVE study, a longitudinal study of HIV-1 infection in intravenous drug users: description of methods and characteristics of participants. NIDA Res Monogr. 1991, 109: 75-100.PubMedGoogle Scholar
- Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, Grinten van der CP, Gustafsson P, et al: Standardisation of spirometry. Eur Respir J. 2005, 26: 319-338. 10.1183/09031936.05.00034805.View ArticlePubMedGoogle Scholar
- Hankinson JL, Odencrantz JR, Fedan KB: Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med. 1999, 159: 179-187.View ArticlePubMedGoogle Scholar
- Gomez FP, Rodriguez-Roisin R: Global initiative for Chronic Obstructive Lung Disease (GOLD) guidelines for chronic obstructive pulmonary disease. Current Opinion in Pulmonary Medicine. 2002, 8: 81-10.1097/00063198-200203000-00001.View ArticlePubMedGoogle Scholar
- Ferris BG: Epidemiology Standardization Project (American Thoracic Society). Am Rev Respir Dis. 1978, 118: 1-120.PubMedGoogle Scholar
- Fletcher CM: The clinical diagnosis of pulmonary emphysema; an experimental study. Proc R Soc Med. 1952, 45: 577-584.PubMedGoogle Scholar
- Bestall JC, Paul EA, Garrod R, Garnham R, Jones PW, Wedzicha JA: Usefulness of the Medical Research Council (MRC) dyspnoea scale as a measure of disability in patients with chronic obstructive pulmonary disease. Thorax. 1999, 54: 581-586. 10.1136/thx.54.7.581.View ArticlePubMedPubMed CentralGoogle Scholar
- Celli BR, Cote CG, Marin JM, Casanova C, Montes de Oca M, Mendez RA, Pinto Plata V, Cabral HJ: The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med. 2004, 350: 1005-1012. 10.1056/NEJMoa021322.View ArticlePubMedGoogle Scholar
- Oga T, Nishimura K, Tsukino M, Sato S, Hajiro T, Mishima M: Longitudinal deteriorations in patient reported outcomes in patients with COPD. Respir Med. 2007, 101: 146-153. 10.1016/j.rmed.2006.04.001.View ArticlePubMedGoogle Scholar
- Hajiro T, Nishimura K, Tsukino M, Ikeda A, Oga T, Izumi T: A comparison of the level of dyspnea vs disease severity in indicating the health-related quality of life of patients with COPD. Chest. 1999, 116: 1632-1637. 10.1378/chest.116.6.1632.View ArticlePubMedGoogle Scholar
- Nishimura K, Izumi T, Tsukino M, Oga T: Dyspnea is a better predictor of 5-year survival than airway obstruction in patients with COPD. Chest. 2002, 121: 1434-1440. 10.1378/chest.121.5.1434.View ArticlePubMedGoogle Scholar
- Enright PL, Kronmal RA, Higgins MW, Schenker MB, Haponik EF: Prevalence and correlates of respiratory symptoms and disease in the elderly. Cardiovascular Health Study. Chest. 1994, 106: 827-834. 10.1378/chest.106.3.827.View ArticlePubMedGoogle Scholar
- George MP, Kannass M, Huang L, Sciurba FC, Morris A: Respiratory symptoms and airway obstruction in HIV-infected subjects in the HAART era. PLoS One. 2009, 4: e6328-10.1371/journal.pone.0006328.View ArticlePubMedPubMed CentralGoogle Scholar
- Diaz PT, Wewers MD, Pacht E, Drake J, Nagaraja HN, Clanton TL: Respiratory symptoms among HIV-seropositive individuals. Chest. 2003, 123: 1977-1982. 10.1378/chest.123.6.1977.View ArticlePubMedGoogle Scholar
- Crothers K, Griffith TA, McGinnis KA, Rodriguez-Barradas MC, Leaf DA, Weissman S, Gibert CL, Butt AA, Justice AC: The impact of cigarette smoking on mortality, quality of life, and comorbid illness among HIV-positive veterans. J Gen Intern Med. 2005, 20: 1142-1145. 10.1111/j.1525-1497.2005.0255.x.View ArticlePubMedPubMed CentralGoogle Scholar
- Matsumoto T, Miike T, Nelson RP, Trudeau WL, Lockey RF, Yodoi J: Elevated serum levels of IL-8 in patients with HIV infection. Clin Exp Immunol. 1993, 93: 149-151. 10.1111/j.1365-2249.1993.tb07957.x.View ArticlePubMedPubMed CentralGoogle Scholar
- Lahdevirta J, Maury CP, Teppo AM, Repo H: Elevated levels of circulating cachectin/tumor necrosis factor in patients with acquired immunodeficiency syndrome. Am J Med. 1988, 85: 289-291. 10.1016/0002-9343(88)90576-1.View ArticlePubMedGoogle Scholar
- Rimaniol AC, Zylberberg H, Zavala F, Viard JP: Inflammatory cytokines and inhibitors in HIV infection: correlation between interleukin-1 receptor antagonist and weight loss. AIDS. 1996, 10: 1349-1356. 10.1097/00002030-199610000-00006.View ArticlePubMedGoogle Scholar
- Denis M, Ghadirian E: Dysregulation of interleukin 8, interleukin 10, and interleukin 12 release by alveolar macrophages from HIV type 1-infected subjects. AIDS Res Hum Retroviruses. 1994, 10: 1619-1627. 10.1089/aid.1994.10.1619.View ArticlePubMedGoogle Scholar
- Yearsley MM, Diaz PT, Knoell D, Nuovo GJ: Correlation of HIV-1 detection and histology in AIDS-associated emphysema. Diagn Mol Pathol. 2005, 14: 48-52. 10.1097/01.pas.0000142168.72253.11.View ArticlePubMedGoogle Scholar
- Talwar A, Sarkar P, Rosen MJ: Pulmonary arterial hypertension in human immunodeficiency virus infection. Postgrad Med. 2009, 121: 56-67. 10.3810/pgm.2009.09.2053.View ArticlePubMedGoogle Scholar
- Selwyn PA, Feingold AR, Hartel D, Schoenbaum EE, Alderman MH, Klein RS, Friedland GH: Increased risk of bacterial pneumonia in HIV-infected intravenous drug users without AIDS. AIDS. 1988, 2: 267-272. 10.1097/00002030-198808000-00005.View ArticlePubMedGoogle Scholar
- Wallace JM, Hansen NI, Lavange L, Glassroth J, Browdy BL, Rosen MJ, Kvale PA, Mangura BT, Reichman LB, Hopewell PC: Respiratory disease trends in the Pulmonary Complications of HIV Infection Study cohort. Pulmonary Complications of HIV Infection Study Group. Am J Respir Crit Care Med. 1997, 155: 72-80.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2466/10/27/prepub