Obstructive Lung Diseases in HIV: A Clinical Review and Identification of Key Future Research Needs

 

 Buy Article Permissions and Reprints

Abstract

HIV infection has shifted from what was once a disease directly impacting short-term mortality to what is now a chronic illness controllable in the era of effective combination antiretroviral therapy (ART). In this setting, life expectancy for HIV-infected individual is nearly comparable to that of individuals without HIV. Subsequent to this increase in life expectancy, there has been recognition of increased multimorbidity among HIV-infected persons, with prevalence of comorbid chronic illnesses now approaching 65%. Obstructive lung diseases, including chronic obstructive pulmonary disease (COPD) and asthma, are prevalent conditions associated with substantial morbidity and mortality in the United States. There is overlap in risk factors for HIV acquisition and chronic lung diseases, including lower socioeconomic status and the use of tobacco and illicit drugs. Objectives of this review are to (1) summarize the current state of knowledge regarding COPD and asthma among HIV-infected persons, (2) highlight implications for clinicians caring for patients with these combined comorbidities, and (3) identify key research initiatives to reduce the burden of obstructive lung diseases among HIV-infected persons.

• References

• 1 Samji H, Cescon A, Hogg RS , et al; North American AIDS Cohort Collaboration on Research and Design (NA-ACCORD) of IeDEA. Closing the gap: increases in life expectancy among treated HIV-positive individuals in the United States and Canada. PLoS ONE 2013; 8 (12) e81355
  CrossrefPubMedGoogle Scholar
• 2 Kim DJ, Westfall AO, Chamot E , et al. Multimorbidity patterns in HIV-infected patients: the role of obesity in chronic disease clustering. J Acquir Immune Defic Syndr 2012; 61 (5) 600-605
  CrossrefPubMedGoogle Scholar
• 3 Effros RB, Fletcher CV, Gebo K , et al. Aging and infectious diseases: workshop on HIV infection and aging: what is known and future research directions. Clin Infect Dis 2008; 47 (4) 542-553
  CrossrefPubMedGoogle Scholar
• 4 Salter ML, Lau B, Go VF, Mehta SH, Kirk GD. HIV infection, immune suppression, and uncontrolled viremia are associated with increased multimorbidity among aging injection drug users. Clin Infect Dis 2011; 53 (12) 1256-1264
  CrossrefPubMedGoogle Scholar
• 5 Shiels MS, Cole SR, Kirk GD, Poole C. A meta-analysis of the incidence of non-AIDS cancers in HIV-infected individuals. J Acquir Immune Defic Syndr 2009; 52 (5) 611-622
  CrossrefPubMedGoogle Scholar
• 6 Barnett CF, Hsue PY, Machado RF. Pulmonary hypertension: an increasingly recognized complication of hereditary hemolytic anemias and HIV infection. JAMA 2008; 299 (3) 324-331
  PubMedGoogle Scholar
• 7 Gómez FP, Rodriguez-Roisin R. Global Initiative for Chronic Obstructive Lung Disease (GOLD) guidelines for chronic obstructive pulmonary disease. Curr Opin Pulm Med 2002; 8 (2) 81-86
  CrossrefPubMedGoogle Scholar
• 8 McHugh MK, Symanski E, Pompeii LA, Delclos GL. Prevalence of asthma among adult females and males in the United States: results from the National Health and Nutrition Examination Survey (NHANES), 2001-2004. J Asthma 2009; 46 (8) 759-766
  PubMedGoogle Scholar
• 9 Mannino DM, Homa DM, Akinbami LJ, Moorman JE, Gwynn C, Redd SC. Surveillance for asthma—United States, 1980-1999. MMWR Surveill Summ 2002; 51 (1) 1-13
  PubMedGoogle Scholar
• 10 Schoener EP, Hopper JA, Pierre JD. Injection drug use in North America. Infect Dis Clin North Am 2002; 16 (3) 535-551 , vii
  CrossrefPubMedGoogle Scholar
• 11 Marshall MM, McCormack MC, Kirk GD. Effect of cigarette smoking on HIV acquisition, progression, and mortality. AIDS Educ Prev 2009; 21 (3, Suppl): 28-39
  CrossrefPubMedGoogle Scholar
• 12 American College of Physicians. Inner-city health care. Ann Intern Med 1997; 126 (6) 485-490
  CrossrefPubMedGoogle Scholar
• 13 Alcabes P, Friedland G. Injection drug use and human immunodeficiency virus infection. Clin Infect Dis 1995; 20 (6) 1467-1479
  CrossrefPubMedGoogle Scholar
• 14 Holmberg SD. The estimated prevalence and incidence of HIV in 96 large US metropolitan areas. Am J Public Health 1996; 86 (5) 642-654
  CrossrefPubMedGoogle Scholar
• 15 Lozano R, Naghavi M, Foreman K , et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380 (9859) 2095-2128
  CrossrefPubMedGoogle Scholar
• 16 Kuhlman JE, Knowles MC, Fishman EK, Siegelman SS. Premature bullous pulmonary damage in AIDS: CT diagnosis. Radiology 1989; 173 (1) 23-26
  CrossrefPubMedGoogle Scholar
• 17 Diaz PT, King MA, Pacht ER , et al. Increased susceptibility to pulmonary emphysema among HIV-seropositive smokers. Ann Intern Med 2000; 132 (5) 369-372
  PubMedGoogle Scholar
• 18 Morris AM, Huang L, Bacchetti P , et al; The Pulmonary Complications of HIV Infection Study Group. Permanent declines in pulmonary function following pneumonia in human immunodeficiency virus-infected persons. Am J Respir Crit Care Med 2000; 162 (2, Pt 1) 612-616
  CrossrefPubMedGoogle Scholar
• 19 Crothers K, Butt AA, Gibert CL, Rodriguez-Barradas MC, Crystal S, Justice AC ; Veterans Aging Cohort 5 Project Team. Increased COPD among HIV-positive compared to HIV-negative veterans. Chest 2006; 130 (5) 1326-1333
  CrossrefPubMedGoogle Scholar
• 20 Crothers K, Huang L, Goulet JL , et al. HIV infection and risk for incident pulmonary diseases in the combination antiretroviral therapy era. Am J Respir Crit Care Med 2011; 183 (3) 388-395
  CrossrefPubMedGoogle Scholar
• 21 Nakamura H, Tateyama M, Tasato D , et al. The prevalence of airway obstruction among Japanese HIV-positive male patients compared with general population; a case-control study of single center analysis. J Infect Chemother 2014; 20 (6) 361-364
  CrossrefPubMedGoogle Scholar
• 22 Drummond MB, Huang L, Diaz PT , et al. Factors associated with abnormal spirometry among HIV-infected individuals. AIDS 2015; 29 (13) 1691-1700
  CrossrefPubMedGoogle Scholar
• 23 Pefura-Yone EW, Fodjeu G, Kengne AP, Roche N, Kuaban C. Prevalence and determinants of chronic obstructive pulmonary disease in HIV infected patients in an African country with low level of tobacco smoking. Respir Med 2015; 109 (2) 247-254
  CrossrefPubMedGoogle Scholar
• 24 Akanbi MO, Taiwo BO, Achenbach CJ , et al. HIV associated chronic obstructive pulmonary disease in Nigeria. J AIDS Clin Res 2015; 6 (5) pii : 453
  PubMedGoogle Scholar
• 25 Onyedum CC, Chukwuka JC, Onwubere BJ, Ulasi II, Onwuekwe IO. Respiratory symptoms and ventilatory function tests in Nigerians with HIV infection. Afr Health Sci 2010; 10 (2) 130-137
  PubMedGoogle Scholar
• 26 Makinson A, Hayot M, Eymard-Duvernay S , et al; ANRS EP48 HIV CHEST Study Team. High prevalence of undiagnosed COPD in a cohort of HIV-infected smokers. Eur Respir J 2015; 45 (3) 828-831
  CrossrefPubMedGoogle Scholar
• 27 Drummond MB, Merlo CA, Astemborski J , et al. The effect of HIV infection on longitudinal lung function decline among IDUs: a prospective cohort. AIDS 2013; 27 (8) 1303-1311
  CrossrefPubMedGoogle Scholar
• 28 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 (7) e6328
  CrossrefPubMedGoogle Scholar
• 29 Gingo MR, George MP, Kessinger CJ , et al. Pulmonary function abnormalities in HIV-infected patients during the current antiretroviral therapy era. Am J Respir Crit Care Med 2010; 182 (6) 790-796
  CrossrefPubMedGoogle Scholar
• 30 Hirani A, Cavallazzi R, Vasu T , et al. Prevalence of obstructive lung disease in HIV population: a cross sectional study. Respir Med 2011; 105 (11) 1655-1661
  CrossrefPubMedGoogle Scholar
• 31 Sampériz G, Guerrero D, López M , et al. Prevalence of and risk factors for pulmonary abnormalities in HIV-infected patients treated with antiretroviral therapy. HIV Med 2014; 15 (6) 321-329
  CrossrefPubMedGoogle Scholar
• 32 Nimmo C, Capocci S, Honeyborne I , et al. Airway bacteria and respiratory symptoms are common in ambulatory HIV-positive UK adults. Eur Respir J 2015; 46 (4) 1208-1211
  CrossrefPubMedGoogle Scholar
• 33 Cui Q, Carruthers S, McIvor A, Smaill F, Thabane L, Smieja M. Effect of smoking on lung function, respiratory symptoms and respiratory diseases amongst HIV-positive subjects: a cross-sectional study. AIDS Res Ther 2010; 7: 6
  CrossrefPubMedGoogle Scholar
• 34 Madeddu G, Fois AG, Calia GM , et al. Chronic obstructive pulmonary disease: an emerging comorbidity in HIV-infected patients in the HAART era?. Infection 2013; 41 (2) 347-353
  CrossrefPubMedGoogle Scholar
• 35 Kristoffersen US, Lebech AM, Mortensen J, Gerstoft J, Gutte H, Kjaer A. Changes in lung function of HIV-infected patients: a 4.5-year follow-up study. Clin Physiol Funct Imaging 2012; 32 (4) 288-295
  CrossrefPubMedGoogle Scholar
• 36 Kunisaki KM, Niewoehner DE, Collins G , et al; International Network for Strategic Initiatives in Global HIV Trials (INSIGHT) START Study Group. Pulmonary function in an international sample of HIV-positive, treatment-naïve adults with CD4 counts > 500 cells/μL: a substudy of the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) trial. HIV Med 2015; 16 (Suppl. 01) 119-128
  CrossrefPubMedGoogle Scholar
• 37 Crothers K, McGinnis K, Kleerup E , et al. HIV infection is associated with reduced pulmonary diffusing capacity. J Acquir Immune Defic Syndr 2013; 64 (3) 271-278
  CrossrefPubMedGoogle Scholar
• 38 Fitzpatrick ME, Gingo MR, Kessinger C , et al. HIV infection is associated with diffusing capacity impairment in women. J Acquir Immune Defic Syndr 2013; 64 (3) 284-288
  CrossrefPubMedGoogle Scholar
• 39 Simonetti JA, Gingo MR, Kingsley L , et al. Pulmonary function in HIV-infected recreational drug users in the era of anti-retroviral therapy. J AIDS Clin Res 2014; 5 (11) 365
  PubMedGoogle Scholar
• 40 Zona S, Santoro A, Besutti G , et al. Burden of subclinical heart and lung disease detected on thoracic CT scans of HIV patients on HAART. J Int AIDS Soc 2014; 17 (4) (Suppl. 03) 19716
  PubMedGoogle Scholar
• 41 Clausen E, Wittman C, Gingo M , et al. Chest computed tomography findings in HIV-infected individuals in the era of antiretroviral therapy. PLoS ONE 2014; 9 (11) e112237
  CrossrefPubMedGoogle Scholar
• 42 Liu JC, Leung JM, Ngan DA , et al. Absolute leukocyte telomere length in HIV-infected and uninfected individuals: evidence of accelerated cell senescence in HIV-associated chronic obstructive pulmonary disease. PLoS ONE 2015; 10 (4) e0124426
  CrossrefPubMedGoogle Scholar
• 43 Leader JK, Huang L, King MA , et al. Risk factors associated with quantitative evidence of lung emphysema and fibrosis in an HIV-infected cohort. J Acquir Immune Defic Syndr 2015; ;doi: 10.1097/QAI.0000000000000894
  PubMedGoogle Scholar
• 44 Attia EF, Akgün KM, Wongtrakool C , et al. Increased risk of radiographic emphysema in HIV is associated with elevated soluble CD14 and nadir CD4. Chest 2014; 146 (6) 1543-1553
  CrossrefPubMedGoogle Scholar
• 45 Akinsete I, Akanmu AS, Okany CC. Spectrum of clinical diseases in HIV-infected adults at the Lagos University Teaching Hospital: a five-year experience [1992-1996]. Afr J Med Med Sci 1998; 27 (3–4) 147-151
  PubMedGoogle Scholar
• 46 Diaz PT, Wewers MD, Pacht E, Drake J, Nagaraja HN, Clanton TL. Respiratory symptoms among HIV-seropositive individuals. Chest 2003; 123 (6) 1977-1982
  CrossrefPubMedGoogle Scholar
• 47 McLeod DT, Neill P, Robertson VJ , et al. Pulmonary diseases in patients infected with the human immunodeficiency virus in Zimbabwe, Central Africa. Trans R Soc Trop Med Hyg 1989; 83 (5) 694-697
  CrossrefPubMedGoogle Scholar
• 48 Campo M, Oursler KK, Huang L , et al. Association of chronic cough and pulmonary function with 6-minute walk test performance in HIV infection. J Acquir Immune Defic Syndr 2014; 65 (5) 557-563
  CrossrefPubMedGoogle Scholar
• 49 Gingo MR, Balasubramani GK, Rice TB , et al. Pulmonary symptoms and diagnoses are associated with HIV in the MACS and WIHS cohorts. BMC Pulm Med 2014; 14: 75
  CrossrefPubMedGoogle Scholar
• 50 Drummond MB, Kirk GD, Ricketts EP , et al. Cross sectional analysis of respiratory symptoms in an injection drug user cohort: the impact of obstructive lung disease and HIV. BMC Pulm Med 2010; 10: 27
  CrossrefPubMedGoogle Scholar
• 51 Rahmanian SD, Wood KL, Lin S , et al. Gender differences in pulmonary function, respiratory symptoms, and macrophage proteomics among HIV-infected smokers. Scientifica (Cairo) 2014; 2014: 613689
  PubMedGoogle Scholar
• 52 Morris A, Gingo MR, George MP , et al. Cardiopulmonary function in individuals with HIV infection in the antiretroviral therapy era. AIDS 2012; 26 (6) 731-740
  CrossrefPubMedGoogle Scholar
• 53 Drummond MB, Kirk GD, Astemborski J , et al. Prevalence and risk factors for unrecognized obstructive lung disease among urban drug users. Int J Chron Obstruct Pulmon Dis 2011; 6: 89-95
  PubMedGoogle Scholar
• 54 Lambert AA, Kirk GD, Astemborski J, Mehta SH, Wise RA, Drummond MB. HIV infection is associated with increased risk for acute exacerbation of COPD. J Acquir Immune Defic Syndr 2015; 69 (1) 68-74
  CrossrefPubMedGoogle Scholar
• 55 Depp TB, Kraemer K, Akgun KM , et al. Risk factors associated with acute exacerbation of chronic obstructive pulmonary disease in HIV-infected and uninfected patients. AIDS 2016; 30 (3) 455-463
  PubMedGoogle Scholar
• 56 Twigg HL, Soliman DM, Day RB , et al. Lymphocytic alveolitis, bronchoalveolar lavage viral load, and outcome in human immunodeficiency virus infection. Am J Respir Crit Care Med 1999; 159 (5, Pt 1): 1439-1444
  CrossrefPubMedGoogle Scholar
• 57 Saetta M, Baraldo S, Corbino L , et al. CD8+ve cells in the lungs of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1999; 160 (2) 711-717
  CrossrefPubMedGoogle Scholar
• 58 Kanner RE, Anthonisen NR, Connett JE ; Lung Health Study Research Group. Lower respiratory illnesses promote FEV(1) decline in current smokers but not ex-smokers with mild chronic obstructive pulmonary disease: results from the lung health study. Am J Respir Crit Care Med 2001; 164 (3) 358-364
  CrossrefPubMedGoogle Scholar
• 59 Morris A, Kingsley LA, Groner G, Lebedeva IP, Beard CB, Norris KA. Prevalence and clinical predictors of Pneumocystis colonization among HIV-infected men. AIDS 2004; 18 (5) 793-798
  CrossrefPubMedGoogle Scholar
• 60 Morris A, Sciurba FC, Lebedeva IP , et al. Association of chronic obstructive pulmonary disease severity and Pneumocystis colonization. Am J Respir Crit Care Med 2004; 170 (4) 408-413
  CrossrefPubMedGoogle Scholar
• 61 Pacht ER, Diaz P, Clanton T, Hart J, Gadek JE. Alveolar fluid glutathione decreases in asymptomatic HIV-seropositive subjects over time. Chest 1997; 112 (3) 785-788
  CrossrefPubMedGoogle Scholar
• 62 Lassiter C, Fan X, Joshi PC , et al. HIV-1 transgene expression in rats causes oxidant stress and alveolar epithelial barrier dysfunction. AIDS Res Ther 2009; 6: 1
  CrossrefPubMedGoogle Scholar
• 63 Dekhuijzen PN, Aben KK, Dekker I , et al. Increased exhalation of hydrogen peroxide in patients with stable and unstable chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996; 154 (3, Pt 1): 813-816
  CrossrefPubMedGoogle Scholar
• 64 Lozupone C, Cota-Gomez A, Palmer BE , et al; Lung HIV Microbiome Project. Widespread colonization of the lung by Tropheryma whipplei in HIV infection. Am J Respir Crit Care Med 2013; 187 (10) 1110-1117
  CrossrefPubMedGoogle Scholar
• 65 Popescu I, Drummond MB, Gama L , et al. Activation-induced cell death drives profound lung CD4(+) T-cell depletion in HIV-associated chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2014; 190 (7) 744-755
  CrossrefPubMedGoogle Scholar
• 66 Liu C, Li B, Li L , et al. Correlations of telomere length, P53 mutation, and chromosomal translocation in soft tissue sarcomas. Int J Clin Exp Pathol 2015; 8 (5) 5666-5673
  PubMedGoogle Scholar
• 67 Lacasse Y, Daigle JM, Martin S, Maltais F. Validity of chronic obstructive pulmonary disease diagnoses in a large administrative database. Can Respir J 2012; 19 (2) e5-e9
  PubMedGoogle Scholar
• 68 Cooke CR, Joo MJ, Anderson SM , et al. The validity of using ICD-9 codes and pharmacy records to identify patients with chronic obstructive pulmonary disease. BMC Health Serv Res 2011; 11: 37
  CrossrefPubMedGoogle Scholar
• 69 Kunisaki KM, Colins G, Nixon DE , et al, the INSIGHT START Pulmonary Substudy Group. Lung function decline in HIV: effects of immediate versus deferred ART treatment on lung function decline in a multisite, international, randomized controlled trial. Antivir Ther 2015; 20 (Suppl. 01) A22
  PubMedGoogle Scholar
• 70 Wallace JM, Stone GS, Browdy BL , et al; Pulmonary Complications of HIV Infection Study Group. Nonspecific airway hyperresponsiveness in HIV disease. Chest 1997; 111 (1) 121-127
  CrossrefPubMedGoogle Scholar
• 71 Poirier CD, Inhaber N, Lalonde RG, Ernst P. Prevalence of bronchial hyperresponsiveness among HIV-infected men. Am J Respir Crit Care Med 2001; 164 (4) 542-545
  CrossrefPubMedGoogle Scholar
• 72 Siberry GK, Leister E, Jacobson DL , et al. Increased risk of asthma and atopic dermatitis in perinatally HIV-infected children and adolescents. Clin Immunol 2012; 142 (2) 201-208
  CrossrefPubMedGoogle Scholar
• 73 Foster SB, Paul ME, Kozinetz CA, Macias CG, Shearer WT. Prevalence of asthma in children and young adults with HIV infection. J Allergy Clin Immunol 2007; 119 (3) 750-752
  CrossrefPubMedGoogle Scholar
• 74 Foster SB, McIntosh K, Thompson B , et al. Increased incidence of asthma in HIV-infected children treated with highly active antiretroviral therapy in the National Institutes of Health Women and Infants Transmission Study. J Allergy Clin Immunol 2008; 122 (1) 159-165
  CrossrefPubMedGoogle Scholar
• 75 Gutin F, Butt A, Alame W, Thomas R, Secord E. Asthma in immune-competent children with human immunodeficiency virus. Ann Allergy Asthma Immunol 2009; 102 (5) 438
  PubMedGoogle Scholar
• 76 Lin RY, Lazarus TS. Asthma and related atopic disorders in outpatients attending an urban HIV clinic. Ann Allergy Asthma Immunol 1995; 74 (6) 510-515
  PubMedGoogle Scholar
• 77 Gingo MR, Wenzel SE, Steele C , et al. Asthma diagnosis and airway bronchodilator response in HIV-infected patients. J Allergy Clin Immunol 2012; 129: 708-14.e8
  CrossrefPubMedGoogle Scholar
• 78 Moorman JE, Akinbami LJ, Bailey CM , et al. National Surveillance of Asthma:United States, 2001–2010. Vital Health Stat 2012; 3 (35) 1-58
  PubMedGoogle Scholar
• 79 Kendall CE, Wong J, Taljaard M , et al. A cross-sectional, population-based study measuring comorbidity among people living with HIV in Ontario. BMC Public Health 2014; 14: 161
  CrossrefPubMedGoogle Scholar
• 80 Moscato G, Maserati R, Marraccini P, Caccamo F, Dellabianca A. Bronchial reactivity to methacholine in HIV-infected individuals without AIDS. Chest 1993; 103 (3) 796-799
  CrossrefPubMedGoogle Scholar
• 81 Israël-Biet D, Labrousse F, Tourani JM, Sors H, Andrieu JM, Even P. Elevation of IgE in HIV-infected subjects: a marker of poor prognosis. J Allergy Clin Immunol 1992; 89 (1, Pt 1): 68-75
  CrossrefPubMedGoogle Scholar
• 82 Kynyk JA, Parsons JP, Para MF, Koletar SL, Diaz PT, Mastronarde JG. HIV and asthma, is there an association?. Respir Med 2012; 106 (4) 493-499
  CrossrefPubMedGoogle Scholar
• 83 Wright DN, Nelson Jr RP, Ledford DK, Fernandez-Caldas E, Trudeau WL, Lockey RF. Serum IgE and human immunodeficiency virus (HIV) infection. J Allergy Clin Immunol 1990; 85 (2) 445-452
  CrossrefPubMedGoogle Scholar
• 84 Corominas M, Garcia JF, Mestre M, Fernández-Viladrich P, Buendia E. Predictors of atopy in HIV-infected patients. Ann Allergy Asthma Immunol 2000; 84 (6) 607-611
  CrossrefPubMedGoogle Scholar
• 85 Puri A, Morris A. Asthma in HIV-infected population: a review of respiratory symptoms, pulmonary function abnormalities and pathophysiology. Epidemiol: Open Access 2014; 4: 1000164
  PubMedGoogle Scholar
• 86 Broide DH, Finkelman F, Bochner BS, Rothenberg ME. Advances in mechanisms of asthma, allergy, and immunology in 2010. J Allergy Clin Immunol 2011; 127 (3) 689-695
  CrossrefPubMedGoogle Scholar
• 87 Holgate ST. Asthma: a simple concept but in reality a complex disease. Eur J Clin Invest 2011; 41 (12) 1339-1352
  CrossrefPubMedGoogle Scholar
• 88 Stacey AR, Norris PJ, Qin L , et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 2009; 83 (8) 3719-3733
  CrossrefPubMedGoogle Scholar
• 89 Barcellini W, Rizzardi GP, Borghi MO, Fain C, Lazzarin A, Meroni PL. TH1 and TH2 cytokine production by peripheral blood mononuclear cells from HIV-infected patients. AIDS 1994; 8 (6) 757-762
  CrossrefPubMedGoogle Scholar
• 90 Clerici M, Shearer GM. A TH1—>TH2 switch is a critical step in the etiology of HIV infection. Immunol Today 1993; 14 (3) 107-111
  CrossrefPubMedGoogle Scholar
• 91 Relucio KI, Beernink HT, Chen D, Israelski DM, Kim R, Holodniy M. Proteomic analysis of serum cytokine levels in response to highly active antiretroviral therapy (HAART). J Proteome Res 2005; 4 (2) 227-231
  CrossrefPubMedGoogle Scholar
• 92 Imami N, Antonopoulos C, Hardy GA, Gazzard B, Gotch FM. Assessment of type 1 and type 2 cytokines in HIV type 1-infected individuals: impact of highly active antiretroviral therapy. AIDS Res Hum Retroviruses 1999; 15 (17) 1499-1508
  CrossrefPubMedGoogle Scholar
• 93 Stokes SC, Tankersley MS. HIV: practical implications for the practicing allergist-immunologist. Ann Allergy Asthma Immunol 2011; 107 (1) 1-9 , quiz 9–11
  CrossrefPubMedGoogle Scholar
• 94 Drummond MB, Dasenbrook EC, Pitz MW, Murphy DJ, Fan E. Inhaled corticosteroids in patients with stable chronic obstructive pulmonary disease: a systematic review and meta-analysis. JAMA 2008; 300 (20) 2407-2416
  CrossrefPubMedGoogle Scholar
• 95 Boyd SD, Hadigan C, McManus M , et al. Influence of low-dose ritonavir with and without darunavir on the pharmacokinetics and pharmacodynamics of inhaled beclomethasone. J Acquir Immune Defic Syndr 2013; 63 (3) 355-361
  CrossrefPubMedGoogle Scholar
• 96 Cui Q, Robinson L, Elston D , et al. Safety and tolerability of varenicline tartrate (Champix(®)/Chantix(®)) for smoking cessation in HIV-infected subjects: a pilot open-label study. AIDS Patient Care STDS 2012; 26 (1) 12-19
  CrossrefPubMedGoogle Scholar
• 97 Vidrine DJ, Marks RM, Arduino RC, Gritz ER. Efficacy of cell phone-delivered smoking cessation counseling for persons living with HIV/AIDS: 3-month outcomes. Nicotine Tob Res 2012; 14 (1) 106-110
  CrossrefPubMedGoogle Scholar
• 98 Ferketich AK, Diaz P, Browning KK , et al. Safety of varenicline among smokers enrolled in the lung HIV study. Nicotine Tob Res 2013; 15 (1) 247-254
  CrossrefPubMedGoogle Scholar
• 99 Humfleet GL, Hall SM, Delucchi KL, Dilley JW. A randomized clinical trial of smoking cessation treatments provided in HIV clinical care settings. Nicotine Tob Res 2013; 15 (8) 1436-1445
  CrossrefPubMedGoogle Scholar
• 100 Shuter J, Morales DA, Considine-Dunn SE, An LC, Stanton CA. Feasibility and preliminary efficacy of a web-based smoking cessation intervention for HIV-infected smokers: a randomized controlled trial. J Acquir Immune Defic Syndr 2014; 67 (1) 59-66
  PubMedGoogle Scholar
• 101 Cropsey KL, Jardin BF, Burkholder GA, Clark CB, Raper JL, Saag MS. An algorithm approach to determining smoking cessation treatment for persons living with HIV/AIDS: results of a pilot trial. J Acquir Immune Defic Syndr 2015; 69 (3) 291-298
  CrossrefPubMedGoogle Scholar