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HIV Infection, Pulmonary Tuberculosis, and COPD in Rural Uganda: A Cross-Sectional Study

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Abstract

Purpose

HIV is associated with chronic obstructive pulmonary disease (COPD) in high resource settings. Similar relationships are less understood in low resource settings. We aimed to estimate the association between HIV infection, tuberculosis, and COPD in rural Uganda.

Methods

The Uganda Non-communicable Diseases and Aging Cohort study observes people 40 years and older living with HIV (PLWH) on antiretroviral therapy, and population-based HIV-uninfected controls in rural Uganda. Participants completed respiratory questionnaires and post-bronchodilator spirometry.

Results

Among 269 participants with spirometry, median age was 52 (IQR 48–55), 48% (n = 130) were ever-smokers, and few (3%, n = 9) reported a history of COPD or asthma. All participants with prior tuberculosis (7%, n = 18) were PLWH. Among 143 (53%) PLWH, median CD4 count was 477 cells/mm3 and 131 (92%) were virologically suppressed. FEV1 was lower among older individuals (− 0.5%pred/year, 95% CI 0.2–0.8, p < 0.01) and those with a history of tuberculosis (− 14.4%pred, 95% CI − 23.5 to − 5.3, p < 0.01). COPD was diagnosed in 9 (4%) participants, eight of whom (89%) were PLWH, six of whom (67%) had a history of tuberculosis, and all of whom (100%) were men. Among 287 participants with complete symptom questionnaires, respiratory symptoms were more likely among women (AOR 3.9, 95% CI 2.0–7.7, p < 0.001) and those in homes cooking with charcoal (AOR 3.2, 95% CI 1.4–7.4, p = 0.008).

Conclusion

In rural Uganda, COPD may be more prevalent among PLWH, men, and those with prior tuberculosis. Future research is needed to confirm these findings and evaluate their broader impacts on health.

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References

  1. GBD 2013 Mortality and Causes of Death Collaborators (2015) Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 385(9963):117–171. https://doi.org/10.1016/S0140-6736(14)61682-2

    Article  Google Scholar 

  2. Diaz-Guzman E, Mannino DM (2014) Epidemiology and prevalence of chronic obstructive pulmonary disease. Clin Chest Med 35(1):7–16. https://doi.org/10.1016/j.ccm.2013.10.002

    Article  PubMed  Google Scholar 

  3. Eisner MD, Anthonisen N, Coultas D et al (2010) An official American Thoracic Society public policy statement: novel risk factors and the global burden of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 182(5):693–718. https://doi.org/10.1164/rccm.200811-1757ST

    Article  PubMed  Google Scholar 

  4. Fourm of Interntational Respiratory Societies (2013) Respiratory diseases in the world: realities of today—opportunities for tomorrow. https://www.ersnet.org/pdf/publications/firs-world-report.pdf

  5. Drummond MB, Huang L, Diaz PT et al (2015) Factors associated with abnormal spirometry among HIV-infected individuals. AIDS 29(13):1691–1700. https://doi.org/10.1097/QAD.0000000000000750

    Article  PubMed  PubMed Central  Google Scholar 

  6. Crothers K, Butt AA, Gibert CL et al (2006) Increased COPD among HIV-positive compared to HIV-negative veterans. Chest 130(5):1326–1333. https://doi.org/10.1378/chest.130.5.1326

    Article  PubMed  Google Scholar 

  7. Crothers K, Huang L, Goulet JL et al (2011) HIV infection and risk for incident pulmonary diseases in the combination antiretroviral therapy era. Am J Respir Crit Care Med 183(3):388–395. https://doi.org/10.1164/rccm.201006-0836OC

    Article  PubMed  PubMed Central  Google Scholar 

  8. Drummond MB, Merlo CA, Astemborski J et al (2013) The effect of HIV infection on longitudinal lung function decline among IDUs: a prospective cohort. AIDS 27(8):1303–1311. https://doi.org/10.1097/QAD.0b013e32835e395d

    Article  PubMed  PubMed Central  Google Scholar 

  9. George MP, Kannass M, Huang L et al (2009) Respiratory symptoms and airway obstruction in HIV-infected subjects in the HAART era. PLoS ONE 4(7):e6328. https://doi.org/10.1371/journal.pone.0006328

    Article  PubMed  PubMed Central  Google Scholar 

  10. Drummond MB, Kirk GD, Astemborski J et al (2012) Association between obstructive lung disease and markers of HIV infection in a high-risk cohort. Thorax 67(4):309–314. https://doi.org/10.1136/thoraxjnl-2011-200702

    Article  PubMed  Google Scholar 

  11. Risso K, Guillouet-de-Salvador F, Valerio L et al (2017) COPD in HIV-infected patients: CD4 cell count highly correlated. PLoS ONE 12(1):e0169359. https://doi.org/10.1371/journal.pone.0169359

    Article  PubMed  PubMed Central  Google Scholar 

  12. van Zyl Smit RN, Pai M, Yew WW et al (2010) Global lung health: the colliding epidemics of tuberculosis, tobacco smoking, HIV and COPD. Eur Respir J 35(1):27–33. https://doi.org/10.1183/09031936.00072909

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ferris BG (1978) Epidemiology standardization project (American Thoracic Society). Am Rev Respir Dis 118(6 Pt 2):1–120

    CAS  PubMed  Google Scholar 

  14. Filmer D, Pritchett LH (2001) Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography 38(1):115–132

    CAS  PubMed  Google Scholar 

  15. WHO STEPwise approach to noncommunicable disease risk factor surveillance (STEPS). http://www.who.int/chp/steps/riskfactor/en/

  16. Miller MR, Hankinson J, Brusasco V et al (2005) Standardisation of spirometry. Eur Respir J 26(2):319–338. https://doi.org/10.1183/09031936.05.00034805

    Article  CAS  PubMed  Google Scholar 

  17. Hankinson JL, Odencrantz JR, Fedan KB (1999) Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med 159(1):179–187. https://doi.org/10.1164/ajrccm.159.1.9712108

    Article  CAS  PubMed  Google Scholar 

  18. Musafiri S, van Meerbeeck JP, Musango L et al (2013) Spirometric reference values for an East-African population. Respiration 85(4):297–304. https://doi.org/10.1159/000337256

    Article  PubMed  Google Scholar 

  19. Pellegrino R, Viegi G, Brusasco V et al (2005) Interpretative strategies for lung function tests. Eur Respir J 26(5):948–968. https://doi.org/10.1183/09031936.05.00035205

    Article  CAS  PubMed  Google Scholar 

  20. Vestbo J, Hurd SS, Agusti AG et al (2013) Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 187(4):347–365. https://doi.org/10.1164/rccm.201204-0596PP

    Article  CAS  PubMed  Google Scholar 

  21. Pefura-Yone EW, Fodjeu G, Kengne AP et al (2015) Prevalence and determinants of chronic obstructive pulmonary disease in HIV infected patients in an African country with low level of tobacco smoking. Respir Med 109(2):247–254. https://doi.org/10.1016/j.rmed.2014.12.003

    Article  PubMed  Google Scholar 

  22. Akanbi MO, Taiwo BO, Achenbach CJ et al. (2015) HIV associated chronic obstructive pulmonary disease in Nigeria. J AIDS Clin Res. https://doi.org/10.4172/2155-6113.1000453

    PubMed  PubMed Central  Google Scholar 

  23. Meghji J, Nadeau G, Davis KJ et al (2016) Noncommunicable lung disease in Sub-Saharan Africa. A community-based cross-sectional study of adults in urban Malawi. Am J Respir Crit Care Med 194(1):67–76. https://doi.org/10.1164/rccm.201509-1807OC

    Article  PubMed  PubMed Central  Google Scholar 

  24. Gingo MR, Morris A, Crothers K (2013) Human immunodeficiency virus-associated obstructive lung diseases. Clin Chest Med 34(2):273–282. https://doi.org/10.1016/j.ccm.2013.02.002

    Article  PubMed  PubMed Central  Google Scholar 

  25. Amaral AF, Coton S, Kato B et al (2015) Tuberculosis associates with both airflow obstruction and low lung function: BOLD results. Eur Respir J 46(4):1104–1112. https://doi.org/10.1183/13993003.02325-2014

    Article  PubMed  PubMed Central  Google Scholar 

  26. Fitzpatrick ME, Singh V, Bertolet M et al (2014) Relationships of pulmonary function, inflammation, and T-cell activation and senescence in an HIV-infected cohort. AIDS 28(17):2505–2515. https://doi.org/10.1097/QAD.0000000000000471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Fitzpatrick ME, Nouraie M, Gingo MR et al (2016) Novel relationships of markers of monocyte activation and endothelial dysfunction with pulmonary dysfunction in HIV-infected persons. AIDS 30(9):1327–1339. https://doi.org/10.1097/QAD.0000000000001092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lassiter C, Fan X, Joshi PC et al (2009) HIV-1 transgene expression in rats causes oxidant stress and alveolar epithelial barrier dysfunction. AIDS Res Ther 6:1. https://doi.org/10.1186/1742-6405-6-1

    Article  PubMed  PubMed Central  Google Scholar 

  29. Neff CP, Chain JL, MaWhinney S et al (2015) Lymphocytic alveolitis is associated with the accumulation of functionally impaired HIV-specific T cells in the lung of antiretroviral therapy-naive subjects. Am J Respir Crit Care Med 191(4):464–473. https://doi.org/10.1164/rccm.201408-1521OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jia H, Lohr M, Jezequel S et al (2001) Cysteine-rich and basic domain HIV-1 Tat peptides inhibit angiogenesis and induce endothelial cell apoptosis. Biochem Biophy Res Commun 283(2):469–479. https://doi.org/10.1006/bbrc.2001.4790

    Article  CAS  Google Scholar 

  31. Morris A, Alexander T, Radhi S et al (2009) Airway obstruction is increased in pneumocystis-colonized human immunodeficiency virus-infected outpatients. J Clin Microbiol 47(11):3773–3776. https://doi.org/10.1128/JCM.01712-09

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kristoffersen US, Lebech AM, Mortensen J et al (2012) Changes in lung function of HIV-infected patients: a 4.5-year follow-up study. Clin Physiol Funct Imaging 32(4):288–295. https://doi.org/10.1111/j.1475-097X.2012.01124.x

    Article  PubMed  Google Scholar 

  33. Gingo MR, George MP, Kessinger CJ et al (2010) Pulmonary function abnormalities in HIV-infected patients during the current antiretroviral therapy era. Am J Respir Crit Care Med 182(6):790–796. https://doi.org/10.1164/rccm.200912-1858OC

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kunisaki KM, Niewoehner DE, Collins G et al (2016) Pulmonary effects of immediate versus deferred antiretroviral therapy in HIV-positive individuals: a nested substudy within the multicentre, international, randomised, controlled strategic timing of antiretroviral treatment (START) trial. Lancet Respir Med 4(12):980–989. https://doi.org/10.1016/S2213-2600(16)30319-8

    Article  PubMed  PubMed Central  Google Scholar 

  35. Siedner MJ, Ng CK, Bassett IV et al (2015) Trends in CD4 count at presentation to care and treatment initiation in sub-Saharan Africa, 2002–2013: a meta-analysis. Clin Infect Dis 60(7):1120–1127. https://doi.org/10.1093/cid/ciu1137

    PubMed  Google Scholar 

  36. Boum Y, 2nd, Atwine D, Orikiriza P et al. (2014) Male Gender is independently associated with pulmonary tuberculosis among sputum and non-sputum producers people with presumptive tuberculosis in Southwestern Uganda. BMC Infect Dis 14:638. https://doi.org/10.1186/s12879-014-0638-5

    Article  PubMed  PubMed Central  Google Scholar 

  37. Borgdorff MW, Nagelkerke NJ, Dye C et al (2000) Gender and tuberculosis: a comparison of prevalence surveys with notification data to explore sex differences in case detection. Int J Tuberc Lung Dis 4(2):123–132

    CAS  PubMed  Google Scholar 

  38. Hamid Salim MA, Declercq E, Van Deun A et al (2004) Gender differences in tuberculosis: a prevalence survey done in Bangladesh. Int J Tuberc Lung Dis 8(8):952–957

    CAS  PubMed  Google Scholar 

  39. Neyrolles O, Quintana-Murci L (2009) Sexual inequality in tuberculosis. PLoS Med 6(12):e1000199. https://doi.org/10.1371/journal.pmed.1000199

    Article  PubMed  PubMed Central  Google Scholar 

  40. van Gemert F, Kirenga B, Chavannes N et al (2015) Prevalence of chronic obstructive pulmonary disease and associated risk factors in Uganda (FRESH AIR Uganda): a prospective cross-sectional observational study. Lancet Glob Health 3(1):e44–e51. https://doi.org/10.1016/S2214-109X(14)70337-7

    Article  PubMed  Google Scholar 

  41. Buist AS, McBurnie MA, Vollmer WM et al (2007) International variation in the prevalence of COPD (the BOLD Study): a population-based prevalence study. Lancet 370(9589):741–750. https://doi.org/10.1016/S0140-6736(07)61377-4

    Article  PubMed  Google Scholar 

  42. Adeloye D, Basquill C, Papana A et al (2015) An estimate of the prevalence of COPD in Africa: a systematic analysis. COPD 12(1):71–81. https://doi.org/10.3109/15412555.2014.908834

    Article  PubMed  Google Scholar 

  43. Pinkerton KE, Harbaugh M, Han MK et al (2015) Women and lung disease. Sex differences and global health disparities. Am J Respir Crit Care Med 192(1):11–16. https://doi.org/10.1164/rccm.201409-1740PP

    Article  PubMed  PubMed Central  Google Scholar 

  44. Hardin M, Cho MH, Sharma S et al (2017) Sex-based genetic association study identifies CELSR1 as a possible chronic obstructive pulmonary disease risk locus among women. Am J Respir Cell Mol Biol 56(3):332–341. https://doi.org/10.1165/rcmb.2016-0172OC

    Article  CAS  PubMed  Google Scholar 

  45. Wan ES, Qiu W, Carey VJ et al (2015) Smoking-associated site-specific differential methylation in buccal mucosa in the COPDGene study. Am J Respir Cell Mol Biol 53(2):246–254. https://doi.org/10.1165/rcmb.2014-0103OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Amaral AFS, Strachan DP, Burney PGJ et al (2017) Female smokers are at greater risk of airflow obstruction than male smokers. UK biobank. Am J Respir Crit Care Med 195(9):1226–1235. https://doi.org/10.1164/rccm.201608-1545OC

    Article  PubMed  Google Scholar 

  47. Kruse GR, Bangsberg DR, Hahn JA et al (2014) Tobacco use among adults initiating treatment for HIV infection in rural Uganda. AIDS Behav 18(7):1381–1389. https://doi.org/10.1007/s10461-014-0737-8

    Article  PubMed  PubMed Central  Google Scholar 

  48. Pampel F (2008) Tobacco use in sub-Sahara Africa: estimates from the demographic health surveys. Soc Sci Med 66(8):1772–1783. https://doi.org/10.1016/j.socscimed.2007.12.003

    Article  PubMed  PubMed Central  Google Scholar 

  49. Mills EJ, Bakanda C, Birungi J et al (2011) Life expectancy of persons receiving combination antiretroviral therapy in low-income countries: a cohort analysis from Uganda. Ann Intern Med 155(4):209–216. https://doi.org/10.7326/0003-4819-155-4-201108160-00358

    Article  PubMed  Google Scholar 

  50. Nsanzimana S, Remera E, Kanters S et al (2015) Life expectancy among HIV-positive patients in Rwanda: a retrospective observational cohort study. Lancet Glob Health 3(3):e169–e177. https://doi.org/10.1016/S2214-109X(14)70364-X

    Article  PubMed  Google Scholar 

  51. Bor J, Herbst AJ, Newell ML et al (2013) Increases in adult life expectancy in rural South Africa: valuing the scale-up of HIV treatment. Science 339(6122):961–965. https://doi.org/10.1126/science.1230413

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Uganda Non-communicable Diseases and Aging Cohort study participants who made this study possible by participating in this work; and Sheila Abaasabyoona, Zulaika Namboga, Doreen Kyomuhendo, Alan Babweteera, and members of the HopeNet Study team for research assistance. No endorsement of manuscript contents or conclusions should be inferred from these acknowledgements.

Funding

This study was funded by the U.S. National Institutes of Health R21HL124712, P30AI060354, P30ES000002, R24AG044325, R25TW009337, and Friends of a Healthy Uganda. The authors acknowledge the following additional sources of support: T32HL116275, K23MH096620, and K23MH099916. Travel support for study investigators was provided by the travel award programs of Massachusetts General Hospital Global Health and the Partners Center of Expertise in Global and Humanitarian Health. Biostatistical consultation was provided with support from Harvard Catalyst, the Harvard Clinical and Translational Science Center (UL1TR001102) and financial contributions from Harvard University and its affiliated academic healthcare centers. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Harvard Catalyst, Harvard University, and its affiliated academic healthcare centers, or the National Institutes of Health.

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Correspondence to Crystal M. North.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional an/or national research committee and with the 1964 Helsinki declation and its later amendemnts or comparable ethical standards.

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North, C.M., Allen, J.G., Okello, S. et al. HIV Infection, Pulmonary Tuberculosis, and COPD in Rural Uganda: A Cross-Sectional Study. Lung 196, 49–57 (2018). https://doi.org/10.1007/s00408-017-0080-8

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