HIV/AIDS, tuberculosis (TB), and tobacco use are three important global health challenges. These epidemics act independently but also collectively, amplifying the health impacts of each. This synergism of diseases is termed “syndemic” ¹1. Singer M, Clair S. Syndemics and public health: Reconceptualizing disease in bio-social context. Med Anthropol Q 2003; 7:423-41.. These three epidemics are usually approached through separate programs led by infectologists, pulmonologists, and behavioralists, respectively. The social determinants of disease, including poverty, low-education, high population-density, and cultural norms, are common to all three. The syndemic also challenges health systems and suggests that a systems-based approach may improve disease outcomes as well as practices.

There is evidence supporting linkages between HIV/AIDS, TB, and tobacco use. TB disease, mortality, and recurrent TB are associated with smoking ²2. U.S. Department of Health and Human Services. The health consequences of smoking: 50 years of progress. A report of the Surgeon General. Atlanta: U.S. Department of Health and Human Services; 2014.. Smoking increases risk for latent TB infection (LTBI), progression to active disease, delayed sputum conversion, default from treatment, relapse, and drug resistance. Second-hand smoke may also increase risk of TB within households.

TB is the most important opportunistic infection for persons living with HIV/AIDS. HIV/AIDS is a risk factor for poor TB treatment outcomes and higher TB mortality ³3. Van Rie A, Westreich D, Sanne I. Tuberculosis in patients receiving antiretroviral treatment: incidence, risk factors, and prevention strategies. J Acquir Immune Defic Syndr 2011; 56:349-55.. Persons living with TB have 1.6 times greater risk of progressing to AIDS and were 2 times more likely to die compared with TB negatives ⁴4. Badri M, Ehrlich R, Wood R, Pulerwitz T, Maartens G. Association between tuberculosis and HIV disease progression in a high tuberculosis prevalence area. Int J Tuberc Lung Dis 2001; 5:225-32.. TB also increases HIV replication due to activation of latent virus in macrophages and T-lymphocytes and is associated with reduced CD4+ counts ⁵5. Mihret A, Abebe M, Bekele Y, Aseffa A, Walzl G, Howe R. Impact of HIV co-infection on plasma level of cytokines and chemokines of pulmonary tuberculosis patients. BMC Infect Dis 2014; 14:125.. In a Danish cohort, more than 60% of HIV/AIDS deaths were associated with smoking ⁶6. Helleberg M, Afzal S, Kronborg G, Larsen CS, Pedersen G, Pedersen C, et al. Mortality attributable to smoking among HIV-1-infected individuals: a nationwide, population-based cohort study. Clin Infect Dis 2013; 56:727-34.. Smoking among Persons living with HIV/AIDS increases risks for pneumonia ⁷7. Shirley DK, Kesari RK, Glesby MJ. Factors associated with smoking in HIV-infected patients and potential barriers to cessation. AIDS Patient Care STDS 2013; 27:604-12. as well as for oropharyngeal diseases ⁸8. Chattopadhyay A, Caplan DJ, Slade GD, Shugars DC, Tien HC, Patton LL. Risk indicators for oral candidiasis and oral hairy leukoplakia in HIV-infected adults. Community Dent Oral Epidemiol 2005; 33:35-44.. Smoking also increases risks for cardiovascular disease, dyslipidemia, insulin resistance, and chronic lung disease among persons living with HIV/AIDS ⁹9. De Socio GLV, Martinelli L, Morosi S, Fiori M, Roscini AR, Stagni G, et al. Is estimated cardiovascular risk higher in HIV-infected patients than in the general population? Scand J Infect Dis 2007; 39:805-12.. Nicotine has modulating effects on immune systems ¹⁰10. Sopori ML, Razani-Boroujerdi S, Singh SP. Immunomodulatory effects of cigarette smoke/nicotine. In: Friedman H, Klein TW, Bendinelli M, editors. Infectious diseases and substance abuse. New York: Springer; 2005. p. 103-9..

Three intersecting epidemics in Brazil

HIV/AIDS, TB, and tobacco are significant health challenges for Brazil, together accounting for 150,000 annual deaths ¹¹11. Torres TS, Luz PM, Derrico M, Velasque L, Grinsztejn E, Veloso VG. Factors associated with tobacco smoking and cessation among HIV-infected individuals under care in Rio de Janeiro, Brazil. PLoS One 2014; 9:e115900.. In 2013, there were 93,000 new TB and 760,000 new HIV cases, with 13,000 co-infected ¹²12. The Joint United Nations Programme on HIV/AIDS. UNAIDS country data profile: Brazil. http://www.unaids.org/sites/default/files/epidocuments/BRA.pdf (acessado em 23/Jul/2015).
http://www.unaids.org/sites/default/file... ^,1313. World Health Organization. Tuberculosis country profile: Brazil. https://extranet.who.int/sree/Reports?op=Replet&name=%2FWHO_HQ_Reports%2FG2%2FPROD%2FEXT%2FTBCountryProfile&ISO2=BR&LAN=EN&outtype=html (acessado em 21/Jul/2015).
https://extranet.who.int/sree/Reports?op... . Expanded HIV diagnosis among TB patients is a priority in Brazil, and in 2013, 70% knew their HIV status compared with 31% in 2003 ¹⁴14. Tuberculose: circulando a informação. http://blogdatuberculose.blogspot.com.br/p/acervo.html (acessado em 27/Jul/2015).
http://blogdatuberculose.blogspot.com.br... .

Tobacco use is still a concern in Brazil, with 15% current adult smoking in 2013 and higher prevalence among those with lowest education (20.2%) ¹⁵15. Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional de Saúde 2013: percepção do estado de saúde, estilos de vida e doenças crônicas, Brasil. http://biblioteca.ibge.gov.br/visualizacao/livros/liv91110.pdf (acessado em 23/Jul/2015).
http://biblioteca.ibge.gov.br/visualizac... . A recent cohort study found that after controlling for socioeconomic status, smokers had 2.5 greater risk for recurrent TB compared to non-smokers and that smokers were more likely to default on TB treatment ¹⁶16. Cavalcante SC, Saraceni V, Cohn S, Soares ECC, Barnes GL, Golub JE, et al. Tuberculosis and smoking among patients entering a DOTS program in Rio de Janeiro city, Brazil. Int J Tuberc Lung Dis 2010; 14(11Suppl 2):S177.. A 2014 Brazilian cohort study of 2,775 persons living with HIV/AIDS found 29.9% current smokers and 23.9% former smokers ¹⁰10. Sopori ML, Razani-Boroujerdi S, Singh SP. Immunomodulatory effects of cigarette smoke/nicotine. In: Friedman H, Klein TW, Bendinelli M, editors. Infectious diseases and substance abuse. New York: Springer; 2005. p. 103-9.. Current smokers were more likely to be less educated; to use alcohol, crack, and cocaine; and to be hospitalized for co-existing conditions.

A syndemic approach

Traditional public health approaches usually involve single programs that do not address interactions of risks or diseases. A syndemic approach to HIV/AIDS and TB should integrate tobacco control in the care of patients with these conditions. At a minimum, improved overall health can be expected as a result of smoking cessation. A more comprehensive approach to the social determinants of tobacco use may also reduce combined effects of TB and HIV/AIDS.

New diagnoses of TB or HIV/AIDS are critical events for patients and could be linked to tobacco interventions. Newly diagnosed TB patients receive directly observed treatment short-course (DOTS), a patient-centered case management approach that requires regular provider contact for six months. This represents an opportunity to address tobacco use among patients and families. Similarly, patients diagnosed with HIV/AIDS and taking anti-retroviral treatment (ART) need significant clinical support to adhere to ART; they may be especially receptive to health interventions such as smoking cessation.

There have been multiple pilot studies on TB and cessation, including in Brazil ¹⁷17. Sereno AB, Soares ECC, Lapa e Silva JR, Nápoles AM, Bialous SA, Costa e Silva VL, et al. Feasibility study of a smoking cessation intervention in Directly Observed Therapy Short-Course tuberculosis treatment clinics in Rio de Janeiro, Brazil. Rev Panam Salud Publica 2012; 32:451-6., with randomized trials in Pakistan ¹⁸18. Siddiqi K, Khan A, Ahmad M, Dogar O, Kanaan M, Newell JN, et al. Action to stop smoking in suspected tuberculosis (ASSIST) in Pakistan: a cluster randomized, controlled trial. Ann Intern Med 2013; 158:667-75. and South Africa ¹⁹19. Louwagie GM, Okuyemi KS, Ayo-Yusuf OA. Efficacy of brief motivational interviewing on smoking cessation at tuberculosis clinics in Tshwane, South Africa: a randomized controlled trial. Addiction 2014; 109:1942-52.. Brief advice and motivational interviewing were effective in reducing smoking among TB patients. A 2014 review of cessation interventions among persons living with HIV/AIDS indicated that these must take into account social context, mental health, and other risk behaviors. Multiple, varied interventions delivered consistently over time were most successful ²⁰20. Moscou-Jackson G, Commodore-Mensah Y, Farley J, DiGiacomo M. Smoking-cessation interventions in people living with HIV infection: a systematic review. J Assoc Nurses AIDS Care 2014; 25:32-45..

Conclusion

There is sufficient evidence that TB, HIV/AIDS, and tobacco use create synergistic disease burdens. Persons with TB and HIV/AIDS who use tobacco may not access health care or social supports necessary for health behavior change. They may not understand the impacts of tobacco use on their infectious diseases, and social norms may facilitate health risk behaviors. Add to this the impacts of poverty, dietary insufficiency, and crowding, and then the challenges to providing comprehensive care become clear. These factors may be best addressed using a systems-based approach.

Brazil has implemented effective TB and HIV/AIDS programs. These may be able to integrate low-cost tobacco control interventions, including cessation services, community participation, and outreach that can reduce tobacco use. To implement integrated tobacco control within TB and HIV/AIDS programs, context-specific research and guidelines are needed. Policies that increase the price of cigarettes, reduce access to tobacco products, support smoke-free homes and workplaces, publicize risks of tobacco use for TB and HIV/AIDS, and mandate cessation counseling in DOTS and ART programs could impact the health of affected populations. However, potential barriers and limitations include: gaining political authority to change policy with DOTS and ART programs; engaging infectologists in the relevance of tobacco control; and involving communities and families in a collective approach to tobacco use among affected patients. Nonetheless, the benefits of a syndemic approach to patients suffering from these conditions would likely far outweigh costs of implementation.

Research to test integration of tobacco control within TB and HIV/AIDS programs should involve the Family Health System in Brazil. In this system, geographically-based Family Medicine teams involving physicians, nurses, practical nurses, and agentes (community health workers) provide comprehensive care to targeted communities. These teams can integrate care for multiple diseases and address community health. Brazil has prioritized tobacco control as a national objective, with notable success in the reduction of smoking prevalence from approximately 35% among adults in 1989 to 15% in 2013 ¹⁵15. Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional de Saúde 2013: percepção do estado de saúde, estilos de vida e doenças crônicas, Brasil. http://biblioteca.ibge.gov.br/visualizacao/livros/liv91110.pdf (acessado em 23/Jul/2015).
http://biblioteca.ibge.gov.br/visualizac... . This bodes well for an integrated approach to tobacco use among populations affected by TB and HIV/AIDS. However, these populations will need more than simple behavioral therapy to become smoke-free (Figure 1).

Acknowledgments

The authors sincerely thank Dr. Valeska Carvalho Figueiredo, Coordinator and Researcher at the Research Center on Smoking and Health (CETAB) of the Serigio Arouca National School of Public Health, Oswaldo Cruz Foundation (ENSP/Fiocruz) and Dr. Valdiléa Veloso, research scientist at the Evandro Chagas National Institute of Infectious Diseases (INI/Fiocruz) for their contributions to this Perspective.

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