Top

Journal of Cancer Research and Clinical Oncology

Published in:

Open Access 26-11-2023 | Human Immunodeficiency Virus | Research

Mortality due to non-AIDS-defining cancers among people living with HIV in Spain over 18 years of follow-up

Authors: I. Suárez-García, Félix Gutierrez, José A. Pérez-Molina, Santiago Moreno, Teresa Aldamiz, Eulalia Valencia Ortega, Adrián Curran, Sara Gutiérrez González, Víctor Asensi, Concha Amador Prous, Inma Jarrin, Marta Rava, CoRIS

Published in: Journal of Cancer Research and Clinical Oncology | Issue 20/2023

Abstract

Purpose

Our aim was to describe non-AIDS-defining cancer (NADC) mortality among people living with HIV (PLWH), to compare it with that of the general population, and to assess potential risk factors.

Methods

We included antiretroviral-naive PLWH from the multicentre CoRIS cohort (2004–2021). We estimated mortality rates and standardised mortality ratios (SMRs). We used cause-specific Cox models to identify risk factors.

Results

Among 17,978 PLWH, NADC caused 21% of all deaths observed during the follow-up. Mortality rate due to NADC was 1.58 (95%CI 1.36, 1.83) × 1000 person-years and lung and liver were the most frequent cancer-related causes of death. PLWH had 79% excess NADC mortality risk compared to the general population with the highest SMR found for Hodgkin lymphoma, anal and liver cancers. The SMRs decreased with age and were the highest in age groups under 50 years. The most important prognostic factor was low CD4 count, followed by smoking, viral hepatitis and HIV transmission through heterosexual contact or injection drug use.

Conclusion

Non-AIDS cancers are an important cause of death among PLWH. The excess mortality related to certain malignancies and the association with immunodeficiency, smoking, and coinfections highlights the need for early detection and treatment of cancer in this population.

Available only for authorised users

Aldaz P, Moreno-Iribas C, Egüés N et al (2011) Mortality by causes in HIV-infected adults: comparison with the general population. BMC Public Health 11:300. https://doi.org/10.1186/1471-2458-11-300CrossRefPubMedPubMedCentral

Aldridge RW, Nellums LB, Bartlett S et al (2018) Global patterns of mortality in international migrants: a systematic review and meta-analysis. Lancet 392:2553–2566. https://doi.org/10.1016/S0140-6736(18)32781-8CrossRefPubMedPubMedCentral

Alejos B, Hernando V, Iribarren J et al (2016) Overall and cause-specific excess mortality in HIV-positive persons compared with the general population: role of HCV coinfection. Medicine (Baltimore) 95:e4727. https://doi.org/10.1097/MD.0000000000004727CrossRefPubMed

Bonnet F, Lewden C, May T et al (2004) Malignancy-related causes of death in human immunodeficiency virus-infected patients in the era of highly active antiretroviral therapy. Cancer 101:317–324. https://doi.org/10.1002/cncr.20354CrossRefPubMed

Borhade A, Dey S (2018) Do migrants have a mortality advantage? Lancet 392:2517–2518. https://doi.org/10.1016/S0140-6736(18)33052-6CrossRefPubMed

Clifford GM, Polesel J, Rickenbach M et al (2005) Cancer risk in the Swiss HIV cohort study: associations with immunodeficiency, smoking, and highly active antiretroviral therapy. J Natl Cancer Inst 97:425–432. https://doi.org/10.1093/jnci/dji072CrossRefPubMed

Collins LF, Sheth AN, Mehta CC et al (2021) The prevalence and burden of non-AIDS comorbidities among women living with or at risk for human immunodeficiency virus infection in the United States. Clin Infect Dis 72:1301–1311. https://doi.org/10.1093/cid/ciaa204CrossRefPubMed

Corrigan KL, Wall KC, Bartlett JA, Suneja G (2019) Cancer disparities in people with HIV: a systematic review of screening for non-AIDS–defining malignancies. Cancer 125:843–853. https://doi.org/10.1002/cncr.31838CrossRefPubMed

Croxford S, Kitching A, Desai S et al (2017) Mortality and causes of death in people diagnosed with HIV in the era of highly active antiretroviral therapy compared with the general population: an analysis of a national observational cohort. Lancet Public Heal 2:e35–e46. https://doi.org/10.1016/S2468-2667(16)30020-2CrossRef

d’Arminio MA, Abrams D, Pradier C et al (2008) HIV-induced immunodeficiency and mortality from AIDS-defining and non-AIDS-defining malignancies. AIDS 22:2143–2153. https://doi.org/10.1097/QAD.0b013e3283112b77CrossRef

de Lédinghen V, Barreiro P, Foucher J et al (2008) Liver fibrosis on account of chronic hepatitis C is more severe in HIV-positive than HIV-negative patients despite antiretroviral therapy. J Viral Hepat 15:427–433. https://doi.org/10.1111/j.1365-2893.2007.00962.xCrossRefPubMed

Engels EA, Yanik EL, Wheeler W et al (2017) Cancer-attributable mortality among people with treated human immunodeficiency virus infection in North America. Clin Infect Dis 65:636–643. https://doi.org/10.1093/cid/cix392CrossRefPubMedPubMedCentral

Observatorio Español de las Drogas y las Adicciones (2021) Alcohol, tabaco y drogas ilegales en España. Madrid

Fontela C, Aguinaga A, Moreno-Iribas C et al (2020) Trends and causes of mortality in a population-based cohort of HIV-infected adults in Spain: comparison with the general population. Sci Rep 10:8922. https://doi.org/10.1038/s41598-020-65841-0CrossRefPubMedPubMedCentral

Franceschi S, Lise M, Clifford GM et al (2010) Changing patterns of cancer incidence in the early-and late-HAART periods: The Swiss HIV Cohort Study. Br J Cancer 103:416–422. https://doi.org/10.1038/sj.bjc.6605756CrossRefPubMedPubMedCentral

García-Abellán J, del Río L, García JA et al (2019) Risk of cancer in HIV-infected patients in Spain, 2004–2015. The CoRIS cohort study. Enferm Infecc Microbiol Clin. https://doi.org/10.1016/j.eimc.2018.11.011CrossRef

Gueler A, Moser A, Calmy A et al (2017) Life expectancy in HIV-positive persons in Switzerland. AIDS 31:427–436. https://doi.org/10.1097/QAD.0000000000001335CrossRefPubMed

Hernández-Ramírez RU, Shiels MS, Dubrow R, Engels EA (2017) Cancer risk in HIV-infected people in the USA from 1996 to 2012: a population-based, registry-linkage study. Lancet HIV 4:e495–e504. https://doi.org/10.1016/S2352-3018(17)30125-XCrossRefPubMedPubMedCentral

Hernando V, Sobrino-Vegas P, Burriel MC et al (2012) Differences in the causes of death of HIV-positive patients in a cohort study by data sources and coding algorithms. AIDS 26:1829–1834. https://doi.org/10.1097/QAD.0b013e328352ada4CrossRefPubMed

Hessol NA, Ma D, Scheer S et al (2018) Changing temporal trends in non-AIDS cancer mortality among people diagnosed with AIDS: San Francisco, California, 1996–2013. Cancer Epidemiol 52:20–27. https://doi.org/10.1016/j.canep.2017.11.004CrossRefPubMed

Hu J, Liu K, Luo J (2019) HIV–HBV and HIV–HCV Coinfection and Liver Cancer Development. pp 231–250

Izquierdo Miguel R, Rava M, Moreno-García E, et al (2023) HIV medical care interruption among people living with HIV in Spain, 2004–2020. AIDS Publish Ah:2004–2020. https://doi.org/10.1097/QAD.0000000000003552

Leierer G, Rieger A, Schmied B et al (2021) A lower CD4 count predicts most causes of death except cardiovascular deaths. The Austrian HIV Cohort Study. Int J Environ Res Public Health 18:12532. https://doi.org/10.3390/ijerph182312532CrossRefPubMedPubMedCentral

Lewden C, Bouteloup V, De Wit S et al (2012) All-cause mortality in treated HIV-infected adults with CD4 >=500/mm3 compared with the general population: evidence from a large European observational cohort collaboration. Int J Epidemiol 41:433–445. https://doi.org/10.1093/ije/dyr164CrossRefPubMed

López C, Masiá M, Padilla S et al (2016) Muertes por enfermedades no asociadas directamente con el sida en pacientes con infección por el VIH: Un estudio de 14 años (1998–2011). Enferm Infecc Microbiol Clin 34:222–227. https://doi.org/10.1016/j.eimc.2015.04.010CrossRefPubMed

Morgan RL, Baack B, Smith BD et al (2013) Eradication of hepatitis C virus infection and the development of hepatocellular carcinoma. Ann Intern Med 158:329. https://doi.org/10.7326/0003-4819-158-5-201303050-00005CrossRefPubMed

Muñoz Hornero C, Muriel A, Montero M et al (2021) Diferencias epidemiológicas y de mortalidad entre hombres y mujeres con infección por VIH en la cohorte CoRIS entre los años 2004 y 2014. Enferm Infecc Microbiol Clin 39:372–382. https://doi.org/10.1016/j.eimc.2020.05.021CrossRef

Osborn M, Guest J, Rimland D (2007) Hepatitis B virus and HIV coinfection: relationship of different serological patterns to survival and liver disease. HIV Med 8:271–279. https://doi.org/10.1111/j.1468-1293.2007.00469.xCrossRefPubMed

Parka LS, Hernandez-Ramirez RU, Silverberg MJ et al (2016) Prevalence of non-HIV cancer risk factors in persons living with HIV/AIDS: A meta-analysis. AIDS 30:273–291. https://doi.org/10.1097/QAD.0000000000000922CrossRef

Picard A, Badoual C, Hourseau M et al (2016) Human papilloma virus prevalence in HIV patients with head and neck squamous cell carcinoma. AIDS 30:1257–1266. https://doi.org/10.1097/QAD.0000000000001030CrossRefPubMed

Poizot-Martin I, Lions C, Allavena C et al (2021) Spectrum and incidence trends of AIDS- and Non–AIDS-defining cancers between 2010 and 2015 in the French Dat’AIDS Cohort. Cancer Epidemiol Biomarkers Prev 30:554–563. https://doi.org/10.1158/1055-9965.EPI-20-1045CrossRefPubMed

R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

Rava M, Domínguez-Domínguez L, Bisbal O et al (2021) Late presentation for HIV remains a major health issue in Spain: Results from a multicenter cohort study, 2004–2018. PLoS ONE 16:e0249864. https://doi.org/10.1371/journal.pone.0249864CrossRefPubMedPubMedCentral

Shiels MS, Engels EA (2017) Evolving epidemiology of HIV-associated malignancies. Curr Opin HIV AIDS 12:6–11. https://doi.org/10.1097/COH.0000000000000327CrossRefPubMedPubMedCentral

Shiels MS, Copeland G, Goodman MT et al (2015) Cancer stage at diagnosis in patients infected with the human immunodeficiency virus and transplant recipients. Cancer 121:2063–2071. https://doi.org/10.1002/cncr.29324CrossRefPubMed

Shiels MS, Althoff KN, Pfeiffer RM et al (2017) HIV infection, immunosuppression, and age at diagnosis of non-AIDS-defining cancers. Clin Infect Dis 64:468–475. https://doi.org/10.1093/cid/ciw764CrossRefPubMedPubMedCentral

Smith CJ, Ryom L, Weber R et al (2014) Trends in underlying causes of death in people with HIV from 1999 to 2011 (D:A:D): a multicohort collaboration. Lancet 384:241–248. https://doi.org/10.1016/S0140-6736(14)60604-8CrossRefPubMed

Sobrino-Vegas P, Gutiérrez F, Berenguer J et al (2011) La cohorte de la red española de investigación en sida y su biobanco: organización, principales resultados y pérdidas al seguimiento. Enferm Infecc Microbiol Clin 29:645–653. https://doi.org/10.1016/j.eimc.2011.06.002CrossRefPubMed

Sociedad Española de Oncología Médica (2023) Las cifras del cáncer en España 2023. Soc Española Oncol Médica

Suneja G, Shiels MS, Melville SK et al (2013) Disparities in the treatment and outcomes of lung cancer among HIV-infected individuals. AIDS 27:459–468. https://doi.org/10.1097/QAD.0b013e32835ad56eCrossRefPubMed

Suneja G, Lin CC, Simard EP et al (2016) Disparities in cancer treatment among patients infected with the human immunodeficiency virus. Cancer 122:2399–2407. https://doi.org/10.1002/cncr.30052CrossRefPubMed

Tenorio AR, Zheng Y, Bosch RJ et al (2014) Soluble markers of inflammation and coagulation but not T-cell activation predict non-AIDS-defining morbid events during suppressive antiretroviral treatment. J Infect Dis 210:1248–1259. https://doi.org/10.1093/infdis/jiu254CrossRefPubMedPubMedCentral

Trickey A, May MT, Vehreschild J et al (2016) Cause-specific mortality in HIV-positive patients who survived ten years after starting antiretroviral therapy. PLoS One 11:e0160460. https://doi.org/10.1371/journal.pone.0160460CrossRefPubMedPubMedCentral

Weber R, Ruppik M, Rickenbach M et al (2013) Decreasing mortality and changing patterns of causes of death in the Swiss HIV Cohort Study. HIV Med 14:195–207. https://doi.org/10.1111/j.1468-1293.2012.01051.xCrossRefPubMed

Yuan T, Hu Y, Zhou X, et al (2022) Incidence and mortality of non-AIDS-defining cancers among people living with HIV: a systematic review and meta-analysis. eClinicalMedicine 52:101613. https://doi.org/10.1016/j.eclinm.2022.101613

Zwahlen M, Harris R, May M et al (2009) Mortality of HIV-infected patients starting potent antiretroviral therapy: comparison with the general population in nine industrialized countries. Int J Epidemiol 38:1624–1633. https://doi.org/10.1093/ije/dyp306CrossRefPubMed

Title: Mortality due to non-AIDS-defining cancers among people living with HIV in Spain over 18 years of follow-up
Authors: I. Suárez-García
Félix Gutierrez
José A. Pérez-Molina
Santiago Moreno
Teresa Aldamiz
Eulalia Valencia Ortega
Adrián Curran
Sara Gutiérrez González
Víctor Asensi
Concha Amador Prous
Inma Jarrin
Marta Rava
CoRIS
Publication date: 26-11-2023
Publisher: Springer Berlin Heidelberg
Keyword: Human Immunodeficiency Virus
Published in: Journal of Cancer Research and Clinical Oncology / Issue 20/2023
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI: https://doi.org/10.1007/s00432-023-05500-9

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 20/2023

Assessing the risk of venous thromboembolism in patients with haematological cancers using three prediction models

Proposal of a diagnostic algorithm for radiation-induced dropped head syndrome in long-term childhood cancer survivors based on a prospective study in a specialized clinical setting and a review of the literature

A self-supervised classification model for endometrial diseases

Combining immunotherapy and radiotherapy in esophageal cancer

Construction of an EMT-related lncRNA prognostic signature for lung adenocarcinoma and functional verification of its hub gene LINC01615

Intratumoral delivery of a Tim-3 antibody-encoding oncolytic adenovirus engages an effective antitumor immune response in liver cancer

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials