Impact of the COVID-19 Pandemic on Mortality among Patients with TB–HIV Coinfection in the Brazilian Amazon: A Case–Control Study

Lucilaide Oliveira Santos; Filipe Anibal Carvalho-Costa; Maria Graciede Filha Santarém Andrade; Maria do Socorro Guimarães de Souza; Nestor Cordeiro dos Santos Neto; Valdete Santos de Araújo; Flor Ernestina Martinez Espinosa; Martha Cecilia Suarez-Mutis

doi:10.1590/SciELOPreprints.12636

##article.authors##

Lucilaide Oliveira Santos Oswaldo Cruz Foundation https://orcid.org/0009-0008-2261-1810
Filipe Anibal Carvalho-Costa Oswaldo Cruz Foundation https://orcid.org/0009-0007-7434-0680
Maria Graciede Filha Santarém Andrade Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Diretoria de Assistência Médica, Gerência de Ambulatório, Manaus, AM, Brasil; Fundação de Vigilância em Saúde do Amazonas Dra. Rosemary Costa Pinto, Centro de Referência para Imunobiológicos Especiais, Manaus, AM, Brasil https://orcid.org/0009-0008-5873-2964
Maria do Socorro Guimarães de Souza Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Diretoria de Assistência Médica, Gerência de Ambulatório, Manaus, AM, Brasil https://orcid.org/0009-0001-1901-3827
Nestor Cordeiro dos Santos Neto Hospital de Messejana Dr. Carlos Alberto Studart Gomes, Serviço de Terapia Intensiva, Fortaleza, CE, Brasil https://orcid.org/0009-0003-9099-9224
Valdete Santos de Araújo Universidade Nilton Lins, Curso de Medicina, Disciplina de Doenças Infecciosas e Parasitárias, Manaus, AM, Brasil; Universidade Estadual do Amazonas, Coordenação de Engenharia Civil, Manaus, AM, Brasil https://orcid.org/0000-0002-8683-9813
Flor Ernestina Martinez Espinosa Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Diretoria de Ensino e Pesquisa, Gerência de Malária, Manaus, AM, Brasil ; Fundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Laboratório Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, Brasil; https://orcid.org/0000-0002-0325-3674
Martha Cecilia Suarez-Mutis Oswaldo Cruz Foundation https://orcid.org/0000-0003-2809-6799

DOI:

https://doi.org/10.1590/SciELOPreprints.12636

Keywords:

TB-HIV-COVID19, Syndemic, Mortality, Brazilian Amazon, Case-Control

Abstract

Background: The COVID-19 pandemic disrupted healthcare services worldwide, potentially worsening outcomes for individuals with chronic infectious diseases, including tuberculosis (TB) and HIV.
Objective: To identify factors associated with mortality among patients with TB–HIV co-infection, and to assess the impact of the COVID-19 pandemic on these outcomes.
Methods: Methods: We analyzed 3,352 TB-HIV cases treated at a referral center in Amazonas, Brazil (2014-2022). Two case-control analyses compared TB-related and non-TB-related deaths with cured TB patients. Multivariate logistic regression was used to identify independent risk factors
Results: In TB-related death group, predictors included diagnosis during the COVID-19 pandemic, rural residence, disseminated TB, prior TB treatment, CD4+ <200, and HAART initiation at or after TB diagnosis. Non-TB deaths were associated with age >60, homelessness, disseminated TB, prior treatment, low CD4+, high viral load, and delayed or absent HAART. Both groups reflected advanced disease, immunosuppression, and poor treatment access.
Conclusions: The pandemic increased TB-related mortality but not non-TB deaths. Mortality was also driven by disease severity, delayed care, and social vulnerability, with rural residence highlighting healthcare barriers. Tackling the TB–HIV–COVID-19 syndemic demands integrated, context-sensitive strategies targeting biological, social, and structural determinants to reduce mortality and improve outcomes in high-burden, resource-limited settings.

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Author Biographies

Lucilaide Oliveira Santos, Oswaldo Cruz Foundation

She holds a medical degree from the Federal University of Amazonas and a medical residency in Infectious and Parasitic Diseases and Tropical Medicine from the Dr. Heitor Vieira Dourado Foundation for Tropical Medicine (FMTHVD). She completed her Master's degree in Tropical Medicine in 2000 at the Oswaldo Cruz Foundation in Rio de Janeiro. She is a professor of Infectious and Parasitic Diseases at the State University of Amazonas and Nilton Lins University, a supervisor of the Internship in Endemic Diseases at the State University of Amazonas, and a supervisor of the Infectious Diseases Residency Program at the FMTHVD. She provides care, teaching, and research at the FMTHVD Hospital and Outpatient Unit, directly participating in the training of medical residents, medical internship students, and undergraduate students. She has experience caring for and monitoring patients with Infectious and Parasitic Diseases, including HIV/AIDS, Systemic Mycoses, Cryptococcosis, and Tuberculosis, among others. Medical Coordinator of the Contingency Plan for COVID-19 and Severe Acute Respiratory Syndrome at Unimed Manaus. She is currently a student in the Stricto Sensu postgraduate program in Tropical Medicine at the Oswaldo Cruz Institute (IOC) of FIOCRUZ/RJ.

Filipe Anibal Carvalho-Costa, Oswaldo Cruz Foundation

He holds an MD from the Federal University of Rio de Janeiro (1993), a Pediatrics residency (1996), and a Master’s (2004) and PhD (2007) in Tropical Medicine from Fiocruz. He worked as a pediatrician in Brazil’s public health system (SUS) until 2008, when he became a Public Health Researcher at Fiocruz. He coordinated Fiocruz’s Graduate Program in Tropical Medicine (2011–2013) and led several institutional partnerships and programs, including Fiocruz’s regional office in Piauí (2012–2020). He has published over 130 scientific articles, supervised 40 Master’s and 10 PhD theses, and is Head of the Laboratory of Epidemiology and Molecular Systematics at the Oswaldo Cruz Institute. He has been a CNPq research fellow since 2012 and a reviewer for LILACS-indexed journals since 2020.

Maria Graciede Filha Santarém Andrade, Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Diretoria de Assistência Médica, Gerência de Ambulatório, Manaus, AM, Brasil; Fundação de Vigilância em Saúde do Amazonas Dra. Rosemary Costa Pinto, Centro de Referência para Imunobiológicos Especiais, Manaus, AM, Brasil

She holds a Bachelor’s degree in Nursing from the Federal University of Amazonas (1995). She is currently a Nurse at the Dr. Heitor Vieira Dourado Tropical Medicine Foundation and at the Amazonas State Health Surveillance Foundation. She has experience in Nursing, with an emphasis on Infectious Diseases and Immunization. She works at the Reference Center for Special Immunobiologicals (CRIE) as the Nurse responsible for Special Vaccine Indications, and for the Reporting and Investigation of Adverse Events Following Vaccination. She is also involved in Hospital Infection Control and Patient Safety at the Unimed Manaus Maternity Hospital.

Maria do Socorro Guimarães de Souza, Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Diretoria de Assistência Médica, Gerência de Ambulatório, Manaus, AM, Brasil

She holds a Bachelor’s degree in Physical Therapy from Nilton Lins University Center (2005) and a postgraduate specialization in Pulmonary and Cardiovascular Functional Physical Therapy. She is currently responsible for the tuberculosis control program at the Dr. Heitor Vieira Dourado Tropical Medicine Foundation.

Nestor Cordeiro dos Santos Neto, Hospital de Messejana Dr. Carlos Alberto Studart Gomes, Serviço de Terapia Intensiva, Fortaleza, CE, Brasil

He holds a medical degree from the State University of Amazonas (2008), a postgraduate specialization in Adult Intensive Care Medicine from the Albert Einstein Israelite Hospital (2013), board certification in Internal Medicine (2015) and in Intensive Care Medicine (2018), and an advanced specialization in Surgical Intensive Care and Anesthesiology (2016). He earned a PhD in Sciences through the Cardiology Program at the Heart Institute (InCor) of the University of São Paulo (USP). He has worked in intensive care at the Cancer Institute of São Paulo (ICESP) and the Heart Institute (InCor). He is currently a staff intensivist at Hospital Oto Aldeota, an on-call intensivist at Messejana Heart Hospital, and a staff internal medicine physician at Leonardo Da Vinci Hospital.

Valdete Santos de Araújo, Universidade Nilton Lins, Curso de Medicina, Disciplina de Doenças Infecciosas e Parasitárias, Manaus, AM, Brasil; Universidade Estadual do Amazonas, Coordenação de Engenharia Civil, Manaus, AM, Brasil

She holds a bachelor’s degree in Civil Engineering from the Federal University of Amazonas (1998), a master’s degree in Urban Engineering from UFSCar (2002), and a PhD in Transportation Engineering from the Alberto Luiz Coimbra Institute for Graduate Studies and Research in Engineering (COPPE/UFRJ) (2010). She is a specialist in Environmental Education and Water Resources (USP), in Engineering Appraisals and Expert Reports (UFAM), and an Occupational Safety Engineer (UEA, 2024). She is an Associate Professor (level A) at the State University of Amazonas (UEA) and a researcher at UFAM. She served as an expert witness for the Amazonas State Public Prosecutor’s Office. She coordinated the Civil Engineering programs at Nilton Lins University (2010–2011) and Uninorte (2011–2012). She was Vice President of the Amazonas Academy of Civil Engineering (AAEC, 2017–2019), Vice President of AFEAG-AM, Vice President of the Brazilian Association of Civil Engineering (ABENC) Amazonas Chapter, and Acting President of the Brazilian Association of Sanitary and Environmental Engineering (ABES) Amazonas Chapter. She is Director of the Encontro das Águas Institute and currently a medical student at Nilton Lins University.

Flor Ernestina Martinez Espinosa, Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Diretoria de Ensino e Pesquisa, Gerência de Malária, Manaus, AM, Brasil ; Fundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Laboratório Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, Brasil;

She holds a medical degree from the Universidad Nacional de Colombia (1991), a residency in Infectious and Parasitic Diseases at the Tropical Medicine Foundation (FMT-HVD, 1996), and a Master’s (1998) and PhD (2003) in Tropical Medicine from the Oswaldo Cruz Institute (IOC/Fiocruz). She is a physician-researcher at FMT-HVD and a public health researcher at ILMD Fiocruz/Amazônia, where she serves as deputy head of the IPCCB Laboratory. She is deputy coordinator and faculty member of the Graduate Program in Tropical Medicine (UEA/FMT-HVD) and teaches in the PPGVIDA program (ILMD/Fiocruz). She has served as a member of CONEP and ethics committees at FMT-HVD and UFAM. Her research focuses on tropical medicine and the impact of infectious diseases on the maternal–fetal dyad, including malaria, Zika, tuberculosis, STIs, coinfections, and clinical epidemiology. She is also a clinical medicine professor at IME.

Martha Cecilia Suarez-Mutis, Oswaldo Cruz Foundation

She holds a medical degree from the National University of Colombia (1990), a specialization in Epidemiology from the National School of Public Health (ENSP/Rio de Janeiro – Manaus Regional Office, 1994); a master's degree (1997) and a doctorate (2007) in Tropical Medicine from the Oswaldo Cruz Institute/Fiocruz. He/She worked as an epidemiologist physician at the Special Indigenous Sanitary District of Alto Solimões (DSEI-AS) between 2000 and 2003 and was a research assistant at the National University of Colombia, Leticia campus. He/She is the head and lead researcher of the Parasitic Diseases Laboratory at the Oswaldo Cruz Institute-IOC-Fiocruz. He/She is a member of the Technical Committee for Monitoring and Advising the National Malaria Control Program of the Brazilian Ministry of Health and of the IOC Working Group supporting the Interministerial Committee for the elimination of tuberculosis and other socially determined diseases (CIEDDS). He/She was a Young Scientist of the State of Rio de Janeiro from 2012 to 2019 by FAPERJ, a Senior Visiting Researcher at the Health Surveillance Foundation of the State of Amazonas from 2012 to 2014, and at the Institut de Recherche pour le Développement (IRD) in Montpellier, France in 2023. He/She is part of the Deliberative Council of the Oswaldo Cruz Institute as head of the Parasitic Diseases Laboratory. He/She belonged to the Research Technical Chamber between 2011-2013 and to the Teaching Technical Chamber (CTE) of Fiocruz, as well as the CTE of the Oswaldo Cruz Institute between 2014 and 2020. He/She coordinated the Graduate Program in Tropical Medicine at the Oswaldo Cruz Institute (PGMT) [Medicine II Area, CAPES level 6] from 2014 to 2020 and was part of the Graduate Committee of the PGMT and the graduate committee of the international graduate project Focem-Mercosur. He/She coordinates the following courses at PGMT: Epidemiology and control of infectious and parasitic diseases, Epidemiology in Tropical Medicine, and Medical Protozoology. He/She is also a faculty member of the Graduate Program in Health Sciences of the Mozambique National Health Institute-Fiocruz partnership, teaching the course Prophylaxis and Therapy in Infectious Diseases. Coordinator of the Southeast Regional Brazilian Health and Environment Olympiad (OBSMA). He/She was part of the Human Research Ethics Committee of the Oswaldo Cruz Institute (CEP Fiocruz/IOC) and of the National University of Colombia, Amazonas campus. He/She has experience in the medical field with an emphasis on Tropical Medicine, mainly working on the following topics: epidemiology, malaria, genomic surveillance of malaria, public health, analysis of endemic processes, health education, indigenous peoples’ health, and border health.