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Social Stressors, Arboviral Infection, and Immune Dysregulation in the Coastal Lowland Region of Ecuador: A Mixed Methods Approach in Ecological Perspective
Denisse Vega Ocasio
Denisse Vega Ocasio
Clinical and Translational Sciences Institute, University of Rochester School of Medicine, Rochester, New York;
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Anna M. Stewart-Ibarra
Anna M. Stewart-Ibarra
InterAmerican Institute for Global Change Research (IAI), Directorate, Montevideo, Uruguay;
State University of New York Upstate Medical University, Department of Medicine, Syracuse, New York;
State University of New York Upstate Medical University, Institute for Global Health and Translational Science, Syracuse, New York;
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State University of New York Upstate Medical University, Department of Medicine, Syracuse, New York;
State University of New York Upstate Medical University, Institute for Global Health and Translational Science, Syracuse, New York;
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Rachel Sippy
Rachel Sippy
Department of Microbiology & Immunology, State University of New York – Upstate Medical University, Syracuse, New York;
Department of Geography, University of Florida, Gainesville, Florida;
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Department of Geography, University of Florida, Gainesville, Florida;
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Christina Li
Christina Li
Department of Chemistry, State University of New York College at Oswego, New York;
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Kaitlyn McCue
Kaitlyn McCue
Department of Chemistry, State University of New York College at Oswego, New York;
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Kestutis G. Bendinskas
Kestutis G. Bendinskas
Department of Chemistry, State University of New York College at Oswego, New York;
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Brooks B. Gump
Brooks B. Gump
Department of Public Health, Syracuse University, Syracuse, New York;
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Cinthya Cueva-Aponte
Cinthya Cueva-Aponte
State University of New York Upstate Medical University, Institute for Global Health and Translational Science, Syracuse, New York;
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Efrain Beltrán Ayala
Efrain Beltrán Ayala
Universidad Técnica de Machala, Medicine, Machala, El Oro, Ecuador;
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Craig N. Morrell
Craig N. Morrell
Aab Cardiovascular Research Institute, University of Rochester School of Medicine, Rochester, New York;
Department of Medicine, University of Rochester School of Medicine, Rochester, New York;
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Department of Medicine, University of Rochester School of Medicine, Rochester, New York;
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Timothy D. Dye
Timothy D. Dye
Department of Obstetrics and Gynecology, University of Rochester School of Medicine and Dentistry, Rochester, New York
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ABSTRACT.
Aedes aegypti, the mosquito that transmits arboviral diseases such as dengue (DENV), chikungunya (CHIKV), and Zika viruses (ZIKV), is present in tropical and subtropical regions of the world. Individuals at risk of mosquito-borne disease (MBD) in the urban tropics face daily challenges linked to their socio-environment conditions, such as poor infrastructure, poverty, crowding, and limited access to adequate healthcare. These daily demands induce chronic stress events and dysregulated immune responses. We sought to investigate the role of socio-ecologic risk factors in distress symptoms and their impact on biological responses to MBD in Machala, Ecuador. Between 2017 and 2019, individuals (≥ 18 years) with suspected arbovirus illness (DENV, ZIKV, and CHIKV) from sentinel clinics were enrolled (index cases, N = 28). Cluster investigations of the index case households and people from four houses within a 200-m radius of index home (associate cases, N = 144) were conducted (total N = 172). Hair samples were collected to measure hair cortisol concentration (HCC) as a stress biomarker. Blood samples were collected to measure serum cytokines concentrations of IL-10, IL-8, TNF-α, and TGF-β. Univariate analyses were used to determine the association of socio-health metrics related to perceived stress scores (PSS), HCC, and immune responses. We found that housing conditions influence PSS and HCC levels in individuals at risk of MBD. Inflammatory cytokine distribution was associated with the restorative phase of immune responses in individuals with low-moderate HCC. These data suggest that cortisol may dampen pro-inflammatory responses and influence activation of the restorative phase of immune responses to arboviral infections.
- Supplemental Materials (DOCX 584 KB)
Author Notes
Financial support: At the time this work was completed, Dr. Vega Ocasio was a trainee in the University of Rochester’s Translational Biomedical Science PhD Program, which is supported by Grant 2TL1TR002000-05 from the National Center for Advancing Translational Sciences, National Institutes of Health. Dr. Vega Ocasio was additionally supported by funds from BWF1014095 from the Burroughs Wellcome Fund. The surveillance study was supported by SUNY Upstate Medical University and Clinical Research Management (CRM). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of this manuscript.
Disclaimer: We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.
Authors’ addresses: Denisse Vega Ocasio, Clinical and Translational Sciences Institute, University of Rochester School of Medicine, Rochester, NY, E-mail: dvegaoc@emory.edu. Anna M. Stewart-Ibarra, Inter-American Institute for Global Change Research, Directorate Montevideo, Uruguay, State University of New York Upstate Medical University, Department of Medicine, Syracuse, NY, and State University of New York Upstate Medical University, Institute for Global Health and Translational Science, Syracuse, NY, E-mail: astewart@dir.iai.int. Rachel Sippy, State University of New York Upstate Medical University, Department of Microbiology and Immunology, Syracuse, NY, and University of Florida, Department of Medical Geography, Gainesville, FL, E-mail: sippyr@upstate.edu. Kestutis G. Bendinskas, State University of New York at Oswego College Stores, Department of Chemistry, Oswego, NY, E-mail: kestutis.bendinskas@gmail.com. Brooks B. Gump, Syracuse University, Department of Public Health, Syracuse, NY, E-mail: bbgump@syr.edu. Cinthya Cueva-Aponte, State University of New York Upstate Medical University, Institute Center for Global Health and Translational Science, Syracuse, NY, E-mail: cin_ka10@hotmail.com. Efrain Beltrán Ayala, Universidad Tecnica de Machala, Medicine, Machala, El Oro, ecuador, E-mail: felixbeltran57@hotmail.com. Craig N. Morrell, University of Rochester School of Medicine and Dentistry, Aab Cardiovascular Research Institute, Rochester, NY, and University of Rochester School of Medicine and Dentistry, Department of Medicine, Rochester, NY, E-mail: craig_morrell@urmc.rochester.edu. Timothy D. Dye, University of Rochester School of Medicine and Dentistry, Department of Obstetrics and Gynecology, Rochester, NY, E-mail: tim_dye@urmc.rochester.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
PAHO , 2017. Reported Cases of Dengue Fever in The Americas by Country or Territory. Available at: http://www.paho.org/data/index.php/en/mnu-topics/indicadores-dengue-en/dengue-nacional-en/252-dengue-pais-ano-en.html. Accessed 2018.
-
2.
Rossi G , Karki S , Smith RL , Brown WM , Ruiz MOH , 2018. The spread of mosquito-borne viruses in modern times: a spatio-temporal analysis of dengue and chikungunya. Spat Spatio-Temporal Epidemiol 26: 113–125.
-
3.
Kenneson A et al., 2017. Social-ecological factors and preventive actions decrease the risk of dengue infection at the household-level: results from a prospective dengue surveillance study in Machala, Ecuador. PLoS Negl Trop Dis 11: e0006150.
-
4.
Stewart Ibarra A et al., 2013. Community perceptions of emerging dengue in urban areas in southern coastal Ecuador (Stewart Ibarra et al 2014, BMC Public Health).
-
5.
Stewart Ibarra AM , Ryan SJ , Beltrán E , Mejía R , Silva M , Muñoz Á , 2013. Dengue vector dynamics (Aedes aegypti) influenced by climate and social factors in Ecuador: implications for targeted control. PLoS One 8: e78263.
-
6.
Stewart-Ibarra AM et al., 2014. Spatiotemporal clustering, climate periodicity, and social-ecological risk factors for dengue during an outbreak in Machala, Ecuador, in 2010. BMC Infect Dis 14: 610.
-
7.
Ali S et al., 2017. Environmental and social change drive the explosive emergence of Zika virus in the Americas. PLoS Negl Trop Dis 11: e0005135.
-
8.
Brathwaite Dick O , San Martín JL , Montoya RH , del Diego J , Zambrano B , Dayan GH , 2012. The history of dengue outbreaks in the Americas. Am J Trop Med Hyg 87: 584–593.
-
9.
Sternthal M , Slopen N , Williams DR , 2011. Racial disparities in health: how much does stress really matter? Du Bois Rev 8: 95–113.
-
10.
Paul Taylor RK , Fry R , Velasco G , Motel S , 2011. Wealth Gaps Rise to Record Highs between Whites, Blacks and Hispanics. Pew Research Center: Social and Demographics Trends.
-
11.
Chida Y , Steptoe A , 2009. Cortisol awakening response and psychosocial factors: a systematic review and meta-analysis. Biol Psychol 80: 265–278.
-
12.
Cohen S , Janicki-Deverts D , Miller GE , 2007. Psychological stress and disease. JAMA 298: 1685–1687.
-
13.
Dhabhar FS , 2014. Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res 58: 193–210.
-
14.
Giurgescu C et al., 2015. The impact of neighborhood quality, perceived stress, and social support on depressive symptoms during pregnancy in African American women. Soc Sci Med 130: 172–180.
-
15.
Hellhammer DH , Wust S , Kudielka BM , 2009. Salivary cortisol as a biomarker in stress research. Psychoneuroendocrinology 34: 163–171.
-
16.
Sladek MR , Doane LD , Luecken LJ , Eisenberg N , 2016. Perceived stress, coping, and cortisol reactivity in daily life: a study of adolescents during the first year of college. Biol Psychol 117: 8–15.
-
17.
Uchino BN , Bowen K , Carlisle M , Birmingham W , 2012. Psychological pathways linking social support to health outcomes: a visit with the “ghosts” of research past, present, and future. Soc Sci Med (1982) 74: 949–957.
-
18.
Herman JP et al., 2016. Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 6: 603–621.
-
19.
Meaney MJ et al., 1996. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18: 49–72.
-
20.
Oakley RH , Cidlowski JA , 2013. The biology of the glucocorticoid receptor: new signaling mechanisms in health and disease. J Allergy Clin Immunol 132: 1033–1044.
-
21.
Kino T et al. , 2017. Endotext [Internet].South Dartmouth, MA: MDText.com, Inc.
-
22.
Morey JN , Boggero IA , Scott AB , Segerstrom SC , 2015. Current directions in stress and human immune function. Curr Opin Psychol 5: 13–17.
-
23.
Lee DY , Kim E , Choi MH , 2015. Technical and clinical aspects of cortisol as a biochemical marker of chronic stress. BMB Rep 48: 209–216.
-
24.
Russell E , Koren G , Rieder M , Van Uum S , 2012. Hair cortisol as a biological marker of chronic stress: current status, future directions and unanswered questions. Psychoneuroendocrinology 37: 589–601.
-
25.
United Nations , 2002. Integrated Assessment of Trade Liberalization and Trade-Related Policies. A Country Study on the Banana Sector in Ecuador. 1–75.
-
26.
Stewart Ibarra A , Henderson R , Heydari N , Borbor-Cordova MJ , Fujii Y , Bardosh K , 2019. Tracking Aedes aegypti in a hotter, wetter, more urban world. 128–149.
-
27.
Publica MdS PROYECCIÓN DE LA POBLACIÓN ECUATORIANA, POR AÑOS CALENDARIO, SEGÚN CANTONES. 2010–2020.
-
28.
Douglas Southgate KF , Strasma J , White A , Lach L , Kellenberg L , Kelly P , 1995. As Assessment of Urban Environmental Problems in Ecuador. Ohio State University.
-
29.
Publica MdS , 2010. Casos de Dengue Reportados en el Epi Local por Semanas Epidemiologicas: Machala, Ecuador In. Departamento de Epidemiologia. Direccion Provincial de Salud de El Oro.
-
30.
Publica MdS , 2018. Gacetas Vectoriales. Available at: https://www.salud.gob.ec/gacetas-vectoriales/. Accessed XXXXX.
-
31.
Stewart-Ibarra AM , Lowe R , 2013. Climate and non-climate drivers of dengue epidemics in southern coastal Ecuador. Am J Trop Med Hyg 88: 971–981.
-
32.
Stewart Ibarra AM et al., 2014. A social-ecological analysis of community perceptions of dengue fever and Aedes aegypti in Machala, Ecuador. BMC Public Health 14: 1135.
-
33.
Stewart-Ibarra AM et al., 2018. The burden of dengue fever and Chikungunya in southern coastal Ecuador: epidemiology, clinical presentation, and phylogenetics from the first two years of a prospective study. Am J Trop Med Hyg 98: 1444–1459.
-
34.
Granda ML , Jimenez WG , 2019. The evolution of socioeconomic health inequalities in Ecuador during a public health system reform (2006–2014). Int J Equity Health 18: 31.
-
35.
Martín JAC , 2015. UNA CIUDAD MEDIA DEL ECUADOR: MACHALA. PROPUESTA DIGNOSITIVA.
-
36.
Coimbra CEA , McElroy A , Patricia K , 2007. Townsend, medical anthropology in ecological perspective, 4th edition. Hum Ecol 35: 647–648.
-
37.
Stewart-Ibarra AM et al., 2017. The high burden of dengue and chikungunya in southern coastal Ecuador: epidemiology, clinical presentation, and phylogenetics from a prospective study in Machala in 2014 and 2015. bioRxiv.
-
38.
Dye TDV et al., 2018. Critical medical ecological perspectives on diabetes in the Pacific islands: colonialism, power, and balance in human-environment interaction over time. Lancet Glob Health 6: S36.
-
39.
Chin NP , Dye TD , 2016. The health and wealth of mountain communities. Matern Child Health J 20: 2413–2414.
-
40.
Dean AGSK , Soe MM , 2006. OpenEpi: Open Source Epidemiologic Statistics for Public Health. Available at: www.OpenEpi.com. Accessed 2018.
-
41.
Sheldon Cohen TK , 1983. Robin Mermelstein a global measure of perceived stress. J Health Soc Behav 24: 385–396.
-
42.
Blodgett J , Walter D , MacKenzie JA , Gump BB , Bendinskas K , 2017. Both hair cortisol and perceived stress during fall exams decrease after the winter break. Austin Biochem 2: 1007–1011. Available at: http://austinpublishinggroup.com/biochemistry/download.php?file=fulltext/biochemistry-v2-id1007.pdf.
-
43.
Prevention CfDCa , 2013. CDC DENV-1-4 Real-Time RT-PCR Assay: for Detection and Serotype Identification of Dengue Virus. National Center for Emerging and Zoonotic Infectious Diseases. Division of Vector-Borne Diseases.
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