Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines

Jacob E. Aronoff; Thomas W. McDade; Linda S. Adair; Nanette R. Lee; Delia B. Carba; Julia L. MacIsaac; Kristy Dever; Parmida Atashzay; Michael S. Kobor; Christopher W. Kuzawa

doi:10.1016/j.bbi.2023.10.003

Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines

Jacob E. Aronoff^*, Thomas W. McDade, Linda S. Adair, Nanette R. Lee, Delia B. Carba, Julia L. MacIsaac, Kristy Dever, Parmida Atashzay, Michael S. Kobor, Christopher W. Kuzawa

^*Corresponding author for this work

Anthropology

Research output: Contribution to journal › Article › peer-review

2 Scopus citations

Abstract

Background: Socioeconomic status (SES) gradients in health are well-documented, and while biological pathways are incompletely understood, chronic inflammation and accelerated immune aging (immunosenescence) among lower SES individuals have been implicated. However, previous findings have come from samples in higher income countries, and it is unclear how generalizable they are to lower- and middle-income countries (LMIC) with different infectious exposures and where adiposity—an important contributor to chronic inflammation—might show different SES patterning. To address this gap, we explored associations between SES and inflammation and immunosenescence in a sample of women in Cebu, Philippines. Methods: Data came from the mothers of the Cebu Longitudinal Health and Nutrition Survey birth cohort (mean age: 47.7, range: 35–69 years). SES was measured as a combination of annual household income, education level, and assets. Chronic inflammation was measured using C-reactive protein (CRP) in plasma samples from 1,834 women. Immunosenescence was measured by the abundance of exhausted CD8T (CD8 + CD28-CD45RA-) and naïve CD8T and CD4T cells, estimated from DNA methylation in whole blood in a random subsample of 1,028. Possible mediators included waist circumference and a collection of proxy measures of pathogen exposure. Results: SES was negatively associated with the measures of immunosenescence, with slight evidence for mediation by a proxy measure for pathogen exposure from the household's drinking water source. In contrast, SES was positively associated with CRP, which was explained by the positive association with waist circumference. Conclusions: Similar to higher income populations, in Cebu there is an SES-gradient in pathogen exposures and immunosenescence. However, lifestyle changes occurring more rapidly among higher SES individuals is contributing to a positive association between SES and adiposity and inflammation. Our results suggest more studies are needed to clarify the relationship between SES and inflammation and immunosenescence across LMIC.

Original language	English (US)
Pages (from-to)	101-108
Number of pages	8
Journal	Brain, Behavior, and Immunity
Volume	115
DOIs	https://doi.org/10.1016/j.bbi.2023.10.003
State	Published - Jan 2024

Funding

We thank the researchers at the USC-Office of Population Studies Foundation, Inc., University of San Carlos, Cebu City, Philippines, for their role in the study design and data collection, and the study participants, who generously provided their time. This research was supported in part through the computational resources and staff contributions provided for the Quest high performance computing facility at Northwestern University which is jointly supported by the Office of the Provost, the Office for Research, and Northwestern University Information Technology. TM also acknowledges financial support from CIFAR as a fellow in the Child and Brain Development program. We thank the researchers at the USC-Office of Population Studies Foundation, Inc. University of San Carlos, Cebu City, Philippines, for their role in the study design and data collection, and the study participants, who generously provided their time. This research was supported in part through the computational resources and staff contributions provided for the Quest high performance computing facility at Northwestern University which is jointly supported by the Office of the Provost, the Office for Research, and Northwestern University Information Technology. TM also acknowledges financial support from CIFAR as a fellow in the Child and Brain Development program. NIH Office of Extramural Research, National Institutes of Health R01 (AG061006; HL085144; HD054501; P2CHD050924; TW05596). Interdisciplinary Obesity Center (RR20649). Center for Environmental Health and Susceptibility (ES10126; project 7-2004-E).

Keywords

Adiposity
C-reactive protein
Cell deconvolution
DNA methylation
Immunosenescence
Inflammation
Socioeconomic status

ASJC Scopus subject areas

Immunology
Endocrine and Autonomic Systems
Behavioral Neuroscience

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.bbi.2023.10.003

Cite this

Aronoff, J. E., McDade, T. W., Adair, L. S., Lee, N. R., Carba, D. B., MacIsaac, J. L., Dever, K., Atashzay, P., Kobor, M. S., & Kuzawa, C. W. (2024). Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines. Brain, Behavior, and Immunity, 115, 101-108. https://doi.org/10.1016/j.bbi.2023.10.003

@article{13f781c1788f46aa8ac322b179a7a32a,

title = "Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines",

abstract = "Background: Socioeconomic status (SES) gradients in health are well-documented, and while biological pathways are incompletely understood, chronic inflammation and accelerated immune aging (immunosenescence) among lower SES individuals have been implicated. However, previous findings have come from samples in higher income countries, and it is unclear how generalizable they are to lower- and middle-income countries (LMIC) with different infectious exposures and where adiposity—an important contributor to chronic inflammation—might show different SES patterning. To address this gap, we explored associations between SES and inflammation and immunosenescence in a sample of women in Cebu, Philippines. Methods: Data came from the mothers of the Cebu Longitudinal Health and Nutrition Survey birth cohort (mean age: 47.7, range: 35–69 years). SES was measured as a combination of annual household income, education level, and assets. Chronic inflammation was measured using C-reactive protein (CRP) in plasma samples from 1,834 women. Immunosenescence was measured by the abundance of exhausted CD8T (CD8 + CD28-CD45RA-) and na{\"i}ve CD8T and CD4T cells, estimated from DNA methylation in whole blood in a random subsample of 1,028. Possible mediators included waist circumference and a collection of proxy measures of pathogen exposure. Results: SES was negatively associated with the measures of immunosenescence, with slight evidence for mediation by a proxy measure for pathogen exposure from the household's drinking water source. In contrast, SES was positively associated with CRP, which was explained by the positive association with waist circumference. Conclusions: Similar to higher income populations, in Cebu there is an SES-gradient in pathogen exposures and immunosenescence. However, lifestyle changes occurring more rapidly among higher SES individuals is contributing to a positive association between SES and adiposity and inflammation. Our results suggest more studies are needed to clarify the relationship between SES and inflammation and immunosenescence across LMIC.",

keywords = "Adiposity, C-reactive protein, Cell deconvolution, DNA methylation, Immunosenescence, Inflammation, Socioeconomic status",

author = "Aronoff, {Jacob E.} and McDade, {Thomas W.} and Adair, {Linda S.} and Lee, {Nanette R.} and Carba, {Delia B.} and MacIsaac, {Julia L.} and Kristy Dever and Parmida Atashzay and Kobor, {Michael S.} and Kuzawa, {Christopher W.}",

note = "Publisher Copyright: {\textcopyright} 2023 Elsevier Inc.",

year = "2024",

month = jan,

doi = "10.1016/j.bbi.2023.10.003",

language = "English (US)",

volume = "115",

pages = "101--108",

journal = "Brain, Behavior, and Immunity",

issn = "0889-1591",

publisher = "Academic Press Inc.",

}

Aronoff, JE, McDade, TW, Adair, LS, Lee, NR, Carba, DB, MacIsaac, JL, Dever, K, Atashzay, P, Kobor, MS & Kuzawa, CW 2024, 'Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines', Brain, Behavior, and Immunity, vol. 115, pp. 101-108. https://doi.org/10.1016/j.bbi.2023.10.003

TY - JOUR

T1 - Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines

AU - Aronoff, Jacob E.

AU - McDade, Thomas W.

AU - Adair, Linda S.

AU - Lee, Nanette R.

AU - Carba, Delia B.

AU - MacIsaac, Julia L.

AU - Dever, Kristy

AU - Atashzay, Parmida

AU - Kobor, Michael S.

AU - Kuzawa, Christopher W.

PY - 2024/1

Y1 - 2024/1

N2 - Background: Socioeconomic status (SES) gradients in health are well-documented, and while biological pathways are incompletely understood, chronic inflammation and accelerated immune aging (immunosenescence) among lower SES individuals have been implicated. However, previous findings have come from samples in higher income countries, and it is unclear how generalizable they are to lower- and middle-income countries (LMIC) with different infectious exposures and where adiposity—an important contributor to chronic inflammation—might show different SES patterning. To address this gap, we explored associations between SES and inflammation and immunosenescence in a sample of women in Cebu, Philippines. Methods: Data came from the mothers of the Cebu Longitudinal Health and Nutrition Survey birth cohort (mean age: 47.7, range: 35–69 years). SES was measured as a combination of annual household income, education level, and assets. Chronic inflammation was measured using C-reactive protein (CRP) in plasma samples from 1,834 women. Immunosenescence was measured by the abundance of exhausted CD8T (CD8 + CD28-CD45RA-) and naïve CD8T and CD4T cells, estimated from DNA methylation in whole blood in a random subsample of 1,028. Possible mediators included waist circumference and a collection of proxy measures of pathogen exposure. Results: SES was negatively associated with the measures of immunosenescence, with slight evidence for mediation by a proxy measure for pathogen exposure from the household's drinking water source. In contrast, SES was positively associated with CRP, which was explained by the positive association with waist circumference. Conclusions: Similar to higher income populations, in Cebu there is an SES-gradient in pathogen exposures and immunosenescence. However, lifestyle changes occurring more rapidly among higher SES individuals is contributing to a positive association between SES and adiposity and inflammation. Our results suggest more studies are needed to clarify the relationship between SES and inflammation and immunosenescence across LMIC.

AB - Background: Socioeconomic status (SES) gradients in health are well-documented, and while biological pathways are incompletely understood, chronic inflammation and accelerated immune aging (immunosenescence) among lower SES individuals have been implicated. However, previous findings have come from samples in higher income countries, and it is unclear how generalizable they are to lower- and middle-income countries (LMIC) with different infectious exposures and where adiposity—an important contributor to chronic inflammation—might show different SES patterning. To address this gap, we explored associations between SES and inflammation and immunosenescence in a sample of women in Cebu, Philippines. Methods: Data came from the mothers of the Cebu Longitudinal Health and Nutrition Survey birth cohort (mean age: 47.7, range: 35–69 years). SES was measured as a combination of annual household income, education level, and assets. Chronic inflammation was measured using C-reactive protein (CRP) in plasma samples from 1,834 women. Immunosenescence was measured by the abundance of exhausted CD8T (CD8 + CD28-CD45RA-) and naïve CD8T and CD4T cells, estimated from DNA methylation in whole blood in a random subsample of 1,028. Possible mediators included waist circumference and a collection of proxy measures of pathogen exposure. Results: SES was negatively associated with the measures of immunosenescence, with slight evidence for mediation by a proxy measure for pathogen exposure from the household's drinking water source. In contrast, SES was positively associated with CRP, which was explained by the positive association with waist circumference. Conclusions: Similar to higher income populations, in Cebu there is an SES-gradient in pathogen exposures and immunosenescence. However, lifestyle changes occurring more rapidly among higher SES individuals is contributing to a positive association between SES and adiposity and inflammation. Our results suggest more studies are needed to clarify the relationship between SES and inflammation and immunosenescence across LMIC.

KW - Adiposity

KW - C-reactive protein

KW - Cell deconvolution

KW - DNA methylation

KW - Immunosenescence

KW - Inflammation

KW - Socioeconomic status

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U2 - 10.1016/j.bbi.2023.10.003

DO - 10.1016/j.bbi.2023.10.003

M3 - Article

C2 - 37820972

AN - SCOPUS:85173978184

SN - 0889-1591

VL - 115

SP - 101

EP - 108

JO - Brain, Behavior, and Immunity

JF - Brain, Behavior, and Immunity

ER -

Socioeconomic status is negatively associated with immunosenescence but positively associated with inflammation among middle-aged women in Cebu, Philippines

Abstract

Funding

Keywords

ASJC Scopus subject areas

UN SDGs

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