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      Biomarkers representing key aging-related biological pathways are associated with subclinical atherosclerosis and all-cause mortality: The Framingham Study

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          Abstract

          Background

          Increased oxidative stress, leukocyte telomere length (LTL) shortening, endothelial dysfunction, and lower insulin-like growth factor (IGF)-1 concentrations reflect key molecular mechanisms of aging. We hypothesized that biomarkers representing these pathways are associated with measures of subclinical atherosclerosis and all-cause mortality.

          Methods and results

          We evaluated up to 2,314 Framingham Offspring Study participants (mean age 61 years, 55% women) with available biomarkers of aging: LTL, circulating concentrations of IGF-1, asymmetrical dimethylarginine (ADMA), and urinary F2-Isoprostanes indexed to urinary creatinine. We evaluated the association of each biomarker with coronary artery calcium [ln (CAC+1)] and carotid intima-media thickness (IMT). In multivariable-adjusted linear regression models, higher ADMA levels were associated with higher CAC values (β ADMA per 1-SD increase 0.25; 95% confidence interval [CI] [0.11, 0.39]). Additionally, shorter LTL and lower IGF-1 values were associated with higher IMT values (β LTL −0.08, 95%CI −0.14, −0.02, and β IGF-1 −0.04, 95%CI −0.08, −0.01, respectively). During a median follow-up of 15.5 years, 593 subjects died. In multivariable-adjusted Cox regression models, LTL and IGF-1 values were inversely associated with all-cause mortality (hazard ratios [HR] per SD increase in biomarker, 0.85, 95% CI 0.74–0.99, and 0.90, 95% CI 0.82–0.98 for LTL and IGF-1, respectively). F2-Isoprostanes and ADMA values were positively associated with all-cause mortality (HR per SD increase in biomarker, 1.15, 95% CI, 1.10–1.22, and 1.10, 95% CI, 1.02–1.20, respectively).

          Conclusion

          In our prospective community-based study, aging-related biomarkers were associated with measures of subclinical atherosclerosis cross-sectionally and with all-cause mortality prospectively, supporting the concept that these biomarkers may reflect the aging process in community-dwelling adults.

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          Most cited references71

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          Heart Disease and Stroke Statistics—2018 Update: A Report From the American Heart Association

          Emelia Benjamin, Salim S. Virani, Clifton Callaway … (2018)
          Article 0 comments Cited 1448 times – based on 0 reviews     Review now
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            A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group.

            A S Levey, J Bosch, J. B. Lewis … (1999)
            Serum creatinine concentration is widely used as an index of renal function, but this concentration is affected by factors other than glomerular filtration rate (GFR). To develop an equation to predict GFR from serum creatinine concentration and other factors. Cross-sectional study of GFR, creatinine clearance, serum creatinine concentration, and demographic and clinical characteristics in patients with chronic renal disease. 1628 patients enrolled in the baseline period of the Modification of Diet in Renal Disease (MDRD) Study, of whom 1070 were randomly selected as the training sample; the remaining 558 patients constituted the validation sample. The prediction equation was developed by stepwise regression applied to the training sample. The equation was then tested and compared with other prediction equations in the validation sample. To simplify prediction of GFR, the equation included only demographic and serum variables. Independent factors associated with a lower GFR included a higher serum creatinine concentration, older age, female sex, nonblack ethnicity, higher serum urea nitrogen levels, and lower serum albumin levels (P < 0.001 for all factors). The multiple regression model explained 90.3% of the variance in the logarithm of GFR in the validation sample. Measured creatinine clearance overestimated GFR by 19%, and creatinine clearance predicted by the Cockcroft-Gault formula overestimated GFR by 16%. After adjustment for this overestimation, the percentage of variance of the logarithm of GFR predicted by measured creatinine clearance or the Cockcroft-Gault formula was 86.6% and 84.2%, respectively. The equation developed from the MDRD Study provided a more accurate estimate of GFR in our study group than measured creatinine clearance or other commonly used equations.
            Article 0 comments Cited 612 times – based on 0 reviews     Review now
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              The intersection between aging and cardiovascular disease.

              Brian North, David A Sinclair (2012)
              The average lifespan of humans is increasing, and with it the percentage of people entering the 65 and older age group is growing rapidly and will continue to do so in the next 20 years. Within this age group, cardiovascular disease will remain the leading cause of death, and the cost associated with treatment will continue to increase. Aging is an inevitable part of life and unfortunately poses the largest risk factor for cardiovascular disease. Although numerous studies in the cardiovascular field have considered both young and aged humans, there are still many unanswered questions as to how the genetic pathways that regulate aging in model organisms influence cardiovascular aging. Likewise, in the molecular biology of aging field, few studies fully assess the role of these aging pathways in cardiovascular health. Fortunately, this gap is beginning to close, and these two fields are merging together. We provide an overview of some of the key genes involved in regulating lifespan and health span, including sirtuins, AMP-activated protein kinase, mammalian target of rapamycin, and insulin-like growth factor 1 and their roles regulating cardiovascular health. We then discuss a series of review articles that will appear in succession and provide a more comprehensive analysis of studies carried out linking genes of aging and cardiovascular health, and perspectives of future directions of these two intimately linked fields.
              Article 0 comments Cited 467 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Cecilia Castro-Diehl: Role: InvestigationRole: Writing – original draft
                Rachel Ehrbar: Role: Formal analysis
                Vanesa Obas: Role: Writing – original draft
                Albin Oh:
                ORCID: https://orcid.org/0000-0002-4211-3113
                Role: Writing – review & editing
                Ramachandran S. Vasan: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Vanessa Xanthakis:
                ORCID: https://orcid.org/0000-0002-7352-621X
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Yan Li: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 14 May 2021
                Publication date Collection: 2021
                Volume: 16
                Issue: 5
                Electronic Location Identifier: e0251308
                Affiliations
                [1 ] Department of Medicine, Section of Preventive Medicine and Epidemiology, Boston University School of Medicine, Boston, Massachusetts, United States of America
                [2 ] Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts, United States of America
                [3 ] Department of Medicine, Internal Medicine Residency Program, Boston University School of Medicine, Boston, Massachusetts, United States of America
                [4 ] Lung, and Blood Institute’s Framingham Heart Study, Boston University’s and National Heart, Framingham, Massachusetts, United States of America
                [5 ] Department of Medicine, Section of Cardiology, Boston University School of Medicine, Boston, Massachusetts, United States of America
                [6 ] Department of Epidemiology, Boston University School of Public Health, Boston, Massachusetts, United States of America
                Shanghai Institute of Hypertension, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-4211-3113
                https://orcid.org/0000-0002-7352-621X
                Article
                Publisher ID: PONE-D-20-32445
                DOI: 10.1371/journal.pone.0251308
                PMC ID: 8121535
                PubMed ID: 33989340
                SO-VID: 58a94e5b-f494-4ffe-b41e-572521e2e3f5
                Copyright © © 2021 Castro-Diehl et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 15 October 2020
                Date accepted : 24 April 2021
                Page count
                Figures: 2, Tables: 4, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000009, Foundation for the National Institutes of Health;
                Award ID: NO1-HC-25195
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000009, Foundation for the National Institutes of Health;
                Award ID: HHSN268201500001I
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000009, Foundation for the National Institutes of Health;
                Award ID: 75N92019D00031
                Award Recipient :
                Funded by: National Heart, Lung and Blood Institute
                Award ID: 2K24 HL04334
                Award Recipient :
                Funded by: National Heart, Lung and Blood Institute
                Award ID: 6R01-NS 17950
                Funded by: National Heart, Lung and Blood Institute
                Award ID: R01 AG021593
                Funded by: National Heart, Lung and Blood Institute
                Award ID: 1RO1-HL64753
                Funded by: National Heart, Lung and Blood Institute
                Award ID: R01-HL076784
                Funded by: National Heart, Lung and Blood Institute
                Award ID: RO1HL080124
                Award Recipient :
                Funded by: National Heart, Lung and Blood Institute
                Award ID: 1R38HL143584
                Funded by: NIH Boston University Cardiovascular Center
                Award ID: N01-HV- 28178
                Award Recipient :
                Funded by: NIH Boston University Cardiovascular Center
                Award ID: HL71039
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000049, National Institute on Aging;
                Award ID: 1R01-AG028321
                Funded by: Boston University School of Medicine
                Award Recipient :
                Funded by: Multidisciplinary Training Program (T32) in Cardiovascular Epidemiology
                Award ID: 5T32HL125232
                Award Recipient :
                Framingham Heart Study (FHS) acknowledges the support of contracts NO1-HC-25195, HHSN268201500001I and 75N92019D00031 from the National Heart, Lung and Blood Institute for this research. This work was also supported by the National Heart, Lung and Blood Institute's 2K24 HL04334 (RSV), 6R01-NS 17950, R01 AG021593, 1RO1-HL64753, R01-HL076784), and RO1HL080124 (RSV), and 1R38HL143584; NIH Boston University Cardiovascular Center, N01-HV- 28178 and NIH grant HL71039 (RSV). This work was also supported by the National Institute on Aging (1R01-AG028321). Dr. Vasan is supported in part by the Evans Medical Foundation and the Jay and Louis Coffman Endowment from the Department of Medicine, Boston University School of Medicine. CCD was supported by the Multidisciplinary Training Program (T32) in Cardiovascular Epidemiology (5T32HL125232). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Biomarkers
                Subject: Medicine and Health Sciences
                Subject: Medical Conditions
                Subject: Cardiovascular Diseases
                Subject: Medicine and Health Sciences
                Subject: Cardiology
                Subject: Cardiovascular Medicine
                Subject: Cardiovascular Diseases
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Atherosclerosis
                Subject: Medicine and Health Sciences
                Subject: Epidemiology
                Subject: Medical Risk Factors
                Subject: Biology and Life Sciences
                Subject: Cell Biology
                Subject: Oxidative Stress
                Subject: Medicine and Health Sciences
                Subject: Endocrinology
                Subject: Endocrine Disorders
                Subject: Diabetes Mellitus
                Subject: Medicine and Health Sciences
                Subject: Medical Conditions
                Subject: Metabolic Disorders
                Subject: Diabetes Mellitus
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Blood Vessels
                Subject: Arteries
                Subject: Carotid Arteries
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Blood Vessels
                Subject: Arteries
                Subject: Carotid Arteries
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Blood Vessels
                Subject: Arteries
                Subject: Coronary Arteries
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Blood Vessels
                Subject: Arteries
                Subject: Coronary Arteries
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