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Biomarkers of mitochondrial dysfunction and inflammaging in older adults and blood pressure variability

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Abstract

Most physiopathological mechanisms underlying blood pressure variability (BPV) are implicated in aging. Vascular aging is associated with chronic low-grade inflammation occurring in late life, known as “inflammaging” and the hallmark “mitochondrial dysfunction” due to age-related stress. We aimed to determine whether plasma levels of the pleiotropic stress-related mitokine growth/differentiation factor 15 (GDF-15) and two inflammatory biomarkers, interleukin 6 (IL-6) and tumor necrosis factor receptor 1 (TNFR-1), are associated with visit-to-visit BPV in a population of community-dwelling older adults. The study population consisted of 1096 community-dwelling participants [median age 75 (72–78) years; 699 females, 63.7%] aged ≥ 70 years from the MAPT study. Plasma blood sample was collected 12 months after enrolment and BP was assessed up to seven times over a 4-year period. Systolic (SBPV) and diastolic BPV (DBPV) were determined through several indicators taking into account BP change over time, the order of measurements and formulas independent of mean BP levels. Higher values of GDF-15 were significantly associated with increased SBPV (all indicators) after adjustment for relevant covariates [adjusted 1-SD increase in GDF-15: β (SE) = 0.07 (0.04), p < 0.044, for coefficient of variation%]. GDF-15 levels were not associated with DBPV. No significant associations were found between IL-6 and BPV, whereas TNFR1 was only partially related to DBPV. Unlike inflammation biomarkers, higher GDF-15 levels were associated with greater SBPV. Our findings support the age-related process of mitochondrial dysfunction underlying BP instability, suggesting that BPV might be a potential marker of aging.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

Dr. Leonardo Bencivenga has been supported by the research grant provided by the Cardiopath PhD program, the research grant provided by the FDIME and the STAR PLUS Research Grant provided by University of Naples Federico II and Compagnia di San Paolo.

Funding

The present work was performed in the context of the INSPIRE Program, a research platform supported by grants from the Region Occitanie/Pyrénées-Méditerranée (Reference number: 1901175) and the European Regional Development Fund (ERDF) (Project number: MP0022856).

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Author notes

  1. Leonardo Bencivenga and Mathilde Strumia These authors equally contributed.

Authors and Affiliations

  1. Department of Advanced Biomedical Sciences, University of Naples “Federico II”, Via Sergio Pansini 5, Napoli, Italy

    Leonardo Bencivenga

  2. Gérontopôle de Toulouse, Institut du Vieillissement, CHU de Toulouse, France

    Leonardo Bencivenga, Mathilde Strumia, Yves Rolland, Sophie Guyonnet, Bruno Vellas, Philipe De Souto Barreto & Laure Rouch

  3. UMR INSERM 1295, Université Toulouse III, Toulouse, France

    Mathilde Strumia, Yves Rolland, Laurent Martinez, Sophie Guyonnet, Sandrine Andrieu, Bruno Vellas, Philipe De Souto Barreto & Laure Rouch

  4. Department of Pharmacy, Toulouse University, Toulouse, France

    Philippe Cestac

  5. Institut Des Maladies Métaboliques Et Cardiovasculaires (I2MC), Toulouse, France

    Angelo Parini & Alexandre Lucas

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  • , Stéphane Chanalet
  • , Françoise Hugon
  • , Fabrice Bonneville
  • , Christophe Cognard
  • , François Chollet
  • , Pierre Payoux
  • , Thierry Voisin
  • , Julien Delrieu
  • , Sophie Peiffer
  • , Anne Hitzel
  • , Michèle Allard
  • , Michel Zanca
  • , Jacques Monteil
  • , Jacques Darcourt
  • , Laurent Molinier
  • , Hélène Derumeaux
  • , Nadège Costa
  • , Bertrand Perret
  • , Claire Vinel
  • , Sylvie Caspar-Bauguil
  • , Pascale Olivier-Abbal
  • , Sandrine Andrieu
  • , Christelle Cantet
  •  & Nicola Coley

Contributions

Study concept and design: LB, YR, PDSB, LR. Acquisition, analysis and interpretation of data: LB, MS, LR. They had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Drafting of the manuscript: LB, PDSB, LR. Critical revision of the manuscript for important intellectual content: YR, LM, BV, PDSB. All authors approved the final version to be published and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Leonardo Bencivenga.

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Conflict of interest

The authors declare no competing interests.

MAPT/DSA group

MAPT Study Group. Principal investigator: Bruno Vellas (Toulouse); coordination: Sophie Guyonnet; project leader: Isabelle Carrié; CRA: Lauréane Brigitte; investigators: Catherine Faisant, Françoise Lala, Julien Delrieu, and Hélène Villars; psychologists: Emeline Combrouze, Carole Badufle, and Audrey Zueras; methodology, statistical analysis, and data management: Sandrine Andrieu, Christelle Cantet, and Christophe Morin; multidomain group: Gabor Abellan Van Kan, Charlotte Dupuy, Yves Rolland (physical and nutritional components), Céline Caillaud, Pierre-Jean Ousset (cognitive component), and Françoise Lala (preventive consultation) (Toulouse). The cognitive component was designed in collaboration with Sherry Willis from the University of Seattle and Sylvie Belleville, Brigitte Gilbert, and Francine Fontaine from the University of Montreal. Co-investigators in associated centers: Jean-François Dartigues, Isabelle Marcet, Fleur Delva, Alexandra Foubert, Sandrine Cerda (Bordeaux); Marie-Noëlle-Cuffi, Corinne Costes (Castres); Olivier Rouaud, Patrick Manckoundia, Valérie Quipourt, Sophie Marilier, Evelyne Franon (Dijon); Lawrence Bories, Marie-Laure Pader, Marie-France Basset, Bruno Lapoujade, Valérie Faure, Michael Li Yung Tong, Christine Malick-Loiseau, Evelyne Cazaban-Campistron (Foix); Françoise Desclaux, Colette Blatge (Lavaur); Thierry Dantoine, Cécile Laubarie-Mouret, Isabelle Saulnier, Jean-Pierre Clément, Marie-Agnès Picat, Laurence Bernard-Bourzeix, Stéphanie Willebois, Iléana Désormais, Noëlle Cardinaud (Limoges); Marc Bonnefoy, Pierre Livet, Pascale Rebaudet, Claire Gédéon, Catherine Burdet, Flavien Terracol (Lyon), Alain Pesce, Stéphanie Roth, Sylvie Chaillou, Sandrine Louchart (Monaco); Kristel Sudres, Nicolas Lebrun, Nadège Barro-Belaygues (Montauban); Jacques Touchon, Karim Bennys, Audrey Gabelle, Aurélia Romano, Lynda Touati, Cécilia Marelli, Cécile Pays (Montpellier); Philippe Robert, Franck Le Duff, Claire Gervais, Sébastien Gonfrier (Nice); Yannick Gasnier and Serge Bordes, Danièle Begorre, Christian Carpuat, Khaled Khales, Jean-François Lefebvre, Samira Misbah El Idrissi, Pierre Skolil, Jean-Pierre Salles (Tarbes). MRI Group: Carole Dufouil (Bordeaux); Stéphane Lehéricy, Marie Chupin, Jean-François Mangin, Ali Bouhayia (Paris); Michèle Allard (Bordeaux); Frédéric Ricolfi (Dijon); Dominique Dubois (Foix); Marie Paule Bonceour Martel (Limoges); François Cotton (Lyon); Alain Bonafé (Montpellier); Stéphane Chanalet (Nice); Françoise Hugon (Tarbes); Fabrice Bonneville, Christophe Cognard, François Chollet (Toulouse). PET Scans Group: Pierre Payoux, Thierry Voisin, Julien Delrieu, Sophie Peiffer, Anne Hitzel, (Toulouse); Michèle Allard (Bordeaux); Michel Zanca (Montpellier); Jacques Monteil (Limoges); Jacques Darcourt (Nice). Medico-economics Group: Laurent Molinier, Hélène Derumeaux, and Nadège Costa (Toulouse). Biological Sample Collection: Bertrand Perret, Claire Vinel, and Sylvie Caspar-Bauguil (Toulouse). Safety Management: Pascale Olivier-Abbal. DSA Group: Sandrine Andrieu, Christelle Cantet, and Nicola Coley.

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Bencivenga, L., Strumia, M., Rolland, Y. et al. Biomarkers of mitochondrial dysfunction and inflammaging in older adults and blood pressure variability. GeroScience 45, 797–809 (2023). https://doi.org/10.1007/s11357-022-00697-y

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