Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts

Robertina Giacconi; Blanca Laffon; Solange Costa; Armanda Teixeira-Gomes; Fabrizio Maggi; Lisa MacEra; Pietro Giorgio Spezia; Francesco Piacenza; Alexander Bürkle; María Moreno-Villanueva; Stefano Bonassi; Vanessa Valdiglesias; Joao Paulo Teixeira; Martijn E.T. Dollé; M. Liset Rietman; Eugène Jansen; Tilman Grune; Efstathios S. Gonos; Claudio Franceschi; Miriam Capri; Birgit Weinberger; Ewa Sikora; Wolfgang Stuetz; Olivier Toussaint; Florence Debacq-Chainiaux; Antti Hervonen; Mikko Hurme; P. Eline Slagboom; Christiane Schön; Jürgen Bernhardt; Nicolle Breusing; Eduardo Pásaro; Ana Maseda; Laura Lorenzo-López; José Carlos Millán-Calenti; Mauro Provinciali; Marco Malavolta

doi:10.1159/000528169

Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts

Robertina Giacconi, Blanca Laffon, Solange Costa, Armanda Teixeira-Gomes, Fabrizio Maggi, Lisa MacEra, Pietro Giorgio Spezia, Francesco Piacenza, Alexander Bürkle, María Moreno-Villanueva, Stefano Bonassi, Vanessa Valdiglesias, Joao Paulo Teixeira, Martijn E.T. Dollé, M. Liset Rietman, Eugène Jansen, Tilman Grune, Efstathios S. Gonos, Claudio Franceschi, Miriam CapriBirgit Weinberger, Ewa Sikora, Wolfgang Stuetz, Olivier Toussaint, Florence Debacq-Chainiaux, Antti Hervonen, Mikko Hurme, P. Eline Slagboom, Christiane Schön, Jürgen Bernhardt, Nicolle Breusing, Eduardo Pásaro, Ana Maseda, Laura Lorenzo-López, José Carlos Millán-Calenti, Mauro Provinciali, Marco Malavolta

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

Abstract

Introduction: Immunosenescence and inflammaging have been implicated in the pathophysiology of frailty. Torquetenovirus (TTV), a single-stranded DNA anellovirus, the major component of the human blood virome, shows an increased replication rate with advancing age. An elevated TTV viremia has been associated with an impaired immune function and an increased risk of mortality in the older population. The objective of this study was to analyze the relation between TTV viremia, physical frailty, and cognitive impairment. Methods: TTV viremia was measured in 1,131 nonfrail, 45 physically frail, and 113 cognitively impaired older adults recruited in the MARK-AGE study (overall mean age 64.7 ± 5.9 years), and then the results were checked in two other independent cohorts from Spain and Portugal, including 126 frail, 252 prefrail, and 141 nonfrail individuals (overall mean age: 77.5 ± 8.3 years). Results: TTV viremia ≥4log was associated with physical frailty (OR: 4.69; 95% CI: 2.06-10.67, p < 0.0001) and cognitive impairment (OR: 3.49, 95% CI: 2.14-5.69, p < 0.0001) in the MARK-AGE population. The association between TTV DNA load and frailty status was confirmed in the Spanish cohort, while a slight association with cognitive impairment was observed (OR: 1.33; 95% CI: 1.000-1.773), only in the unadjusted model. No association between TTV load and frailty or cognitive impairment was found in the Portuguese sample, although a negative association between TTV viremia and MMSE score was observed in Spanish and Portuguese females. Conclusions: These findings demonstrate an association between TTV viremia and physical frailty, while the association with cognitive impairment was observed only in the younger population from the MARK-AGE study. Further research is necessary to clarify TTV's clinical relevance in the onset and progression of frailty and cognitive decline in older individuals.

Original language	English
Pages (from-to)	684-693
Number of pages	10
Journal	Gerontology
Volume	69
Issue number	6
DOIs	https://doi.org/10.1159/000528169
Publication status	Published - 1 Jun 2023

Funding

This work was supported by the European Commission (Project Full Name: European Study to Establish Biomarkers of Human Ageing; Project Acronym: MARK-AGE; Project No. 200880) and in part by the Project: SInergie di RIcerca della Rete Aging (SIRI) by Italian Health Ministry. Support was also obtained from the Spanish Ministry of Science and Innovation: MCIN/AEI/10.13039/501100011033 (Grant PID2020-113788RB-I00), Xunta de Galicia (ED431B 2022/16, ED431F 2017/09), the Ministry of Education, Culture and Sport (BEAGAL18/00142 to V.V.), and the Spanish Ministry of Economy and Competitiveness, co-financed by the European Social Fund (RYC-2015-18394 to L.L-L). Armanda Gomes is supported by Funda\u00E7\u00E3o para a Ci\u00EAncia e Tecnologia (FCT-MCTES), and the European Social Fund, through Programa Operacional Capital Humano (POCH), under the Grant SFRH/BD/121802/2016.

Funders	Funder number
Fundação para a Ciência e a Tecnologia
Italian Health Ministry
Ministerio de Economía y Competitividad
European Commission
Ministerio de Educación, Cultura y Deporte	BEAGAL18/00142
Ministerio de Ciencia e Innovación	MCIN/AEI/10.13039/501100011033, PID2020-113788RB-I00
European Social Fund	RYC-2015-18394
Seventh Framework Programme	200880
FCT-MCTES	SFRH/BD/121802/2016
Xunta de Galicia	ED431F 2017/09, ED431B 2022/16

UN SDGs

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

SDG 3 Good Health and Well-being

Keywords

Aging
Cognitive impairment
Inflammation
Physical frailty
Torquetenovirus

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10.1159/000528169

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Giacconi, R., Laffon, B., Costa, S., Teixeira-Gomes, A., Maggi, F., MacEra, L., Spezia, P. G., Piacenza, F., Bürkle, A., Moreno-Villanueva, M., Bonassi, S., Valdiglesias, V., Teixeira, J. P., Dollé, M. E. T., Rietman, M. L., Jansen, E., Grune, T., Gonos, E. S., Franceschi, C., ... Malavolta, M. (2023). Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts. Gerontology, 69(6), 684-693. https://doi.org/10.1159/000528169

@article{3952aede443e4fa6b3b3ef1bf7ed5a89,

title = "Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts",

abstract = "Introduction: Immunosenescence and inflammaging have been implicated in the pathophysiology of frailty. Torquetenovirus (TTV), a single-stranded DNA anellovirus, the major component of the human blood virome, shows an increased replication rate with advancing age. An elevated TTV viremia has been associated with an impaired immune function and an increased risk of mortality in the older population. The objective of this study was to analyze the relation between TTV viremia, physical frailty, and cognitive impairment. Methods: TTV viremia was measured in 1,131 nonfrail, 45 physically frail, and 113 cognitively impaired older adults recruited in the MARK-AGE study (overall mean age 64.7 ± 5.9 years), and then the results were checked in two other independent cohorts from Spain and Portugal, including 126 frail, 252 prefrail, and 141 nonfrail individuals (overall mean age: 77.5 ± 8.3 years). Results: TTV viremia ≥4log was associated with physical frailty (OR: 4.69; 95\% CI: 2.06-10.67, p < 0.0001) and cognitive impairment (OR: 3.49, 95\% CI: 2.14-5.69, p < 0.0001) in the MARK-AGE population. The association between TTV DNA load and frailty status was confirmed in the Spanish cohort, while a slight association with cognitive impairment was observed (OR: 1.33; 95\% CI: 1.000-1.773), only in the unadjusted model. No association between TTV load and frailty or cognitive impairment was found in the Portuguese sample, although a negative association between TTV viremia and MMSE score was observed in Spanish and Portuguese females. Conclusions: These findings demonstrate an association between TTV viremia and physical frailty, while the association with cognitive impairment was observed only in the younger population from the MARK-AGE study. Further research is necessary to clarify TTV's clinical relevance in the onset and progression of frailty and cognitive decline in older individuals.",

keywords = "Aging, Cognitive impairment, Inflammation, Physical frailty, Torquetenovirus",

author = "Robertina Giacconi and Blanca Laffon and Solange Costa and Armanda Teixeira-Gomes and Fabrizio Maggi and Lisa MacEra and Spezia, \{Pietro Giorgio\} and Francesco Piacenza and Alexander B{\"u}rkle and Mar{\'i}a Moreno-Villanueva and Stefano Bonassi and Vanessa Valdiglesias and Teixeira, \{Joao Paulo\} and Doll{\'e}, \{Martijn E.T.\} and Rietman, \{M. Liset\} and Eug{\`e}ne Jansen and Tilman Grune and Gonos, \{Efstathios S.\} and Claudio Franceschi and Miriam Capri and Birgit Weinberger and Ewa Sikora and Wolfgang Stuetz and Olivier Toussaint and Florence Debacq-Chainiaux and Antti Hervonen and Mikko Hurme and Slagboom, \{P. Eline\} and Christiane Sch{\"o}n and J{\"u}rgen Bernhardt and Nicolle Breusing and Eduardo P{\'a}saro and Ana Maseda and Laura Lorenzo-L{\'o}pez and Mill{\'a}n-Calenti, \{Jos{\'e} Carlos\} and Mauro Provinciali and Marco Malavolta",

year = "2023",

month = jun,

day = "1",

doi = "10.1159/000528169",

language = "English",

volume = "69",

pages = "684--693",

journal = "Gerontology",

issn = "0304-324X",

publisher = "S. Karger AG",

number = "6",

}

Giacconi, R, Laffon, B, Costa, S, Teixeira-Gomes, A, Maggi, F, MacEra, L, Spezia, PG, Piacenza, F, Bürkle, A, Moreno-Villanueva, M, Bonassi, S, Valdiglesias, V, Teixeira, JP, Dollé, MET, Rietman, ML, Jansen, E, Grune, T, Gonos, ES, Franceschi, C, Capri, M, Weinberger, B, Sikora, E, Stuetz, W, Toussaint, O , Debacq-Chainiaux, F, Hervonen, A, Hurme, M, Slagboom, PE, Schön, C, Bernhardt, J, Breusing, N, Pásaro, E, Maseda, A, Lorenzo-López, L, Millán-Calenti, JC, Provinciali, M & Malavolta, M 2023, 'Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts', Gerontology, vol. 69, no. 6, pp. 684-693. https://doi.org/10.1159/000528169

TY - JOUR

T1 - Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts

AU - Giacconi, Robertina

AU - Laffon, Blanca

AU - Costa, Solange

AU - Teixeira-Gomes, Armanda

AU - Maggi, Fabrizio

AU - MacEra, Lisa

AU - Spezia, Pietro Giorgio

AU - Piacenza, Francesco

AU - Bürkle, Alexander

AU - Moreno-Villanueva, María

AU - Bonassi, Stefano

AU - Valdiglesias, Vanessa

AU - Teixeira, Joao Paulo

AU - Dollé, Martijn E.T.

AU - Rietman, M. Liset

AU - Jansen, Eugène

AU - Grune, Tilman

AU - Gonos, Efstathios S.

AU - Franceschi, Claudio

AU - Capri, Miriam

AU - Weinberger, Birgit

AU - Sikora, Ewa

AU - Stuetz, Wolfgang

AU - Toussaint, Olivier

AU - Debacq-Chainiaux, Florence

AU - Hervonen, Antti

AU - Hurme, Mikko

AU - Slagboom, P. Eline

AU - Schön, Christiane

AU - Bernhardt, Jürgen

AU - Breusing, Nicolle

AU - Pásaro, Eduardo

AU - Maseda, Ana

AU - Lorenzo-López, Laura

AU - Millán-Calenti, José Carlos

AU - Provinciali, Mauro

AU - Malavolta, Marco

PY - 2023/6/1

Y1 - 2023/6/1

N2 - Introduction: Immunosenescence and inflammaging have been implicated in the pathophysiology of frailty. Torquetenovirus (TTV), a single-stranded DNA anellovirus, the major component of the human blood virome, shows an increased replication rate with advancing age. An elevated TTV viremia has been associated with an impaired immune function and an increased risk of mortality in the older population. The objective of this study was to analyze the relation between TTV viremia, physical frailty, and cognitive impairment. Methods: TTV viremia was measured in 1,131 nonfrail, 45 physically frail, and 113 cognitively impaired older adults recruited in the MARK-AGE study (overall mean age 64.7 ± 5.9 years), and then the results were checked in two other independent cohorts from Spain and Portugal, including 126 frail, 252 prefrail, and 141 nonfrail individuals (overall mean age: 77.5 ± 8.3 years). Results: TTV viremia ≥4log was associated with physical frailty (OR: 4.69; 95% CI: 2.06-10.67, p < 0.0001) and cognitive impairment (OR: 3.49, 95% CI: 2.14-5.69, p < 0.0001) in the MARK-AGE population. The association between TTV DNA load and frailty status was confirmed in the Spanish cohort, while a slight association with cognitive impairment was observed (OR: 1.33; 95% CI: 1.000-1.773), only in the unadjusted model. No association between TTV load and frailty or cognitive impairment was found in the Portuguese sample, although a negative association between TTV viremia and MMSE score was observed in Spanish and Portuguese females. Conclusions: These findings demonstrate an association between TTV viremia and physical frailty, while the association with cognitive impairment was observed only in the younger population from the MARK-AGE study. Further research is necessary to clarify TTV's clinical relevance in the onset and progression of frailty and cognitive decline in older individuals.

AB - Introduction: Immunosenescence and inflammaging have been implicated in the pathophysiology of frailty. Torquetenovirus (TTV), a single-stranded DNA anellovirus, the major component of the human blood virome, shows an increased replication rate with advancing age. An elevated TTV viremia has been associated with an impaired immune function and an increased risk of mortality in the older population. The objective of this study was to analyze the relation between TTV viremia, physical frailty, and cognitive impairment. Methods: TTV viremia was measured in 1,131 nonfrail, 45 physically frail, and 113 cognitively impaired older adults recruited in the MARK-AGE study (overall mean age 64.7 ± 5.9 years), and then the results were checked in two other independent cohorts from Spain and Portugal, including 126 frail, 252 prefrail, and 141 nonfrail individuals (overall mean age: 77.5 ± 8.3 years). Results: TTV viremia ≥4log was associated with physical frailty (OR: 4.69; 95% CI: 2.06-10.67, p < 0.0001) and cognitive impairment (OR: 3.49, 95% CI: 2.14-5.69, p < 0.0001) in the MARK-AGE population. The association between TTV DNA load and frailty status was confirmed in the Spanish cohort, while a slight association with cognitive impairment was observed (OR: 1.33; 95% CI: 1.000-1.773), only in the unadjusted model. No association between TTV load and frailty or cognitive impairment was found in the Portuguese sample, although a negative association between TTV viremia and MMSE score was observed in Spanish and Portuguese females. Conclusions: These findings demonstrate an association between TTV viremia and physical frailty, while the association with cognitive impairment was observed only in the younger population from the MARK-AGE study. Further research is necessary to clarify TTV's clinical relevance in the onset and progression of frailty and cognitive decline in older individuals.

KW - Aging

KW - Cognitive impairment

KW - Inflammation

KW - Physical frailty

KW - Torquetenovirus

UR - https://www.scopus.com/pages/publications/85163220706

U2 - 10.1159/000528169

DO - 10.1159/000528169

M3 - Article

C2 - 36538907

AN - SCOPUS:85163220706

SN - 0304-324X

VL - 69

SP - 684

EP - 693

JO - Gerontology

JF - Gerontology

IS - 6

ER -

Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts

Abstract

Funding

UN SDGs

Keywords

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