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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 ha...

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Published in:Gerontology (Basel) 2023-06, Vol.69 (6), p.684-693
Main Authors: Giacconi, Robertina, Laffon, Blanca, Costa, Solange, Teixeira-Gomes, Armanda, Maggi, Fabrizio, Macera, Lisa, Spezia, Pietro Giorgio, Piacenza, Francesco, Bürkle, Alexander, Moreno-Villanueva, María, Bonassi, Stefano, Valdiglesias, Vanessa, Teixeira, Joao Paulo, Dollé, Martijn E.T., Rietman, M. Liset, Jansen, Eugène, Grune, Tilman, Gonos, Efstathios S., Franceschi, Claudio, Capri, Miriam, Weinberger, Birgit, Sikora, Ewa, Stuetz, Wolfgang, Toussaint, Olivier, Debacq-Chainiaux, Florence, Hervonen, Antti, Hurme, Mikko, Slagboom, P. Eline, Schön, Christiane, Bernhardt, Jürgen, Breusing, Nicolle, Pásaro, Eduardo, Maseda, Ana, Lorenzo-López, Laura, Millán-Calenti, José Carlos, Provinciali, Mauro, Malavolta, Marco
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container_issue 6
container_start_page 684
container_title Gerontology (Basel)
container_volume 69
creator Giacconi, Robertina
Laffon, Blanca
Costa, Solange
Teixeira-Gomes, Armanda
Maggi, Fabrizio
Macera, Lisa
Spezia, Pietro Giorgio
Piacenza, Francesco
Bürkle, Alexander
Moreno-Villanueva, María
Bonassi, Stefano
Valdiglesias, Vanessa
Teixeira, Joao Paulo
Dollé, Martijn E.T.
Rietman, M. Liset
Jansen, Eugène
Grune, Tilman
Gonos, Efstathios S.
Franceschi, Claudio
Capri, Miriam
Weinberger, Birgit
Sikora, Ewa
Stuetz, Wolfgang
Toussaint, Olivier
Debacq-Chainiaux, Florence
Hervonen, Antti
Hurme, Mikko
Slagboom, P. Eline
Schön, Christiane
Bernhardt, Jürgen
Breusing, Nicolle
Pásaro, Eduardo
Maseda, Ana
Lorenzo-López, Laura
Millán-Calenti, José Carlos
Provinciali, Mauro
Malavolta, Marco
description 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.
doi_str_mv 10.1159/000528169
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Liset ; Jansen, Eugène ; Grune, Tilman ; Gonos, Efstathios S. ; Franceschi, Claudio ; Capri, Miriam ; Weinberger, Birgit ; Sikora, Ewa ; Stuetz, Wolfgang ; Toussaint, Olivier ; Debacq-Chainiaux, Florence ; Hervonen, Antti ; Hurme, Mikko ; Slagboom, P. Eline ; Schön, Christiane ; Bernhardt, Jürgen ; Breusing, Nicolle ; Pásaro, Eduardo ; Maseda, Ana ; Lorenzo-López, Laura ; Millán-Calenti, José Carlos ; Provinciali, Mauro ; Malavolta, Marco</creator><creatorcontrib>Giacconi, Robertina ; Laffon, Blanca ; Costa, Solange ; Teixeira-Gomes, Armanda ; Maggi, Fabrizio ; Macera, Lisa ; Spezia, Pietro Giorgio ; Piacenza, Francesco ; Bürkle, Alexander ; Moreno-Villanueva, María ; Bonassi, Stefano ; Valdiglesias, Vanessa ; Teixeira, Joao Paulo ; Dollé, Martijn E.T. ; Rietman, M. Liset ; Jansen, Eugène ; Grune, Tilman ; Gonos, Efstathios S. ; Franceschi, Claudio ; Capri, Miriam ; Weinberger, Birgit ; Sikora, Ewa ; Stuetz, Wolfgang ; Toussaint, Olivier ; Debacq-Chainiaux, Florence ; Hervonen, Antti ; Hurme, Mikko ; Slagboom, P. Eline ; Schön, Christiane ; Bernhardt, Jürgen ; Breusing, Nicolle ; Pásaro, Eduardo ; Maseda, Ana ; Lorenzo-López, Laura ; Millán-Calenti, José Carlos ; Provinciali, Mauro ; Malavolta, Marco</creatorcontrib><description>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 &lt; 0.0001) and cognitive impairment (OR: 3.49, 95% CI: 2.14–5.69, p &lt; 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.</description><identifier>ISSN: 0304-324X</identifier><identifier>EISSN: 1423-0003</identifier><identifier>DOI: 10.1159/000528169</identifier><identifier>PMID: 36538907</identifier><language>eng</language><publisher>Basel, Switzerland: S. 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Liset</creatorcontrib><creatorcontrib>Jansen, Eugène</creatorcontrib><creatorcontrib>Grune, Tilman</creatorcontrib><creatorcontrib>Gonos, Efstathios S.</creatorcontrib><creatorcontrib>Franceschi, Claudio</creatorcontrib><creatorcontrib>Capri, Miriam</creatorcontrib><creatorcontrib>Weinberger, Birgit</creatorcontrib><creatorcontrib>Sikora, Ewa</creatorcontrib><creatorcontrib>Stuetz, Wolfgang</creatorcontrib><creatorcontrib>Toussaint, Olivier</creatorcontrib><creatorcontrib>Debacq-Chainiaux, Florence</creatorcontrib><creatorcontrib>Hervonen, Antti</creatorcontrib><creatorcontrib>Hurme, Mikko</creatorcontrib><creatorcontrib>Slagboom, P. Eline</creatorcontrib><creatorcontrib>Schön, Christiane</creatorcontrib><creatorcontrib>Bernhardt, Jürgen</creatorcontrib><creatorcontrib>Breusing, Nicolle</creatorcontrib><creatorcontrib>Pásaro, Eduardo</creatorcontrib><creatorcontrib>Maseda, Ana</creatorcontrib><creatorcontrib>Lorenzo-López, Laura</creatorcontrib><creatorcontrib>Millán-Calenti, José Carlos</creatorcontrib><creatorcontrib>Provinciali, Mauro</creatorcontrib><creatorcontrib>Malavolta, Marco</creatorcontrib><title>Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts</title><title>Gerontology (Basel)</title><addtitle>Gerontology</addtitle><description>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 &lt; 0.0001) and cognitive impairment (OR: 3.49, 95% CI: 2.14–5.69, p &lt; 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. 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Liset</au><au>Jansen, Eugène</au><au>Grune, Tilman</au><au>Gonos, Efstathios S.</au><au>Franceschi, Claudio</au><au>Capri, Miriam</au><au>Weinberger, Birgit</au><au>Sikora, Ewa</au><au>Stuetz, Wolfgang</au><au>Toussaint, Olivier</au><au>Debacq-Chainiaux, Florence</au><au>Hervonen, Antti</au><au>Hurme, Mikko</au><au>Slagboom, P. Eline</au><au>Schön, Christiane</au><au>Bernhardt, Jürgen</au><au>Breusing, Nicolle</au><au>Pásaro, Eduardo</au><au>Maseda, Ana</au><au>Lorenzo-López, Laura</au><au>Millán-Calenti, José Carlos</au><au>Provinciali, Mauro</au><au>Malavolta, Marco</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts</atitle><jtitle>Gerontology (Basel)</jtitle><addtitle>Gerontology</addtitle><date>2023-06-01</date><risdate>2023</risdate><volume>69</volume><issue>6</issue><spage>684</spage><epage>693</epage><pages>684-693</pages><issn>0304-324X</issn><eissn>1423-0003</eissn><abstract>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 &lt; 0.0001) and cognitive impairment (OR: 3.49, 95% CI: 2.14–5.69, p &lt; 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.</abstract><cop>Basel, Switzerland</cop><pub>S. Karger AG</pub><pmid>36538907</pmid><doi>10.1159/000528169</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-1796-7037</orcidid><orcidid>https://orcid.org/0000-0001-9077-0401</orcidid><orcidid>https://orcid.org/0000-0003-1069-2656</orcidid><orcidid>https://orcid.org/0000-0001-6137-6544</orcidid><orcidid>https://orcid.org/0000-0002-6743-014X</orcidid><orcidid>https://orcid.org/0000-0003-0650-8852</orcidid><orcidid>https://orcid.org/0000-0001-8693-5250</orcidid><orcidid>https://orcid.org/0000-0003-3949-395X</orcidid><orcidid>https://orcid.org/0000-0002-7084-946X</orcidid><orcidid>https://orcid.org/0000-0002-8442-1763</orcidid><orcidid>https://orcid.org/0000-0003-3787-5268</orcidid><orcidid>https://orcid.org/0000-0002-3151-5897</orcidid><orcidid>https://orcid.org/0000-0002-6693-539X</orcidid><orcidid>https://orcid.org/0000-0002-5572-1089</orcidid><orcidid>https://orcid.org/0000-0003-3069-0404</orcidid><orcidid>https://orcid.org/0000-0001-7649-2599</orcidid><orcidid>https://orcid.org/0000-0002-8011-5849</orcidid><orcidid>https://orcid.org/0000-0003-4870-6515</orcidid><orcidid>https://orcid.org/0000-0001-7971-8960</orcidid><oa>free_for_read</oa></addata></record>
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source Karger Journals
subjects Aged
Care and treatment
Clinical Section: Research Article
Diagnosis
DNA viruses
Health aspects
Psychological aspects
title Association of Torquetenovirus Viremia with Physical Frailty and Cognitive Impairment in Three Independent European Cohorts
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