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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 |
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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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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.</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. Karger AG</publisher><subject>Aged ; Care and treatment ; Clinical Section: Research Article ; Diagnosis ; DNA viruses ; Health aspects ; Psychological aspects</subject><ispartof>Gerontology (Basel), 2023-06, Vol.69 (6), p.684-693</ispartof><rights>2023 S. Karger AG, Basel</rights><rights>2023 S. Karger AG, Basel.</rights><rights>COPYRIGHT 2023 S. Karger AG</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c400t-7c76910e0ffb9a017046eb7d45bd6f20e114fc35edfcfdb18cb59cb770e821203</citedby><orcidid>0000-0002-1796-7037 ; 0000-0001-9077-0401 ; 0000-0003-1069-2656 ; 0000-0001-6137-6544 ; 0000-0002-6743-014X ; 0000-0003-0650-8852 ; 0000-0001-8693-5250 ; 0000-0003-3949-395X ; 0000-0002-7084-946X ; 0000-0002-8442-1763 ; 0000-0003-3787-5268 ; 0000-0002-3151-5897 ; 0000-0002-6693-539X ; 0000-0002-5572-1089 ; 0000-0003-3069-0404 ; 0000-0001-7649-2599 ; 0000-0002-8011-5849 ; 0000-0003-4870-6515 ; 0000-0001-7971-8960</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,2423,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36538907$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Giacconi, Robertina</creatorcontrib><creatorcontrib>Laffon, Blanca</creatorcontrib><creatorcontrib>Costa, Solange</creatorcontrib><creatorcontrib>Teixeira-Gomes, Armanda</creatorcontrib><creatorcontrib>Maggi, Fabrizio</creatorcontrib><creatorcontrib>Macera, Lisa</creatorcontrib><creatorcontrib>Spezia, Pietro Giorgio</creatorcontrib><creatorcontrib>Piacenza, Francesco</creatorcontrib><creatorcontrib>Bürkle, Alexander</creatorcontrib><creatorcontrib>Moreno-Villanueva, María</creatorcontrib><creatorcontrib>Bonassi, Stefano</creatorcontrib><creatorcontrib>Valdiglesias, Vanessa</creatorcontrib><creatorcontrib>Teixeira, Joao Paulo</creatorcontrib><creatorcontrib>Dollé, Martijn E.T.</creatorcontrib><creatorcontrib>Rietman, M. 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 < 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.</description><subject>Aged</subject><subject>Care and treatment</subject><subject>Clinical Section: Research Article</subject><subject>Diagnosis</subject><subject>DNA viruses</subject><subject>Health aspects</subject><subject>Psychological aspects</subject><issn>0304-324X</issn><issn>1423-0003</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNpV0UGL1DAUB_Agiju7evAuEhBED9WXpm3a4zDs6sKCHkbxVtL0ZRptk5qkK4NffjPMOOglgT-_l7zkEfKCwXvGyuYDAJR5zarmEVmxIudZCvhjsgIORcbz4vsFuQzhRwohZ_CUXPCq5HUDYkX-rENwyshonKVO063zvxaMaN298Uug34zHyUj628SBfhn2wSg50hsvzRj3VNqebtzOmmjukd5OszR-QhupsXQ7eEyZ7XHGtKTwevFuRmlTyeB8DM_IEy3HgM9P-xX5enO93XzK7j5_vN2s7zJVAMRMKFE1DBC07hoJTEBRYSf6ouz6SueAjBVa8RJ7rXTfsVp1ZaM6IQDrnOXAr8jb47mzd-lxIbaTCQrHUVp0S2hzUVZVuqKuE319pDs5YmusdtFLdeDtWpQcSsHEQb35Rw0oxzgENy6HTwz_w3dHqLwLwaNuZ28m6fctg_YwuvY8umRfnbpcugn7s_w7qwReHsFP6Xfoz-BU_wArlpzz</recordid><startdate>20230601</startdate><enddate>20230601</enddate><creator>Giacconi, Robertina</creator><creator>Laffon, Blanca</creator><creator>Costa, Solange</creator><creator>Teixeira-Gomes, Armanda</creator><creator>Maggi, Fabrizio</creator><creator>Macera, Lisa</creator><creator>Spezia, Pietro Giorgio</creator><creator>Piacenza, Francesco</creator><creator>Bürkle, Alexander</creator><creator>Moreno-Villanueva, María</creator><creator>Bonassi, Stefano</creator><creator>Valdiglesias, Vanessa</creator><creator>Teixeira, Joao Paulo</creator><creator>Dollé, Martijn E.T.</creator><creator>Rietman, M. 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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 < 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.</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> |
fulltext | fulltext |
identifier | ISSN: 0304-324X |
ispartof | Gerontology (Basel), 2023-06, Vol.69 (6), p.684-693 |
issn | 0304-324X 1423-0003 |
language | eng |
recordid | cdi_pubmed_primary_36538907 |
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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