Immune parameters identify Italian centenarians with a longer five-year survival independent of their health and functional status

L. Bucci, R. Ostan, E. Giampieri, E. Cevenini, E. Pini, M. Scurti, R. Vescovini, P. Sansoni, C. Caruso, D. Mari, F. Ronchetti, M. O. Borghi, G. Ogliari, C. Grossi, M. Capri, S. Salvioli, G. Castellani, C. Franceschi, D. Monti

Research output: Contribution to journalArticle

Abstract

Centenarians are rare and exceptional individuals characterized by a peculiar phenotype. They are the best example of healthy aging in humans as most of them have escaped or substantially delayed the onset of major age-related diseases. Within this scenario, the purpose of the present work was to understand if immune status is associated with survival and health status in centenarians. To this aim, 116 centenarians were concomitantly characterized for their immunological, health and functional status, and followed-up for five-year survival. On the basis of previous knowledge we focused on a core of fundamental and basic immune parameters (number of leukocytes, monocytes, total lymphocytes, CD3+ T lymphocytes, CD4+ helper T lymphocytes, CD8+ cytotoxic T lymphocytes, CD19+ B lymphocytes and plasma levels of IgM), and the most important findings can be summarized as follows: i. a hierarchical cluster analysis was able to define Cluster1 (88 centenarians) and Cluster2 (28 centenarians) characterized by low and high values of all these immune parameters, respectively; ii. centenarians of Cluster2 showed a statistically longer five-year survival and more favorable values of other important immune (naïve, activated/memory and effector/memory T cells) and metabolic (glycemia, insulin and HOMA-IR) parameters, in accord with previous observations that centenarians have a peculiar immune profile, a preserved insulin pathway and a lower incidence of type 2 diabetes; and iii. unexpectedly, parameters related to frailty, as well as functional and cognitive status, did not show any significant correlation with the immune clustering, despite being capable per se of predicting survival. In conclusion, high values of basic immunological parameters and important T cell subsets correlate with five-year survival in centenarians, independent of other phenotypic characteristics. This unexpected biological scenario is compatible with the general hypothesis that in centenarians a progressive disconnection and loss of biological coherence among the different functions of the body occur, where survival/mortality result from the failure of any of these domains which apparently follow an independent age-related trajectory.

Original languageEnglish
Pages (from-to)14-20
Number of pages7
JournalExperimental Gerontology
Volume54
DOIs
Publication statusPublished - 2014

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T-cells
Health Status
Health
Survival
Lymphocytes
Insulin
Data storage equipment
Cluster analysis
Medical problems
Cluster Analysis
Immunoglobulin M
Aging of materials
T-Lymphocytes
Trajectories
Plasmas
T-Lymphocyte Subsets
Cytotoxic T-Lymphocytes
Helper-Inducer T-Lymphocytes
Leukocyte Count
Age of Onset

Keywords

  • Centenarians
  • Cluster analysis
  • Health status
  • Immune system
  • Survival

ASJC Scopus subject areas

  • Ageing
  • Biochemistry
  • Cell Biology
  • Endocrinology
  • Genetics
  • Molecular Biology
  • Medicine(all)

Cite this

Immune parameters identify Italian centenarians with a longer five-year survival independent of their health and functional status. / Bucci, L.; Ostan, R.; Giampieri, E.; Cevenini, E.; Pini, E.; Scurti, M.; Vescovini, R.; Sansoni, P.; Caruso, C.; Mari, D.; Ronchetti, F.; Borghi, M. O.; Ogliari, G.; Grossi, C.; Capri, M.; Salvioli, S.; Castellani, G.; Franceschi, C.; Monti, D.

In: Experimental Gerontology, Vol. 54, 2014, p. 14-20.

Research output: Contribution to journalArticle

Bucci, L, Ostan, R, Giampieri, E, Cevenini, E, Pini, E, Scurti, M, Vescovini, R, Sansoni, P, Caruso, C, Mari, D, Ronchetti, F, Borghi, MO, Ogliari, G, Grossi, C, Capri, M, Salvioli, S, Castellani, G, Franceschi, C & Monti, D 2014, 'Immune parameters identify Italian centenarians with a longer five-year survival independent of their health and functional status', Experimental Gerontology, vol. 54, pp. 14-20. https://doi.org/10.1016/j.exger.2014.01.023
Bucci, L. ; Ostan, R. ; Giampieri, E. ; Cevenini, E. ; Pini, E. ; Scurti, M. ; Vescovini, R. ; Sansoni, P. ; Caruso, C. ; Mari, D. ; Ronchetti, F. ; Borghi, M. O. ; Ogliari, G. ; Grossi, C. ; Capri, M. ; Salvioli, S. ; Castellani, G. ; Franceschi, C. ; Monti, D. / Immune parameters identify Italian centenarians with a longer five-year survival independent of their health and functional status. In: Experimental Gerontology. 2014 ; Vol. 54. pp. 14-20.
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abstract = "Centenarians are rare and exceptional individuals characterized by a peculiar phenotype. They are the best example of healthy aging in humans as most of them have escaped or substantially delayed the onset of major age-related diseases. Within this scenario, the purpose of the present work was to understand if immune status is associated with survival and health status in centenarians. To this aim, 116 centenarians were concomitantly characterized for their immunological, health and functional status, and followed-up for five-year survival. On the basis of previous knowledge we focused on a core of fundamental and basic immune parameters (number of leukocytes, monocytes, total lymphocytes, CD3+ T lymphocytes, CD4+ helper T lymphocytes, CD8+ cytotoxic T lymphocytes, CD19+ B lymphocytes and plasma levels of IgM), and the most important findings can be summarized as follows: i. a hierarchical cluster analysis was able to define Cluster1 (88 centenarians) and Cluster2 (28 centenarians) characterized by low and high values of all these immune parameters, respectively; ii. centenarians of Cluster2 showed a statistically longer five-year survival and more favorable values of other important immune (na{\"i}ve, activated/memory and effector/memory T cells) and metabolic (glycemia, insulin and HOMA-IR) parameters, in accord with previous observations that centenarians have a peculiar immune profile, a preserved insulin pathway and a lower incidence of type 2 diabetes; and iii. unexpectedly, parameters related to frailty, as well as functional and cognitive status, did not show any significant correlation with the immune clustering, despite being capable per se of predicting survival. In conclusion, high values of basic immunological parameters and important T cell subsets correlate with five-year survival in centenarians, independent of other phenotypic characteristics. This unexpected biological scenario is compatible with the general hypothesis that in centenarians a progressive disconnection and loss of biological coherence among the different functions of the body occur, where survival/mortality result from the failure of any of these domains which apparently follow an independent age-related trajectory.",
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AU - Ostan, R.

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AU - Cevenini, E.

AU - Pini, E.

AU - Scurti, M.

AU - Vescovini, R.

AU - Sansoni, P.

AU - Caruso, C.

AU - Mari, D.

AU - Ronchetti, F.

AU - Borghi, M. O.

AU - Ogliari, G.

AU - Grossi, C.

AU - Capri, M.

AU - Salvioli, S.

AU - Castellani, G.

AU - Franceschi, C.

AU - Monti, D.

PY - 2014

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N2 - Centenarians are rare and exceptional individuals characterized by a peculiar phenotype. They are the best example of healthy aging in humans as most of them have escaped or substantially delayed the onset of major age-related diseases. Within this scenario, the purpose of the present work was to understand if immune status is associated with survival and health status in centenarians. To this aim, 116 centenarians were concomitantly characterized for their immunological, health and functional status, and followed-up for five-year survival. On the basis of previous knowledge we focused on a core of fundamental and basic immune parameters (number of leukocytes, monocytes, total lymphocytes, CD3+ T lymphocytes, CD4+ helper T lymphocytes, CD8+ cytotoxic T lymphocytes, CD19+ B lymphocytes and plasma levels of IgM), and the most important findings can be summarized as follows: i. a hierarchical cluster analysis was able to define Cluster1 (88 centenarians) and Cluster2 (28 centenarians) characterized by low and high values of all these immune parameters, respectively; ii. centenarians of Cluster2 showed a statistically longer five-year survival and more favorable values of other important immune (naïve, activated/memory and effector/memory T cells) and metabolic (glycemia, insulin and HOMA-IR) parameters, in accord with previous observations that centenarians have a peculiar immune profile, a preserved insulin pathway and a lower incidence of type 2 diabetes; and iii. unexpectedly, parameters related to frailty, as well as functional and cognitive status, did not show any significant correlation with the immune clustering, despite being capable per se of predicting survival. In conclusion, high values of basic immunological parameters and important T cell subsets correlate with five-year survival in centenarians, independent of other phenotypic characteristics. This unexpected biological scenario is compatible with the general hypothesis that in centenarians a progressive disconnection and loss of biological coherence among the different functions of the body occur, where survival/mortality result from the failure of any of these domains which apparently follow an independent age-related trajectory.

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