1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Nutrition
  4. Volume 38, 2018
  5. Article

Annual Review of Nutrition

Volume 38, 2018

Nutrition and Inflammation: Are Centenarians Similar to Individuals on Calorie-Restricted Diets?

Abstract

Individuals capable of reaching the extreme limit of human life such as centenarians are characterized by an exceptionally healthy phenotype—that is, a low number of diseases, low blood pressure, optimal metabolic and endocrine parameters, and increased diversity in the gut microbiota—and they are epigenetically younger than their chronological age. We present data suggesting that such a remarkable phenotype is largely similar to that found in adults following a calorie-restricted diet. Interviews with centenarians and historical data on the nutritional and lifestyle habits of Italians during the twentieth century suggest that as children and into adulthood, centenarians lived in an environment that was nonobesogenic, but at the same time the environment did not produce malnutrition. Centenarians appear to be creatures of habit, and we argue that their habit of eating meals at the same time each day favored the maintenance of circadian rhythms, including their sleep cycle. Finally, we argue that centenarians’ chronic inflammatory status, which we dubbed inflammaging, is peculiar, likely adaptive, and less detrimental than in younger people.

Keyword(s): calorie restriction, centenarians, circadian rhythms, inflammaging, longevity, nutrition
Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-082117-051637
2018-08-21
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/nutr/38/1/annurev-nutr-082117-051637.html?itemId=/content/journals/10.1146/annurev-nutr-082117-051637&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Arai Y, Hirose N, Nakazawa S, Yamamura K, Shimizu KI et al. 2001. Lipoprotein metabolism in Japanese centenarians: effects of apolipoprotein E polymorphism and nutritional status. J. Am. Geriatr. Soc. 49:111434–41
     [Google Scholar]
  2. 2.  Atzmon G, Barzilai N, Hollowell JG, Surks MI, Gabriely I 2009. Extreme longevity is associated with increased serum thyrotropin. J. Clin. Endocrinol. Metab. 94:41251–54
     [Google Scholar]
  3. 3.  Baggio G, Donazzan S, Monti D, Mari D, Martini S et al. 1998. Lipoprotein(a) and lipoprotein profile in healthy centenarians: a reappraisal of vascular risk factors. FASEB J 12:6433–37
     [Google Scholar]
  4. 4.  Baranowska B, Bik W, Baranowska-Bik A, Wolinska-Witort E, Szybinska A et al. 2006. Neuroendocrine control of metabolic homeostasis in Polish centenarians. J. Physiol. Pharmacol. 57:Suppl. 655–61
     [Google Scholar]
  5. 5.  Barbieri B 1961. I consumi del primo secolo dell'Unità d'Italia (1861–1961) [Consumption during the first century of the Unification of Italy (1861–1961)] Milan: Giuffrè
     [Google Scholar]
  6. 6.  Barzilai N, Huffman DM, Muzumdar RH BA 2012. The critical role of metabolic pathways in aging. Diabetes 61:61315–22
     [Google Scholar]
  7. 7.  Bellavia D, Fradà G, Di Franco P, Feo S, Franceschi C et al. 1999. C4, BF, C3 allele distribution and complement activity in healthy aged people and centenarians. J. Gerontol. A Biol. Sci. Med. Sci. 54:4B150–53
     [Google Scholar]
  8. 8.  Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R et al. 2016. Gut microbiota and extreme longevity. Curr. Biol. 26:111480–85
     [Google Scholar]
  9. 9.  Biagi E, Nylund L, Candela M, Ostan R, Bucci L et al. 2010. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLOS ONE 5:5e10667
     [Google Scholar]
  10. 10.  Bik W, Baranowska-Bik A, Wolinska-Witort E, Kalisz M, Broczek K et al. 2013. Assessment of adiponectin and its isoforms in Polish centenarians. Exp. Gerontol. 48:401–7
     [Google Scholar]
  11. 11.  Braghin P 1978. Inchiesta sulla miseria (1951–1952) [Inquiry on misery (1951–1952)] Turin: Piccola Bibl. Einaudi
     [Google Scholar]
  12. 12.  Bruunsgaard H, Andersen-Ranberg K, Jeune B, Pedersen AN, Skinhoj P, Pedersen BK 1999. A high plasma concentration of TNF-α is associated with dementia in centenarians. J. Gerontol. A Biol. Sci. Med. Sci. 54:7M357–64
     [Google Scholar]
  13. 13.  Calder PC, Bosco N, Bourdet-Sicard R, Capuron L, Delzenne N et al. 2017. Health relevance of the modification of low grade inflammation in ageing (inflammageing) and the role of nutrition. Ageing Res. Rev. 40:95–119
     [Google Scholar]
  14. 14.  Capri M, Santoro A, Garagnani P, Bacalini MG, Pirazzini C et al. 2014. Genes of human longevity: an endless quest?. Curr. Vasc. Pharmacol. 12:5707–17
     [Google Scholar]
  15. 15.  Carrieri G, Bonafè M, De Luca M, Rose G, Varcasia O et al. 2001. Mitochondrial DNA haplogroups and APOE4 allele are non-independent variables in sporadic Alzheimer's disease. Hum. Genet. 108:3194–98
     [Google Scholar]
  16. 16.  Carroll JE, Irwin MR, Levine M, Seeman TE, Absher D et al. 2017. Epigenetic aging and immune senescence in women with insomnia symptoms: findings from the Women's Health Initiative Study. Biol. Psychiatry 81:2136–44
     [Google Scholar]
  17. 17.  Chang-Quan H, Bi-Rong D, Yan Z 2012. Association between sleep quality and cognitive impairment among Chinese nonagenarians/centenarians. J. Clin. Neurophysiol. 29:3250–55
     [Google Scholar]
  18. 18.  Collino S, Montoliu I, Martin FPJ, Scherer M, Mari D et al. 2013. Metabolic signatures of extreme longevity in Northern Italian centenarians reveal a complex remodeling of lipids, amino acids, and gut microbiota metabolism. PLOS ONE 8:3e56564
     [Google Scholar]
  19. 19.  Coppola R, Mari D, Lattuada A, Franceschi C 2003. Von Willebrand factor in Italian centenarians. Haematologica 88:139–43
     [Google Scholar]
  20. 20.  Cossarizza A, Ortolani C, Paganelli R, Barbieri D, Monti D et al. 1996. CD45 isoforms expression on CD4+ and CD8+ T cells throughout life, from newborns to centenarians: implications for T cell memory. Mech. Ageing Dev. 86:3173–95
     [Google Scholar]
  21. 21.  Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U 2000. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–61
     [Google Scholar]
  22. 22.  Das SK, Balasubramanian P, Weerasekara YK 2017. Nutrition modulation of human aging: the calorie restriction paradigm. Mol. Cell. Endocrinol. 455:148–57
     [Google Scholar]
  23. 23.  Dato S, Rose G, Crocco P, Monti D, Garagnani P et al. 2017. The genetics of human longevity: an intricacy of genes, environment, culture and microbiome. Mech. Ageing Dev. 165:147–55
     [Google Scholar]
  24. 24.  De Bernardi A 2015. I consumi alimentari in Italia: uno specchio del cambiamento [Food consumption in Italy: a mirror of change] Rome: Treccani http://www.treccani.it/enciclopedia/i-consumi-alimentari-in-italia-uno-specchio-del-cambiamento_%28L%27Italia-e-le-sue-Regioni%29/
    [Google Scholar]
  25. 25.  Doyle S, Menaker M 2007. Circadian photoreception in vertebrates. Cold Spring Harb. Symp. Quant. Biol. 72:1499–508
     [Google Scholar]
  26. 26.  Ershler WB 1993. Interleukin-6: a cytokine for gerontologists. J. Am. Geriatr. Soc. 41:2176–81
     [Google Scholar]
  27. 27.  Fagnoni FF, Vescovini R, Mazzola M, Bologna G, Nigro E et al. 1996. Expansion of cytotoxic CD8+ CD28− T cells in healthy ageing people, including centenarians. Immunology 88:4501–7
     [Google Scholar]
  28. 28.  Fagnoni FF, Vescovini R, Passeri G, Bologna G, Pedrazzoni M et al. 2000. Shortage of circulating naive CD8+ T cells provides new insights on immunodeficiency in aging. Blood 95:92860–68
     [Google Scholar]
  29. 29.  Fetissov SO 2016. Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour. Nat. Rev. Endocrinol. 13:111–25
     [Google Scholar]
  30. 30.  Fontana L, Klein S, Holloszy JO, Premachandra BN 2006. Effect of long-term calorie restriction with adequate protein and micronutrients on thyroid hormones. J. Clin. Endocrinol. Metab. 91:83232–35
     [Google Scholar]
  31. 31.  Fontana L, Partridge L, Longo VD 2010. Extending healthy life span—from yeast to humans. Science 328:5976321–26
     [Google Scholar]
  32. 32.  Fontana L, Villareal DT, Das SK, Smith SR, Meydani SN et al. 2016. Effects of 2-year calorie restriction on circulating levels of IGF-1, IGF-binding proteins and cortisol in nonobese men and women: a randomized clinical trial. Aging Cell 15:122–27
     [Google Scholar]
  33. 33.  Fontana L, Villareal DT, Weiss EP, Racette SB, Steger-May K et al. 2007. Calorie restriction or exercise: effects on coronary heart disease risk factors. A randomized, controlled trial. Am. J. Physiol. Endocrinol. Metab. 293:1E197–202
     [Google Scholar]
  34. 34.  Fontana L, Weiss EP, Villareal DT, Klein S, Holloszy JO 2008. Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Aging Cell 7:5681–87
     [Google Scholar]
  35. 35.  Franceschi C 2017. Obesity in geroscience—is cellular senescence the culprit?. Nat. Rev. Endocrinol. 13:276–78
     [Google Scholar]
  36. 36.  Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M et al. 2000. Inflamm-aging: an evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 908:244–54
     [Google Scholar]
  37. 37.  Franceschi C, Campisi J 2014. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol. A Biol. Sci. Med. Sci. 69:Suppl. 1S4–9
     [Google Scholar]
  38. 38.  Franceschi C, Capri M, Monti D, Giunta S, Olivieri F et al. 2007. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 128:192–105
     [Google Scholar]
  39. 39.  Franceschi C, Garagnani P, Vitale G, Capri M, Salvioli S 2017. Inflammaging and ‘garb-aging.’ Trends Endocrinol. . Metab 28:3199–212
     [Google Scholar]
  40. 40.  Franceschi C, Passarino G, Mari D, Monti D 2017. Centenarians as a 21st century healthy aging model: a legacy of humanity and the need for a world-wide consortium (WWC100+). Mech. Ageing Dev. 165:Pt. B55–58
     [Google Scholar]
  41. 41.  Franceschi C, Salvioli S, Garagnani P, de Eguileor M, Monti D, Capri M 2017. Immunobiography and the heterogeneity of immune responses in the elderly: a focus on inflammaging and trained immunity. Front. Immunol. 8:982
     [Google Scholar]
  42. 42.  Franceschi C, Valensin S, Bonafè M, Paolisso G, Yashin AI et al. 2000. The network and the remodeling theories of aging: historical background and new perspectives. Exp. Gerontol. 35:6–7879–96
     [Google Scholar]
  43. 43.  Fransen F, van Beek AA, Borghuis T, El Aidy S, Hugenholtz F et al. 2017. Aged gut microbiota contributes to systemical inflammaging after transfer to germ-free mice. Front. Immunol. 8:1385
     [Google Scholar]
  44. 44.  Fulop T, Larbi A, Dupuis G, Le Page A, Frost E et al. 2018. Immunosenescence and inflamm-aging as two sides of the same coin: friends or foes?. Front. Immunol. 8:1960
     [Google Scholar]
  45. 45.  Gangemi S, Basile G, Merendino RA, Minciullo PL, Novick D et al. 2003. Increased circulating interleukin-18 levels in centenarians with no signs of vascular disease: another paradox of longevity?. Exp. Gerontol. 38:6669–72
     [Google Scholar]
  46. 46.  Gangemi S, Basile G, Monti D, Merendino RA, Di Pasquale G et al. 2005. Age-related modifications in circulating IL-15 levels in humans. Mediators Inflamm 2005:4245–47
     [Google Scholar]
  47. 47.  Gareri P, Lacava R, Rossi MG, Iorio C, Galasso MA et al. 1996. Hypertension in a group of centenarians. Arch. Gerontol. Geriatr. 22:Suppl. 1373–76
     [Google Scholar]
  48. 48.  Genedani S, Filaferro M, Carone C, Ostan R, Bucci L et al. 2008. Influence of f-MLP, ACTH(1–24) and CRH on in vitro chemotaxis of monocytes from centenarians. Neuroimmunomodulation 15:4–6285–89
     [Google Scholar]
  49. 49.  Gerli R, Monti D, Bistoni O, Mazzone AM, Peri G et al. 2000. Chemokines, sTNF-Rs and sCD30 serum levels in healthy aged people and centenarians. Mech. Ageing Dev. 121:37–46
     [Google Scholar]
  50. 50.  Giuliani N, Sansoni P, Girasole G, Vescovini R, Passeri G et al. 2001. Serum interleukin-6, soluble interleukin-6 receptor and soluble gp130 exhibit different patterns of age- and menopause-related changes. Exp. Gerontol. 36:36547–57
     [Google Scholar]
  51. 51.  Govindarajan K, MacSharry J, Casey PG, Shanahan F, Joyce SA, Gahan CGM 2016. Unconjugated bile acids influence expression of circadian genes: a potential mechanism for microbe–host crosstalk. PLOS ONE 11:12e0167319
     [Google Scholar]
  52. 52.  Guillaumond F, Dardente H, Giguere VCN 2005. Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J. Biol. Rhythms 20:391–403
     [Google Scholar]
  53. 53.  He Y, Chen X, Yan D, Xiao F, Liu Y et al. 2015. Thyroid function decreases with age and may contribute to longevity in Chinese centenarians’ families. J. Am. Geriatr. Soc. 63:71474–76
     [Google Scholar]
  54. 54.  Heilbronn LK, de Jonge L, Frisard MI, DeLany JP, Larson-Meyer DE et al. 2006. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals. JAMA 295:131539–48
     [Google Scholar]
  55. 55.  Horvath S, Pirazzini C, Bacalini MG, Gentilini D, Di Blasio AM et al. 2015. Decreased epigenetic age of PBMCs from Italian semi-supercentenarians and their offspring. Aging 7:121159–70
     [Google Scholar]
  56. 56.  Irwin MR, Opp MR 2017. Sleep health: reciprocal regulation of sleep and innate immunity. Neuropsychopharmacology 42:1129–55
     [Google Scholar]
  57. 57. ISTAT (Ist. Naz. Stat.). 1958. Sommario di statistiche storiche italiane, 1861–1955 [Summary of Italian historical statistics, 1861–1955] Rome: ISTAT. http://www.istat.it/it/files/2011/03/sommariostatistichestoriche1861-1955.pdf
    [Google Scholar]
  58. 58. ISTAT (Ist. Naz. Stat.). 2016. Bilancio demografico nazionale: anno 2015 [National demographic balance: year 2015] Rome: ISTAT http://www.istat.it/it/files/2016/06/Bilancio-demografico-2015-1.pdf?title=Bilancio+demografico+nazionale+-+10%2Fgiu%2F2016+-+Testo+integrale.pdf
    [Google Scholar]
  59. 59. ISTAT (Ist. Naz. Stat.). 2018. Serie storiche: sanità e salute Rome: ISTAT http://seriestoriche.istat.it/index.php?id=1&no_cache=1&tx_usercento_centofe%5Bcategoria%5D=4&tx_usercento_centofe%5Baction%5D=show&tx_usercento_centofe%5Bcontroller%5D=Categoria&cHash=8664faf9f1b9afc9dd19013b95483b35
  60. 60.  Johnston JD 2014. Physiological responses to food intake throughout the day. Nutr. Rev. 27:107–18
     [Google Scholar]
  61. 61.  Johnston JD, Ordovás JM, Scheer FA, Turek FW 2016. Circadian rhythms, metabolism, and chrononutrition in rodents. Adv. Nutr. 7:399–406
     [Google Scholar]
  62. 62.  Katewa SD, Akagi K, Bose N, Rakshit K, Camarella T et al. 2016. Peripheral circadian clocks mediate dietary restriction–dependent changes in lifespan and fat metabolism in Drosophila. . Cell Metab 23:1143–54
     [Google Scholar]
  63. 63.  Kennedy BK, Berger SL, Brunet A, Campisi J, Cuervo AM et al. 2014. Geroscience: linking aging to chronic disease. Cell 159:709–13
     [Google Scholar]
  64. 64.  Kheirbek RE, Fokar A, Shara N, Bell-Wilson LK, Moore HJ et al. 2017. Characteristics and incidence of chronic illness in community-dwelling predominantly male U.S. veteran centenarians. J. Am. Geriatr. Soc. 65:92100–6
     [Google Scholar]
  65. 65.  Korre M, Tsoukas MA, Frantzeskou E, Yang J, Kales SN 2014. Mediterranean diet and workplace health promotion. Curr. Cardiovasc. Risk Rep. 8:12416
     [Google Scholar]
  66. 66.  Lecoultre V, Ravussin E, Redman LM 2011. The fall in leptin concentration is a major determinant of the metabolic adaptation induced by caloric restriction independently of the changes in leptin circadian rhythms. J. Clin. Endocrinol. Metab. 96:9E1512–16
     [Google Scholar]
  67. 67.  Lee C, Longo VD 2016. Dietary restriction with and without caloric restriction for healthy aging. F1000Research 5:F1000 Faculty Rev.117
     [Google Scholar]
  68. 68.  Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY et al. 2015. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17:5681–89
     [Google Scholar]
  69. 69.  Lio D, Malaguarnera M, Maugeri D, Ferlito L, Bennati E et al. 2008. Laboratory parameters in centenarians of Italian ancestry. Exp. Gerontol. 43:2119–22
     [Google Scholar]
  70. 70.  Lockley SW, Arendt J, Skene DJ 2007. Visual impairment and circadian rhythm disorders. Dialogues Clin. Neurosci. 9:301–14
     [Google Scholar]
  71. 71.  Loft S, Velthuis-te Wierik EJ, van den Berg H, Poulsen HE 1995. Energy restriction and oxidative DNA damage in humans. Cancer Epidemiol. Biomarkers Prev. 4:5515–19
     [Google Scholar]
  72. 72.  Lopez-Legarrea P, Fuller NR, Zulet MA, Martinez JA, Caterson ID 2014. The influence of Mediterranean, carbohydrate and high protein diets on gut microbiota composition in the treatment of obesity and associated inflammatory state. Asia Pac. J. Clin. Nutr. 23:3360–68
     [Google Scholar]
  73. 73.  Magri F, Sarra S, Cinchetti W, Guazzoni V, Fioravanti M et al. 2004. Qualitative and quantitative changes of melatonin levels in physiological and pathological aging and in centenarians. J. Pineal Res. 36:4256–61
     [Google Scholar]
  74. 74.  Mari D, Mannucci PM, Coppola R, Bottasso B, Bauer KA, Rosenberg RD 1995. Hypercoagulability in centenarians: the paradox of successful aging. Blood 85:113144–49
     [Google Scholar]
  75. 75.  Mariotti S, Barbesino G, Caturegli P, Bartalena L, Sansoni P et al. 1993. Complex alteration of thyroid function in healthy centenarians. J. Clin. Endocrinol. Metab. 77:51130–34
     [Google Scholar]
  76. 76.  Mariotti S, Sansoni P, Barbesino G, Caturegli P, Monti D et al. 1992. Thyroid and other organ-specific autoantibodies in healthy centenarians. Lancet 339:88081506–8
     [Google Scholar]
  77. 77.  Martucci M, Ostan R, Biondi F, Bellavista E, Fabbri C et al. 2017. Mediterranean diet and inflammaging within the hormesis paradigm. Nutr. Rev. 75:6442–55
     [Google Scholar]
  78. 78.  Mattison J, Colman R, Beasley T, Allison D, Kemnitz J et al. 2017. Caloric restriction improves health and survival of rhesus monkeys. Nat. Commun. 8:14063
     [Google Scholar]
  79. 79.  Mazzotti DR, Guindalini C, Moraes WA, Andersen ML, Cendoroglo MS et al. 2014. Human longevity is associated with regular sleep patterns, maintenance of slow wave sleep, and favorable lipid profile. Front. Aging Neurosci. 6:134
     [Google Scholar]
  80. 80.  Mendoza J, Graff C, Dardente H, Pevet P, Challet E 2005. Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle. J. Neurosci. 25:1514–22
     [Google Scholar]
  81. 81.  Meroni PL, Mari D, Monti D, Coppola R, Capri M et al. 2004. Anti-β2 glycoprotein I antibodies in centenarians. Exp. Gerontol. 39:101459–65
     [Google Scholar]
  82. 82.  Metchnikoff I 1908. The Prolongation of Life: Optimistic Studies New York/London: Putnam's
  83. 83.  Meydani SN, Das SK, Pieper CF, Lewis MR, Klein S et al. 2016. Long-term moderate calorie restriction inhibits inflammation without impairing cell-mediated immunity: a randomized controlled trial in non-obese humans. Aging 8:71416–31
     [Google Scholar]
  84. 84.  Mirzaei H, Suarez JA, Longo VD 2014. Protein and amino acid restriction, aging and disease: from yeast to humans. Trends Endocrinol. Metab. 25:11558–66
     [Google Scholar]
  85. 85.  Mitchell SJ, Madrigal-Matute J, Scheibye-Knudsen M, Fang E, Aon M et al. 2016. Effects of sex, strain, and energy intake on hallmarks of aging in mice. Cell Metab 23:1093–112
     [Google Scholar]
  86. 86.  Miura Y, Hashii N, Tsumoto H, Takakura D, Ohta Y et al. 2015. Change in N-glycosylation of plasma proteins in Japanese semisupercentenarians. PLOS ONE 10:11e0142645
     [Google Scholar]
  87. 87.  Mohawk JA, Green CB, Takahashi JS 2012. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35:1445–62
     [Google Scholar]
  88. 88.  Montanari M 2010. L'identità italiana in cucina [Italian identity in cooking] Rome: Laterza
     [Google Scholar]
  89. 89.  Montoliu I, Scherer M, Beguelin F, DaSilva L, Mari D et al. 2014. Serum profiling of healthy aging identifies phospho- and sphingolipid species as markers of human longevity. Aging 6:19–25
     [Google Scholar]
  90. 90.  Morgan L, Hampton S, Gibbs M, Arendt J 2003. Circadian aspects of postprandial metabolism. Chronobiol. Int. 20:795–808
     [Google Scholar]
  91. 91.  Morrisette-Thomas V, Cohen AA, Fulop T, Riesco E, Legault V et al. 2014. Inflamm-aging does not simply reflect increases in pro-inflammatory markers. Mech. Ageing Dev. 139:49–57
     [Google Scholar]
  92. 92.  Most J, Tosti V, Redman LM, Fontana L 2016. Calorie restriction in humans: an update. Ageing Res. Rev. 39:36–45
     [Google Scholar]
  93. 93.  Mukherji A, Kobiita A, Ye T, Chambon P 2013. Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153:4812–27
     [Google Scholar]
  94. 94.  Nasi M, Troiano L, Lugli E, Pinti M, Ferraresi R et al. 2006. Thymic output and functionality of the IL-7/IL-7 receptor system in centenarians: implications for the neolymphogenesis at the limit of human life. Aging Cell 5:2167–75
     [Google Scholar]
  95. 95.  Ostan R, Bucci L, Capri M, Salvioli S, Scurti M et al. 2008. Immunosenescence and immunogenetics of human longevity. Neuroimmunomodulation 15:4–6224–40
     [Google Scholar]
  96. 96.  Ostan R, Lanzarini C, Pini E, Scurti M, Vianello D et al. 2015. Inflammaging and cancer: a challenge for the Mediterranean diet. Nutrients 7:42589–621
     [Google Scholar]
  97. 97.  Ostan R, Monti D, Gueresi P, Bussolotto M, Franceschi C, Baggio G 2016. Gender, aging and longevity in humans: an update of an intriguing/neglected scenario paving the way to a gender-specific medicine. Clin. Sci. 130:191711–25
     [Google Scholar]
  98. 98.  Pallauf K, Giller K, Huebbe P, Rimbach G 2013. Nutrition and healthy ageing: calorie restriction or polyphenol-rich “MediterrAsian” diet?. Oxidative Med. Cell. Longev. 2013:707421
     [Google Scholar]
  99. 99.  Paolisso G, Ammendola S, Del Buono A, Gambardella A, Riondino M et al. 1997. Serum levels of insulin-like growth factor-I (IGF-I) and IGF-binding protein-3 in healthy centenarians: relationship with plasma leptin and lipid concentrations, insulin action, and cognitive function. J. Clin. Endocrinol. Metab. 82:72204–9
     [Google Scholar]
  100. 100.  Paolisso G, Barbieri M, Rizzo MR, Carella C, Rotondi M et al. 2001. Low insulin resistance and preserved β-cell function contribute to human longevity but are not associated with TH–INS genes. Exp. Gerontol. 37:149–56
     [Google Scholar]
  101. 101.  Paolisso G, Gambardella A, Ammendola S, D'Amore A, Balbi V et al. 1996. Glucose tolerance and insulin action in healthy centenarians. Am. J. Physiol. 270:5E890–94
     [Google Scholar]
  102. 102.  Paschos GK, FitzGerald GA 2017. Circadian clocks and metabolism: implications for microbiome and aging. Trends Genet 33:10760–69
     [Google Scholar]
  103. 103.  Passeri G, Pini G, Troiano L, Vescovini R, Sansoni P et al. 2003. Low vitamin D status, high bone turnover, and bone fractures in centenarians. J. Clin. Endocrinol. Metab. 88:115109–15
     [Google Scholar]
  104. 104.  Pinti M, Cevenini E, Nasi M, De Biasi S, Salvioli S et al. 2014. Circulating mitochondrial DNA increases with age and is a familiar trait: implications for “inflamm-aging. .” Eur. J. Immunol. 44:51552–62
     [Google Scholar]
  105. 105.  Potter G, Skene D, Arendt J, Cade J, Grant P, Hardie L 2016. Circadian rhythm and sleep disruption: causes, metabolic consequences, and countermeasures. Endocr. Rev. 37:584–608
     [Google Scholar]
  106. 106.  Rampelli S, Candela M, Turroni S, Biagi E, Collino S et al. 2013. Functional metagenomic profiling of intestinal microbiome in extreme ageing. Aging 5:12902–12
     [Google Scholar]
  107. 107.  Rattan SI 2008. Hormesis in aging. Ageing Res. Rev. 7:36–78
     [Google Scholar]
  108. 108.  Ravussin E, Redman LM, Rochon J, Das SK, Fontana L et al. 2015. A 2-year randomized controlled trial of human caloric restriction: feasibility and effects on predictors of health span and longevity. J. Gerontol. A Biol. Sci. Med. Sci. 70:91097–104
     [Google Scholar]
  109. 109.  Richmond RL, Law J, Kay-Lambkin F 2011. Higher blood pressure associated with higher cognition and functionality among centenarians in Australia. Am. J. Hypertens. 24:3299–303
     [Google Scholar]
  110. 110.  Richmond RL, Law J, Kay-Lambkin F 2011. Physical, mental, and cognitive function in a convenience sample of centenarians in Australia. J. Am. Geriatr. Soc. 59:61080–86
     [Google Scholar]
  111. 111.  Ristow M, Schmeisser K 2014. Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS). Dose Response 12:2288–341
     [Google Scholar]
  112. 112.  Rose G, Santoro A, Salvioli S 2016. Mitochondria and mitochondria-induced signalling molecules as longevity determinants. Mech. Ageing Dev. 165:115–28
     [Google Scholar]
  113. 113.  Round JL, Mazmanian SK 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9:5313–23
     [Google Scholar]
  114. 114.  Samuelsson SM, Alfredson BB, Hagberg B, Samuelsson G, Nordbeck B et al. 1997. The Swedish Centenarian Study: a multidisciplinary study of five consecutive cohorts at the age of 100. Int. J. Aging Hum. Dev. 45:3223–53
     [Google Scholar]
  115. 115.  Santoro A, Ostan R, Candela M, Biagi E, Brigidi P et al. 2018. Gut microbiota changes in the extreme decades of human life: a focus on centenarians. Cell. Mol. Life Sci. 75:1129–48
     [Google Scholar]
  116. 116.  Schibler U, Gotic I, Saini C, Gos P, Curie T et al. 2015. Clock-talk: interactions between central and peripheral circadian oscillators in mammals. Cold Spring Harb. Symp. Quant. Biol. 80:223–32
     [Google Scholar]
  117. 117.  Sgarbi G, Matarrese P, Pinti M, Lanzarini C, Ascione B et al. 2014. Mitochondria hyperfusion and elevated autophagic activity are key mechanisms for cellular bioenergetic preservation in centenarians. Aging 4:296–310
     [Google Scholar]
  118. 118.  Singh R, Lakhanpal DKS 2012. Late-onset intermittent fasting dietary restriction as a potential intervention to retard age-associated brain function impairments in male rats. Age 34:917–33
     [Google Scholar]
  119. 119.  Somogyi S 1959. Cento anni di bilanci familiari in Italia (1857–1956) [One hundred years of family budgets in Italy (1857–1956)] Milan: Feltrinelli
     [Google Scholar]
  120. 120.  Spadafora F, Curti A, Teti R, Belmonte M, Castagna A et al. 1996. Aspects of sleep in centenarians. Arch. Gerontol. Geriatr. 22:1419–22
     [Google Scholar]
  121. 121.  Spazzafumo L, Olivieri F, Abbatecola AM, Castellani G, Monti D et al. 2013. Remodelling of biological parameters during human ageing: evidence for complex regulation in longevity and in type 2 diabetes. Age 35:2419–29
     [Google Scholar]
  122. 122.  Strasser B, Berger K, Fuchs D 2015. Effects of a caloric restriction weight loss diet on tryptophan metabolism and inflammatory biomarkers in overweight adults. Eur. J. Nutr. 54:1101–7
     [Google Scholar]
  123. 123.  Stubbs TM, Bonder MJ, Stark A-K, Krueger F, von Meyenn F et al. 2017. Multi-tissue DNA methylation age predictor in mouse. Genome Biol 18:168
     [Google Scholar]
  124. 124.  Tafaro L, Cicconetti P, Baratta A, Brukner N, Ettorre E et al. 2007. Sleep quality of centenarians: cognitive and survival implications. Arch. Gerontol. Geriatr. 44:1385–89
     [Google Scholar]
  125. 125.  Tauber AI 2003. Timeline: Metchnikoff and the phagocytosis theory. Nat. Rev. Mol. Cell Biol. 4:11897–901
     [Google Scholar]
  126. 126.  Tezze C, Romanello V, Desbats MA, Fadini GP, Albiero M et al. 2017. Age-associated loss of OPA1 in muscle impacts muscle mass, metabolic homeostasis, systemic inflammation, and epithelial senescence. Cell Metab 25:61374–89.e6
     [Google Scholar]
  127. 127.  Thaiss CA, Levy M, Korem T, Dohnalová L, Shapiro H et al. 2016. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell 167:61495–510.e12
     [Google Scholar]
  128. 128.  Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J et al. 2014. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159:3514–29
     [Google Scholar]
  129. 129.  Tognini P, Murakami M, Sassone-Corsi P 2017. Interplay between microbes and the circadian clock. Cold Spring Harb. Perspect. Biol. In press. https://doi.org/10.1101/cshperspect.a028365
    [Crossref]
  130. 130. United Nations. 2017. Life expectancy at birth: both sexes. World Population Prospects 2017 New York: United Nations https://esa.un.org/unpd/wpp/Download/SpecialAggregates/Ecological/
    [Google Scholar]
  131. 131. United Nations. 2017. Population by age groups: both sexes. World Population Prospects 2017 New York: United Nations https://esa.un.org/unpd/wpp/Download/Standard/Population/
    [Google Scholar]
  132. 132.  Vanhooren V, Desmyter L, Liu X-E, Cardelli M, Franceschi C et al. 2007. N-glycomic changes in serum proteins during human aging. Rejuvenation Res 10:4521–31a
     [Google Scholar]
  133. 133.  Vanhooren V, Dewaele S, Libert C, Engelborghs S, De Deyn PP et al. 2010. Serum N-glycan profile shift during human ageing. Exp. Gerontol. 45:10738–43
     [Google Scholar]
  134. 134.  Vaughan K, Kaiser T, Peaden R, Anson R, de Cabo R, Mattison J 2017. Caloric restriction study design limitations in rodent and nonhuman primate studies. J. Gerontol. A Biol. Sci. Med. Sci. 73:1248–53
     [Google Scholar]
  135. 135.  Velthuis-te Wierik EJ, van den Berg H, Schaafsma G, Hendriks HF, Brouwer A 1994. Energy restriction, a useful intervention to retard human ageing? Results of a feasibility study. Eur. J. Clin. Nutr. 48:2138–48
     [Google Scholar]
  136. 136.  Villareal DT, Fontana L, Das SK, Redman L, Smith SR et al. 2016. Effect of two-year caloric restriction on bone metabolism and bone mineral density in non-obese younger adults: a randomized clinical trial. J. Bone Miner. Res. 31:140–51
     [Google Scholar]
  137. 137.  Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K et al. 2006. Bone mineral density response to caloric restriction–induced weight loss or exercise-induced weight loss. Arch. Intern. Med. 166:222502–10
     [Google Scholar]
  138. 138.  Vitale G, Barbieri M, Kamenetskaya M, Paolisso G 2017. GH/IGF-I/insulin system in centenarians. Mech. Ageing Dev. 165:107–14
     [Google Scholar]
  139. 139.  Vitale G, Brugts M, Ogliari G, Castaldi D, Fatti L et al. 2012. Low circulating IGF-I bioactivity is associated with human longevity: findings in centenarians’ offspring. Aging 4:9580–89
     [Google Scholar]
  140. 140.  Walford RL, Harris SB, Gunion MW 1992. The calorically restricted low-fat nutrient-dense diet in Biosphere 2 significantly lowers blood glucose, total leukocyte count, cholesterol, and blood pressure in humans. PNAS 89:2311533–37
     [Google Scholar]
  141. 141.  Walford RL, Mock D, Verdery R, Maccallum T 2002. Calorie restriction in Biosphere 2: alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period. J. Gerontol. A Biol. Sci. Med. Sci. 57:6211–24
     [Google Scholar]
  142. 142.  Wall R, Ross RP, Fitzgerald GF, Stanton C 2010. Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr. Rev. 68:5280–89
     [Google Scholar]
  143. 143.  Wang T, Tsui B, Kreisberg JF, Robertson NA, Gross AM et al. 2017. Epigenetic aging signatures in mice livers are slowed by dwarfism, calorie restriction and rapamycin treatment. Genome Biol 18:157
     [Google Scholar]
  144. 144.  Wehrens SMT, Christou S, Isherwood C, Archer SN, Skene DJ et al. 2017. Meal timing regulates the human circadian system. Curr. Biol. 27:121768–75.e3
     [Google Scholar]
  145. 145.  Weiss E, Racette S, Villareal D, Fontana L, Steger-May K et al. 2006. Improvements in glucose tolerance and insulin action induced by increasing energy expenditure or decreasing energy intake: a randomized controlled trial. Am. J. Clin. Nutr. 84:1033–42
     [Google Scholar]
  146. 146.  Weiss E, Racette S, Villareal D, Fontana L, Steger-May K et al. 2007. Lower extremity muscle size and strength and aerobic capacity decrease with caloric restriction but not with exercise-induced weight loss. J. Appl. Physiol. 102:634–40
     [Google Scholar]
  147. 147.  Whittington RA, Planel E, Terrando N 2017. Impaired resolution of inflammation in Alzheimer's disease: a review. Front. Immunol. 8:1464
     [Google Scholar]
  148. 148.  Willcox BJ, Willcox DC, Todoriki H, Fujiyoshi A, Yano K et al. 2007. Caloric restriction, the traditional Okinawan diet, and healthy aging: the diet of the world's longest-lived people and its potential impact on morbidity and life span. Ann N. Y. Acad. Sci. 1114:434–455
     [Google Scholar]
  149. 149.  Willcox DC, Willcox BJ, Todoriki H, Curb JD, Suzuki M 2006. Caloric restriction and human longevity: What can we learn from the Okinawans?. Biogerontology 7:3173–77
     [Google Scholar]
  150. 150.  Yan L, Gao S HD 2013. Calorie restriction can reverse, as well as prevent, aging cardiomyopathy. Age 35:2177–82
     [Google Scholar]
  151. 151.  Zyczkowska J, Klich-Raczka A, Mossakowska M, Gasowski J, Wieczorowska-Tobis K et al. 2004. Blood pressure in centenarians in Poland. J. Hum. Hypertens. 18:10713–16
     [Google Scholar]
/content/journals/10.1146/annurev-nutr-082117-051637
Loading
Nutrition and Inflammation: Are Centenarians Similar to Individuals on Calorie-Restricted Diets?
Annual Review of Nutrition 38, 329 (2018); https://doi.org/10.1146/annurev-nutr-082117-051637
/content/journals/10.1146/annurev-nutr-082117-051637
/content/journals/10.1146/annurev-nutr-082117-051637
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error