Long-term moderate calorie restriction inhibits inflammation without impairing cell-mediated immunity: A randomized controlled trial in non-obese humans

Aging

Volumn 8, Issue 7, 2016, Pages 1416-1431

  Meydani, Simin N ^a   Das, Sai K ^a   Pieper, Carl F ^b   Lewis, Michael R ^c   Klein, Sam ^d   Dixit, Vishwa D ^e   Gupta, Alok K ^f   Villareal, Dennis T ^g   Bhapkar, Manjushri ^b   Huang, Megan ^b   Fuss, Paul J ^a   Roberts, Susan B ^a   Holloszy, John O ^d   Fontana, Luigi ^d,h,i  

^a TUFTS UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF VERMONT   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^g MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^h UNIVERSITY OF BRESCIA   (Italy)

ⁱ CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

Calorie restriction; Cell mediated immunity; Familial longevity; Human; Inflammation; Vaccine response

Indexed keywords

BIOLOGICAL MARKER; C REACTIVE PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LEPTIN; TUMOR NECROSIS FACTOR;

ADULT; BLOOD; BODY COMPOSITION; CALORIC INTAKE; CALORIC RESTRICTION; CLINICAL TRIAL; CONTROLLED STUDY; DIET; DIET THERAPY; FEMALE; HUMAN; INFLAMMATION; LYMPHOCYTE COUNT; MALE; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME;

ADULT; BIOMARKERS; BODY COMPOSITION; C-REACTIVE PROTEIN; CALORIC RESTRICTION; DIET; ENERGY INTAKE; FEMALE; HUMANS; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; LEPTIN; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85008669410     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100994     Document Type: Article

References (51)

1. Fontana L, Partridge L and Longo VD. Extending healthy life span-from yeast to humans. Science. 2010; 328:321-26.
2. Franceschi C and Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol A Biol Sci Med Sci. 2014; 69 Suppl 1:4-9.
3. Meyer TE, Kovacs SJ, Ehsani AA, Klein S, Holloszy JO and Fontana L. Long-term caloric restriction ameliorates the decline in diastolic function in humans. J Am Coll Cardiol. 2006; 47:398-402.
4. Howcroft TK, Campisi J, Louis GB, Smith MT, Wise B, Wyss-Coray T, Augustine AD, McElhaney JE, Kohanski R and Sierra F. The role of inflammation in age-related disease. Aging (Albany NY). 2013; 5:84-93. doi: 10.18632/aging.100531.
5. Koenig W. High-sensitivity C-reactive protein and atherosclerotic disease: from improved risk prediction to riskguided therapy. Int J Cardiol. 2013; 168:5126-34.
6. Hotamisligil GS, Shargill NS and Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesitylinked insulin resistance. Science. 1993; 259:87-91.
7. Lavie CJ, Milani RV, Verma A and O'Keefe JH. C-reactive protein and cardiovascular diseases-is it ready for primetime? Am J Med Sci. 2009; 338:486-92.
8. Taube A, Schlich R, Sell H, Eckardt K and Eckel J. Inflammation and metabolic dysfunction: links to cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2012; 302:2148-65.
9. Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R and Simsolo RB. The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J Clin Invest. 1995; 95:2111-19.
10. Zahorska-Markiewicz B, Janowska J, Olszanecka-Glinianowicz M and Zurakowski A. Serum concentrations of TNF-alpha and soluble TNF-alpha receptors in obesity. Int J Obes Relat Metab Disord. 2000; 24:1392-95.
11. Formoso G, Taraborrelli M, Guagnano MT, D'Adamo M, Di Pietro N, Tartaro A and Consoli A. Magnetic resonance imaging determined visceral fat reduction associates with enhanced IL-10 plasma levels in calorie restricted obese subjects. PLoS One. 2012; 7:52774.
12. Roecker EB, Kemnitz JW, Ershler WB and Weindruch R. Reduced immune responses in rhesus monkeys subjected to dietary restriction. J Gerontol A Biol Sci Med Sci. 1996; 51:276-79.
13. Gardner EM. Caloric restriction decreases survival of aged mice in response to primary influenza infection. J Gerontol A Biol Sci Med Sci. 2005; 60:688-94.
14. Ritz BW, Aktan I, Nogusa S and Gardner EM. Energy restriction impairs natural killer cell function and increases the severity of influenza infection in young adult male C57BL/6 mice. J Nutr. 2008; 138:2269-75.
15. Messaoudi I, Warner J, Fischer M, Park B, Hill B, Mattison J, Lane MA, Roth GS, Ingram DK, Picker LJ, Douek DC, Mori M and Nikolich-Zugich J. Delay of T cell senescence by caloric restriction in aged long-lived nonhuman primates. Proc Natl Acad Sci U S A. 2006; 103:19448-53.
16. Yang H, Youm YH and Dixit VD. Inhibition of thymic adipogenesis by caloric restriction is coupled with reduction in age-related thymic involution. J Immunol. 2009; 183:3040-52.
17. Schaible UE and Kaufmann SH. Malnutrition and infection: complex mechanisms and global impacts. PLoS Med. 2007; 4:115.
18. Stewart TM, Bhapkar M, Das S, Galan K, Martin CK, McAdams L, Pieper C, Redman L, Roberts S, Stein RI, Rochon J and Williamson DA. Comprehensive Assessment of Long-term Effects of Reducing Intake of Energy Phase 2 (CALERIE Phase 2) screening and recruitment: methods and results. Contemp Clin Trials. 2013; 34:10-20.
19. Ravussin E, Redman LM, Rochon J, Das SK, Fontana L, Kraus WE, Romashkan S, Williamson DA, Meydani SN, Villareal DT, Smith SR, Stein RI, Scott TM, et al. 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. 2015; 70:1097-1104.
20. Lam QL and Lu L. Role of leptin in immunity. Cell Mol Immunol. 2007; 4:1-13.
21. Ershler WB, Sun WH, Binkley N, Gravenstein S, Volk MJ, Kamoske G, Klopp RG, Roecker EB, Daynes RA and Weindruch R. Interleukin-6 and aging: blood levels and mononuclear cell production increase with advancing age and in vitro production is modifiable by dietary restriction. Lymphokine Cytokine Res. 1993; 12:225-30.
22. Fontana L. Neuroendocrine factors in the regulation of inflammation: excessive adiposity and calorie restriction. Exp Gerontol. 2009; 44:41-45.
23. Rienstra M, Sun JX, Magnani JW, Sinner MF, Lubitz SA, Sullivan LM, Ellinor PT and Benjamin EJ. White blood cell count and risk of incident atrial fibrillation (from the Framingham Heart Study). Am J Cardiol. 2012; 109:533-37.
24. Lorenzo C, Hanley AJ and Haffner SM. Differential white cell count and incident type 2 diabetes: the Insulin Resistance Atherosclerosis Study. Diabetologia. 2014; 57:83-92.
25. Shankar A, Klein BE and Klein R. Relationship between white blood cell count and incident hypertension. Am J Hypertens. 2004; 17:233-39.
26. Margolis KL, Manson JE, Greenland P, Rodabough RJ, Bray PF, Safford M, Grimm RH, Jr., Howard BV, Assaf AR and Prentice R. Leukocyte count as a predictor of cardiovascular events and mortality in postmenopausal women: the Women's Health Initiative Observational Study. Arch Intern Med. 2005; 165:500-508.
27. Toriola AT, Cheng TY, Neuhouser ML, Wener MH, Zheng Y, Brown E, Miller JW, Song X, Beresford SA, Gunter MJ, Caudill MA and Ulrich CM. Biomarkers of inflammation are associated with colorectal cancer risk in women but are not suitable as early detection markers. Int J Cancer. 2013; 132:2648-58.
28. Shankar A, Wang JJ, Rochtchina E, Yu MC, Kefford R and Mitchell P. Association between circulating white blood cell count and cancer mortality: a population-based cohort study. Arch Intern Med. 2006; 166:188-94.
29. Chae JS, Paik JK, Kang R, Kim M, Choi Y, Lee SH and Lee JH. Mild weight loss reduces inflammatory cytokines, leukocyte count, and oxidative stress in overweight and moderately obese participants treated for 3 years with dietary modification. Nutr Res. 2013; 33:195-203.
30. Loffreda S, Yang SQ, Lin HZ, Karp CL, Brengman ML, Wang DJ, Klein AS, Bulkley GB, Bao C, Noble PW, Lane MD and Diehl AM. Leptin regulates proinflammatory immune responses. FASEB J. 1998; 12:57-65.
31. Fontana L, Eagon JC, Trujillo ME, Scherer PE and Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007; 56:1010-13.
32. Bordone L and Guarente L. Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol. 2005; 6:298-305.
33. Guarente L. Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell. 2008; 132:171-76.
34. Barzilai N, Huffman DM, Muzumdar RH and Bartke A. The critical role of metabolic pathways in aging. Diabetes. 2012; 61:1315-22.
35. Hotamisligil GS and Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol. 2008; 8:923-34.
36. Ahmed T, Das SK, Golden JK, Saltzman E, Roberts SB and Meydani SN. Calorie restriction enhances T-cell-mediated immune response in adult overweight men and women. J Gerontol A Biol Sci Med Sci. 2009; 64:1107-13.
37. Clinthorne JF, Adams DJ, Fenton JI, Ritz BW and Gardner EM. Short-term re-feeding of previously energy-restricted C57BL/6 male mice restores body weight and body fat and attenuates the decline in natural killer cell function after primary influenza infection. J Nutr. 2010; 140:1495-1501.
38. Sun D, Muthukumar AR, Lawrence RA and Fernandes G. Effects of calorie restriction on polymicrobial peritonitis induced by cecum ligation and puncture in young C57BL/6 mice. Clin Diagn Lab Immunol. 2001; 8:1003-11.
39. Goldberg EL, Romero-Aleshire MJ, Renkema KR, Ventevogel MS, Chew WM, Uhrlaub JL, Smithey MJ, Limesand KH, Sempowski GD, Brooks HL and Nikolich-Zugich J. Lifespanextending caloric restriction or mTOR inhibition impair adaptive immunity of old mice by distinct mechanisms. Aging Cell. 2015; 14:130-38.
40. Kristan DM. Chronic calorie restriction increases susceptibility of laboratory mice (Mus musculus) to a primary intestinal parasite infection. Aging Cell. 2007; 6:817-25.
41. Rochon J, Bales CW, Ravussin E, Redman LM, Holloszy JO, Racette SB, Roberts SB, Das SK, Romashkan S, Galan KM, Hadley EC and Kraus WE. Design and conduct of the CALERIE study: comprehensive assessment of the long-term effects of reducing intake of energy. J Gerontol A Biol Sci Med Sci. 2011; 66:97-108.
42. Pieper C, Redman L, Racette S, Roberts S, Bhapkar M, Rochon J, Martin C, Kraus W, Das S, Williamson D and Ravussin E. Development of adherence metrics for caloric restriction interventions. Clin Trials. 2011; 8:155-64.
43. Rickman AD, Williamson DA, Martin CK, Gilhooly CH, Stein RI, Bales CW, Roberts S and Das SK. The CALERIE Study: design and methods of an innovative 25% caloric restriction intervention. Contemp Clin Trials. 2011; 32:874-81.
44. Diggle PJ, Heagerty P, Liang K-Y and Zeger SL. Analysis of Longitudinal Data. 2002. New York: Oxford University Press.
45. Fitzmaurice G, Laird NM and Ware JH. Applied Longitudinal Analysis. 2002. New York City: Wiley.
46. Jennrich RI and Schluchter MD. Unbalanced repeatedmeasures models with structured covariance matrices. Biometrics. 1986; 42:805-20.
47. Wright S. Adjusted P-values for simultaneous inference. Biometrics. 1992; 48:1005-13.
48. Lawless J. Statistical Models and Methods for Lifetime Data. 2003. New York: John Wiley & Sons.
49. Liang KY. Longitudinal data analysis using generalized linear models. Biometrika 1986; 78:13-22.
50. McCullagh P and Nelder JA. Generalized Linear Models. London New York: Chapman and Hall. 1989.
51. Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004; 159:702-06.