Effect of modest caloric restriction on oxidative stress in women, a randomized trial

Maciej S Buchowski, Nobuko Hongu, Sari Acra, Li Wang, Joshua Warolin, L Jackson Roberts 2nd, Maciej S Buchowski, Nobuko Hongu, Sari Acra, Li Wang, Joshua Warolin, L Jackson Roberts 2nd

Abstract

Objectives: It is not established to what extent caloric intake must be reduced to lower oxidative stress in humans. The aim of this study was to determine the effect of short-term, moderate caloric restriction on markers of oxidative stress and inflammation in overweight and obese premenopausal women.

Materials/methods: Randomized trial comparison of 25% caloric restriction (CR) or control diet in 40 overweight or obese women (body mass index 32±5.8 kg/m(2)) observed for 28 days and followed for the next 90 days. Weight, anthropometry, validated markers of oxidative stress (F(2)-isoprostane) and inflammation (C-reactive protein), adipokines, hormones, lipids, interleukins, and blood pressure were assessed at baseline, during the intervention, and at follow-up.

Results: Baseline median F(2)-isoprostane concentration (57.0, IQR = 40.5-79.5) in the CR group was 1.75-fold above average range for normal weight women (32.5 pg/ml). After starting of the caloric restriction diet, F(2)-isoprostane levels fell rapidly in the CR group, reaching statistical difference from the control group by day 5 (median 33.5, IQR = 26.0-48.0, P<0.001) and remained suppressed while continuing on the caloric restriction diet. Three months after resuming a habitual diet, concentrations of F(2)-isoprostane returned to baseline elevated levels in ∼80% of the women.

Conclusions: Oxidative stress can be rapidly reduced and sustained through a modest reduction in caloric intake suggesting potential health benefits in overweight and obese women.

Trial registration: Clinicaltrials.gov NCT00808275.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. CONSORT flow diagram.
Figure 1. CONSORT flow diagram.
Figure 2. Median plasma concentrations of F…
Figure 2. Median plasma concentrations of F2-isoprostane (prostaglandin F2-like compound) in overweight and obese women at baseline (Day 0), during dietary intervention (Days 1–29), and after 90-day follow-up (Days 42 and 119) in the CR (caloric restricted) diet (75% of energy requirement) group (n = 32) and in the control group (n = 8) without diet restrictions (100% of energy requirement).
Vertical bars represent 95% bootstrap confidence intervals.

References

    1. Vincent HK, Innes KE, Vincent KR (2007) Oxidative stress and potential interventions to reduce oxidative stress in overweight and obesity. Diabetes, Obesity and Metabolism 9: 813–839.
    1. Lumeng CN, Saltiel AR (2011) Inflammatory links between obesity and metabolic disease. The Journal of Clinical Investigation 121: 2111–2117.
    1. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860–867.
    1. Basu S (2008) F2-Isoprostanes in Human Health and Diseases: From Molecular Mechanisms to Clinical Implications. Antioxidants & Redox Signaling 10: 1405–1434.
    1. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, et al. (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. The Journal of Clinical Investigation 114: 1752–1761.
    1. Tinahones FJ, Murri-Pierri M, Garrido-Sanchez L, Garcia-Almeida JM, Garcia-Serrano S, et al. (2008) Oxidative Stress in Severely Obese Persons Is Greater in Those With Insulin Resistance. Obesity 17: 240–246.
    1. Ouchi N, Parker JL, Lugus JJ, Walsh K (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11: 85–97.
    1. Keaney JF Jr, Larson MG, Vasan RS, Wilson PWF, Lipinska I, et al. (2003) Obesity and Systemic Oxidative Stress: Clinical Correlates of Oxidative Stress in The Framingham Study. Arterioscler Thromb Vasc Biol 23: 434–439.
    1. Sawyer DB (2011) Oxidative Stress in Heart Failure: What Are We Missing? The American Journal of the Medical Sciences 342: 120–124 doi: 110.1097/MAJ.1090b1013e3182249fcd.
    1. Barocas DA, Motley S, Cookson MS, Chang SS, Penson DF, et al. (2011) Oxidative Stress Measured by Urine F2-Isoprostane Level is Associated With Prostate Cancer. The Journal of Urology 185: 2102–2107.
    1. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, et al. (2007) Inflammation in prostate carcinogenesis. Nat Rev Cancer 7: 256–269.
    1. Couillard C, Ruel G, Archer WR, Pomerleau S, Bergeron J, et al. (2005) Circulating levels of oxidative stress markers and endothelial adhesion molecules in men with abdominal obesity. Journal of Clinical Endocrinology & Metabolism 90: 6454–6459.
    1. Helmersson J, Vessby B, Larsson A, Basu S (2004) Association of type 2 diabetes with cyclooxygenase-mediated inflammation and oxidative stress in an elderly population. Circulation 109: 1729–1734.
    1. Tchernof A, Nolan A, Sites CK, Ades PA, Poehlman ET (2002) Weight Loss Reduces C-Reactive Protein Levels in Obese Postmenopausal Women. Circulation 105: 564–569.
    1. Klimcakova E, Kovacikova M, Stich V, Langin D (2010) Adipokines and dietary interventions in human obesity. Obesity Reviews 11: 446–456.
    1. Rolland C, Hession M (2011) Broom (2011) Effect of weight loss on adipokine levels in obese patients. Diabetes Metab Syndr Obes 4: 315–323.
    1. Meydani M, Das S, Band M, Epstein S, Roberts S (2011) The effect of caloric restriction and glycemic load on measures of oxidative stress and antioxidants in humans: results from the CALERIE Trial of Human Caloric Restriction. J Nutr Health Aging 15: 456–460.
    1. National Health and Nutrition Examination Survey (NHANES): Anthropometry Procedures Manual. In: Prevention CfDCa, editor. Atlanta, GA: CDC. 3: 20–23 and 23: 30–21.
    1. Weir J (1949) New methods for calculating metabolic rate with special reference to protein metabolism. The Journal of Physiology 109: 1–9.
    1. Miller PE, Mitchell DC, Harala PL, Pettit JM, Smiciklas-Wright H, et al. (2011) Development and evaluation of a method for calculating the Healthy Eating Index-2005 using the Nutrition Data System for Research. Public Health Nutrition 14: 306–313.
    1. Harnack L, Stevens M, Van H, Schakel S, Dwyer J, et al.. (2008) A computer-based approach for assessing dietary supplement use in conjunction with dietary recalls. J Food Compost Anal 21 (Supplement): S78–S82.
    1. Bingham S, Cummings J (1985) Urine nitrogen as an independent validatory measure of dietary intake: a study of nitrogen balance in individuals consuming their normal diet. The American Journal of Clinical Nutrition 42: 1276–1289.
    1. McCullough ML, Swain JF, Malarick C, Moore TJ (1991) Feasibility of outpatient electrolyte balance studies. Journal of the American College of Nutrition 10: 140–148.
    1. Feskanich D, Sielaff BH, Chong K, Buzzard IM (1989) Computerized collection and analysis of dietary intake information. Comput Methods Programs Biomed 30: 47–57.
    1. Johnson RK, Driscoll P, Goran MI (1996) Comparison of multiple-pass 24-hour recall estimates of energy intake with total energy expenditure determined by the doubly labeled water method in young children. J Am Diet Assoc 96: 1140–1144.
    1. Morrow JD, Roberts LJ 2nd (1999) Mass spectrometric quantification of F2-isoprostanes in biological fluids and tissues as measure of oxidant stress. Methods in enzymology 300: 3–12.
    1. Kadiiska MB, Gladen BC, Baird DD, Germolec D, Graham LB, et al. (2005) Biomarkers of Oxidative Stress Study II: Are oxidation products of lipids, proteins, and DNA markers of CCl4 poisoning? Free Radical Biology and Medicine 38: 698–710.
    1. Milne GL, Musiek ES, Morrow JD (2005) F2-Isoprostanes as markers of oxidative stress in vivo: An overview. Biomarkers 10: 10–23.
    1. Morrow JD, Hill KE, Burk RF, Nammour TM, Badr KF, et al. (1990) A Series of Prostaglandin F2-Like Compounds are Produced in vivo in Humans by a Non-Cyclooxygenase, Free Radical-Catalyzed Mechanism. PNAS 87: 9383–9387.
    1. Milne GL, Yin H, Hardy KD, Davies SS, Roberts LJ (2011) Isoprostane Generation and Function. Chemical Reviews 111: 5973–5996.
    1. Chevion M, Berenshtein E, Stadtman ER (2000) Human studies related to protein oxidation: protein carbonyl content as a marker of damage. Free Radic Res 33 Suppl: S99–108
    1. Dizdaroglu M, Nackerdien Z, Chao BC, Gajewski E, Rao G (1991) Chemical nature of in vivo DNA base damage in hydrogen peroxide-treated mammalian cells. Arch Biochem Biophys 285: 388–390.
    1. Koizumi A, Weindruch R, Walford RL (1987) Influences of dietary restriction and age on liver enzyme activities and lipid peroxidation in mice. J Nutr 117: 361–367.
    1. Rao G, Xia E, Nadakavukaren MJ, Richardson A (1990) Effect of dietary restriction on the age-dependent changes in the expression of antioxidant enzymes in rat liver. J Nutr 120: 602–609.
    1. Gomi F, Matsuo M (1998) Effects of aging and food restriction on the antioxidant enzyme activity of rat livers. J Gerontol A Biol Sci Med Sci 53: B161–167.
    1. Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273: 59–63.
    1. Redman LM, Ravussin E (2011) Caloric restriction in humans: impact on physiological, psychological, and behavioral outcomes. Antioxid Redox Signal 14: 275–287.
    1. 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: a randomized controlled trial. JAMA 295: 1539–1548.
    1. Yagi K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15: 212–216.
    1. Davi G, Guagnano MT, Ciabattoni G, Basili S, Falco A, et al. (2002) Platelet Activation in Obese Women: Role of Inflammation and Oxidant Stress. JAMA 288: 2008–2014.
    1. Tsai IJ, Croft KD, Mori TA, Falck JR, Beilin LJ, et al. (2009) 20-HETE and F2-isoprostanes in the metabolic syndrome: the effect of weight reduction. Free Radical Biology and Medicine 46: 263–270.
    1. Roberts LJ, Morrow JD (2000) Measurement of F2-isoprostanes as an index of oxidative stress in vivo. Free Radical Biology and Medicine 28: 505.
    1. Ridker PM, Rifai N, Clearfield M, Downs JR, Weis SE, et al. (2001) Measurement of C-Reactive Protein for the Targeting of Statin Therapy in the Primary Prevention of Acute Coronary Events. N Engl J Med 344: 1959–1965.
    1. Richelle M, Turini ME, Guidoux R, Tavazzi I, Métairon S, et al. (1999) Urinary isoprostane excretion is not confounded by the lipid content of the diet. FEBS Letters 459: 259–262.
    1. Gopaul N, Halliwell B, Anggård E (2000) Measurement of plasma F2-isoprostanes as an index of lipid peroxidation does not appear to be confounded by diet. Free Radic Res 33: 115–127.
    1. Codoñer-Franch P, Valls-Bellés V, Arilla-Codoñer A, Alonso-Iglesias E Oxidant mechanisms in childhood obesity: the link between inflammation and oxidative stress. Translational Research.
    1. Tsai WC LY, Lin CC, Chao TH, Chen JH (2004) Effects of oxidative stress on endothelial function after a high-fat meal. Clin Science 106: 315–319.
    1. Bae J-H, Bassenge E, Kim K-B, Kim Y-N, Kim K-S, et al. (2001) Postprandial hypertriglyceridemia impairs endothelial function by enhanced oxidant stress. Atherosclerosis 155: 517.
    1. Ziccardi P, Nappo F, Giugliano G, Esposito K, Marfella R, et al. (2002) Reduction of Inflammatory Cytokine Concentrations and Improvement of Endothelial Functions in Obese Women After Weight Loss Over One Year. Circulation 105: 804–809.
    1. Wray DW, Nishiyama SK, Donato AJ, Carlier P, Bailey DM, et al.. (2011) The Paradox of Oxidative Stress and Exercise With Advancing Age. Exercise and Sport Sciences Reviews 39: 68–76 10.1097/JES.1090b1013e31820d37657.
    1. Higdon JV, Frei B (2003) Obesity and Oxidative Stress: A Direct Link to CVD? Arterioscler Thromb Vasc Biol 23: 365–367.
    1. Heilbronn L, Civitarese AE, Bogacka I, Smith S, Hulver M, et al. (2005) Glucose tolerance and skeletal muscle gene expression in response to alternate day fasting. Obes Res 13: 574–581.
    1. Hall KD, Jordan PN (2008) Modeling weight-loss maintenance to help prevent body weight regain. The American Journal of Clinical Nutrition 88: 1495–1503.
    1. Strychar I, Lavoie M-È, Messier L, Karelis AD, Doucet É, et al. (2009) Anthropometric, Metabolic, Psychosocial, and Dietary Characteristics of Overweight/Obese Postmenopausal Women with a History of Weight Cycling: A MONET (Montreal Ottawa New Emerging Team) Study. Journal of the American Dietetic Association 109: 718–724.
    1. Pieper C, Redman L, Racette S, Roberts S, Bhapkar M, et al. (2011) Development of adherence metrics for caloric restriction interventions. Clin Trials 8: 155–164.
    1. Field AE, Manson JE, Taylor CB, Willett WC, Colditz GA (2004) Association of weight change, weight control practices, and weight cycling among women in the Nurses' Health Study II. International journal of obesity and related metabolic disorders : journal of the International Association for the Study of Obesity 28: 1134–1142.
    1. Lahti-Koski M, Mannisto S, Pietinen P, Vartiainen E (2005) Prevalence of weight cycling and its relation to health indicators in Finland. Obes Res 13: 333–341.
    1. Osborn R, Forys K, Psota T, Sbrocco T (2011) Yo-yo dieting in African American women: weight cycling and health. Ethn Dis 21: 274–280.
    1. Cereda E, Malavazos AE, Caccialanza R, Rondanelli M, Fatati G, et al. (2011) Weight cycling is associated with body weight excess and abdominal fat accumulation: A cross-sectional study. Clinical Nutrition 30: 718–723.
    1. Dulloo AG, Jacquet J, Montani J-P (2012) How dieting makes some fatter: from a perspective of human body composition autoregulation. Proceedings of the Nutrition Society 71: 379–389.
    1. Hooper LE, Foster-Schubert KE, Weigle DS, Sorensen B, Ulrich CM, et al. (2010) Frequent intentional weight loss is associated with higher ghrelin and lower glucose and androgen levels in postmenopausal women. Nutrition Research 30: 163–170.
    1. Graci S, Izzo G, Savino S, Cattani L, Lezzi G, et al. (2003) Weight cycling and cardiovascular risk factors in obesity. International journal of obesity and related metabolic disorders : journal of the International Association for the Study of Obesity 28: 65–71.
    1. Stevens VL, Jacobs EJ, Sun J, Patel AV, McCullough ML, et al. (2012) Weight Cycling and Mortality in a Large Prospective US Study. American Journal of Epidemiology 175: 785–792.
    1. Hooper LE, Foster-Schubert KE, Weigle DS, Sorensen B, Ulrich CM, et al. (2010) Frequent intentional weight loss is associated with higher ghrelin and lower glucose and androgen levels in postmenopausal women. Nutr Res 30: 163–170.
    1. Institute of Medicine (2000) Panel on Dietary Antioxidants and Related Compounds: Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids. Washington, D.C.: National Academy Press. 506 p. p.
    1. Heilbronn L, Ravussin E (2003) Caloric restriction and aging: review of the literature and implications for studies in humans. The American Journal of Clinical Nutrition 78: 361–369.
    1. Davalos A, Gomez-Cordoves C, Bartolome B (2004) Extending applicability of the oxygen radical absorbance capacity (ORAC-fluorescein) assay. J Agric Food Chem 52: 48–54.
    1. Apak R, Guclu K, Ozyurek M, Bektasoglu B, Bener M (2010) Cupric ion reducing antioxidant capacity assay for antioxidants in human serum and for hydroxyl radical scavengers. Methods Mol Biol 594: 215–239.
    1. Nemzer BV, Rodriguez LC, Hammond L, Disilvestro R, Hunter JM, et al. (2011) Acute reduction of serum 8-iso-PGF2-alpha and advanced oxidation protein products in vivo by a polyphenol-rich beverage; a pilot clinical study with phytochemical and in vitro antioxidant characterization. Nutr J 10: 67.
    1. Wray DW, Nishiyama SK, Harris RA, Zhao J, McDaniel J, et al. (2012) Acute reversal of endothelial dysfunction in the elderly after antioxidant consumption. Hypertension 59: 818–824.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다