Effects of weight loss during a very low carbohydrate diet on specific adipose tissue depots and insulin sensitivity in older adults with obesity: a randomized clinical trial

Amy M Goss, Barbara Gower, Taraneh Soleymani, Mariah Stewart, May Pendergrass, Mark Lockhart, Olivia Krantz, Shima Dowla, Nikki Bush, Valene Garr Barry, Kevin R Fontaine, Amy M Goss, Barbara Gower, Taraneh Soleymani, Mariah Stewart, May Pendergrass, Mark Lockhart, Olivia Krantz, Shima Dowla, Nikki Bush, Valene Garr Barry, Kevin R Fontaine

Abstract

Background: Insulin resistance and accumulation of visceral adipose tissue (VAT) and intermuscular adipose tissue (IMAT) place aging adults with obesity at high risk of cardio-metabolic disease. A very low carbohydrate diet (VLCD) may be a means of promoting fat loss from the visceral cavity and skeletal muscle, without compromising lean mass, and improve insulin sensitivity in aging adults with obesity.

Objective: To determine if a VLCD promotes a greater loss of fat (total, visceral and intermuscular), preserves lean mass, and improves insulin sensitivity compared to a standard CHO-based/low-fat diet (LFD) in older adults with obesity.

Design: Thirty-four men and women aged 60-75 years with obesity (body mass index [BMI] 30-40 kg/m2) were randomized to a diet prescription of either a VLCD (< 10:25:> 65% energy from CHO:protein:fat) or LFD diet (55:25:20) for 8 weeks. Body composition by dual-energy X-ray absorptiometry (DXA), fat distribution by magnetic resonance imaging (MRI), insulin sensitivity by euglycemic hyperinsulinemic clamp, and lipids by a fasting blood draw were assessed at baseline and after the intervention.

Results: Participants lost an average of 9.7 and 2.0% in total fat following the VLCD and LFD, respectively (p < 0.01). The VLCD group experienced ~ 3-fold greater loss in VAT compared to the LFD group (- 22.8% vs - 1.0%, p < 0.001) and a greater decrease in thigh-IMAT (- 24.4% vs - 1.0%, p < 0.01). The VLCD group also had significantly greater thigh skeletal muscle (SM) at 8 weeks following adjustment for change in total fat mass. Finally, the VLCD had greater increases in insulin sensitivity and HDL-C and decreases in fasting insulin and triglycerides compared to the LFD group.

Conclusions: Weight loss resulting from consumption of a diet lower in CHO and higher in fat may be beneficial for older adults with obesity by depleting adipose tissue depots most strongly implicated in poor metabolic and functional outcomes and by improving insulin sensitivity and the lipid profile.

Trial registration: NCT02760641. Registered 03 May 2016 - Retrospectively registered.

Conflict of interest statement

Competing interestsK.F. serves on the scientific advisory board to Virta Health Corp and has stock options. He also serves on the scientific advisory board to Atkins Nutritionals. The other authors have nothing to disclose.

© The Author(s) 2020.

Figures

Fig. 1
Fig. 1
Individual changes in body composition in response to the low fat diet (LFD) and the very low carbohydrate diet (VLCD)
Fig. 2
Fig. 2
Mean change in adipose tissue depots following consumption of the very low carbohydrate and low fat diets. Participants in the VLCD group experienced 3-fold greater loss of VAT and IMAT when compared to the LFD group. (** indicates P < 0.01 for effect of diet)
Fig. 3
Fig. 3
Mean change in resting energy expenditure and respiratory quotient following consumption of the very low carbohydrate and low fat diets. (*** indicates P < 0.001)

References

    1. Decaria JE, Sharp C, Petrella RJ. Scoping review report: obesity in older adults. Int J Obes (2005) 2012;36:1141–1150. doi: 10.1038/ijo.2012.29.
    1. Lakdawalla DN, Goldman DP, Shang B. The health and cost consequences of obesity among the future elderly. Health Aff (Project Hope) 2005;24(Suppl 2):W5r30–W5r41. doi: 10.1377/hlthaff.W5.R30.
    1. Addison O, Drummond MJ, LaStayo PC, et al. Intramuscular fat and inflammation differ in older adults: the impact of frailty and inactivity. J Nutr Health Aging. 2014;18:532–538. doi: 10.1007/s12603-014-0019-1.
    1. Goss AM, Gower BA. Insulin sensitivity is associated with thigh adipose tissue distribution in healthy postmenopausal women. Metabolism. 2012;61:1817–1823. doi: 10.1016/j.metabol.2012.05.016.
    1. Kim JE, Dunville K, Li J, et al. Intermuscular adipose tissue content and intramyocellular lipid fatty acid saturation are associated with glucose homeostasis in middle-aged and older adults. Endocrinol Metab (Seoul, Korea) 2017;32:257–264. doi: 10.3803/EnM.2017.32.2.257.
    1. Murphy RA, Reinders I, Register TC, et al. Associations of BMI and adipose tissue area and density with incident mobility limitation and poor performance in older adults. Am J Clin Nutr. 2014;99:1059–1065. doi: 10.3945/ajcn.113.080796.
    1. Kalinkovich A, Livshits G. Sarcopenic obesity or obese sarcopenia: a cross talk between age-associated adipose tissue and skeletal muscle inflammation as a main mechanism of the pathogenesis. Ageing Res Rev. 2017;35:200–221. doi: 10.1016/j.arr.2016.09.008.
    1. Locher JL, Goldsby TU, Goss AM, Kilgore ML, Gower B, Ard JD. Calorie restriction in overweight older adults: do benefits exceed potential risks? Exp Gerontol. 2016;86:4–13. doi: 10.1016/j.exger.2016.03.009.
    1. Bojsen-Moller KN, Lundsgaard AM, Madsbad S, Kiens B, Holst JJ. Hepatic insulin clearance in regulation of systemic insulin concentrations-role of carbohydrate and energy availability. Diabetes. 2018;67:2129–2136. doi: 10.2337/db18-0539.
    1. Goss AM, Chandler-Laney PC, Ovalle F, et al. Effects of a eucaloric reduced-carbohydrate diet on body composition and fat distribution in women with PCOS. Metabolism. 2014;63:1257–1264. doi: 10.1016/j.metabol.2014.07.007.
    1. Goss AM, Goree LL, Ellis AC, et al. Effects of diet macronutrient composition on body composition and fat distribution during weight maintenance and weight loss. Obesity (Silver Spring) 2013;21:1139–1142. doi: 10.1002/oby.20191.
    1. Gower BA, Goss AM. A lower-carbohydrate, higher-fat diet reduces abdominal and intermuscular fat and increases insulin sensitivity in adults at risk of type 2 diabetes. J Nutr. 2015;145:177S–183S. doi: 10.3945/jn.114.195065.
    1. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Phys. 1979;237:E214–E223.
    1. Katz A, Nambi SS, Mather K, et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab. 2000;85:2402–2410. doi: 10.1210/jcem.85.7.6661.
    1. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502. doi: 10.1093/clinchem/18.6.499.
    1. St-Onge MP, Wang Z, Horlick M, Wang J, Heymsfield SB. Dual-energy X-ray absorptiometry lean soft tissue hydration: independent contributions of intra- and extracellular water. Am J Physiol Endocrinol Metab. 2004;287:E842–E847. doi: 10.1152/ajpendo.00361.2003.
    1. Santanasto AJ, Glynn NW, Newman MA, et al. Impact of weight loss on physical function with changes in strength, muscle mass, and muscle fat infiltration in overweight to moderately obese older adults: a randomized clinical trial. J Obes. 2011;2011:516576. 10.1155/2011/516576.
    1. Messier SP, Mihalko SL, Legault C, et al. Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial. Jama. 2013;310:1263–1273. doi: 10.1001/jama.2013.277669.
    1. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev. 2010;11:11–18. doi: 10.1111/j.1467-789X.2009.00623.x.
    1. Beavers KM, Beavers DP, Houston DK, et al. Associations between body composition and gait-speed decline: results from the health, aging, and body composition study. Am J Clin Nutr. 2013;97:552–560. doi: 10.3945/ajcn.112.047860.
    1. Miljkovic-Gacic I, Gordon CL, Goodpaster BH, et al. Adipose tissue infiltration in skeletal muscle: age patterns and association with diabetes among men of African ancestry. Am J Clin Nutr. 2008;87:1590–1595. doi: 10.1093/ajcn/87.6.1590.
    1. Bergia RE, 3rd, Kim JE, Campbell WW. Differential relationship between intermuscular adipose depots with indices of cardiometabolic health. Int J Endocrinol. 2018;2018:2751250. doi: 10.1155/2018/2751250.
    1. Kreitzman SN, Coxon AY, Szaz KF. Glycogen storage: illusions of easy weight loss, excessive weight regain, and distortions in estimates of body composition. Am J Clin Nutr. 1992;56:292S–293S. doi: 10.1093/ajcn/56.1.292S.
    1. Olsson KE, Saltin B. Variation in total body water with muscle glycogen changes in man. Acta Physiol Scand. 1970;80:11–18. doi: 10.1111/j.1748-1716.1970.tb04764.x.
    1. Manninen AH. Very-low-carbohydrate diets and preservation of muscle mass. Nutr Metab (Lond) 2006;3:9. doi: 10.1186/1743-7075-3-9.
    1. Boden G, Sargrad K, Homko C, Mozzoli M, Stein TP. Effect of a low-carbohydrate diet on appetite, blood glucose levels, and insulin resistance in obese patients with type 2 diabetes. Ann Intern Med. 2005;142:403–411. doi: 10.7326/0003-4819-142-6-200503150-00006.
    1. Gu Y, Zhao A, Huang F, et al. Very low carbohydrate diet significantly alters the serum metabolic profiles in obese subjects. J Proteome Res. 2013;12:5801–5811. doi: 10.1021/pr4008199.
    1. Gu Y, Yu H, Li Y, et al. Beneficial effects of an 8-week, very low carbohydrate diet intervention on obese subjects. Evid Based Complement Alternat Med. 2013;2013:760804.
    1. Sharman MJ, Gomez AL, Kraemer WJ, Volek JS. Very low-carbohydrate and low-fat diets affect fasting lipids and postprandial lipemia differently in overweight men. J Nutr. 2004;134:880–885. doi: 10.1093/jn/134.4.880.
    1. Partsalaki I, Karvela A, Spiliotis BE. Metabolic impact of a ketogenic diet compared to a hypocaloric diet in obese children and adolescents. J Pediatr Endocrinol Metab. 2012;25:697–704. doi: 10.1515/jpem-2012-0131.
    1. Samaha FF, Iqbal N, Seshadri P, et al. A low-carbohydrate as compared with a low-fat diet in severe obesity. N Engl J Med. 2003;348:2074–2081. doi: 10.1056/NEJMoa022637.
    1. Sachs S, Zarini S, Kahn DE, et al. Intermuscular adipose tissue directly modulates skeletal muscle insulin sensitivity in humans. Am J Physiol Endocrinol Metab. 2019;316(5):E866–79. 10.1152/ajpendo.00243.2018.
    1. Gardner CD, Trepanowski JF, Del Gobbo LC, et al. Effect of low-fat vs low-carbohydrate diet on 12-month weight loss in overweight adults and the association with genotype pattern or insulin secretion: the DIETFITS randomized clinical trial. Jama. 2018;319:667–679. doi: 10.1001/jama.2018.0245.
    1. Yancy WS, Jr, Westman EC, McDuffie JR, et al. A randomized trial of a low-carbohydrate diet vs orlistat plus a low-fat diet for weight loss. Arch Intern Med. 2010;170:136–145. doi: 10.1001/archinternmed.2009.492.
    1. Volek JS, Fernandez ML, Feinman RD, Phinney SD. Dietary carbohydrate restriction induces a unique metabolic state positively affecting atherogenic dyslipidemia, fatty acid partitioning, and metabolic syndrome. Prog Lipid Res. 2008;47:307–318. doi: 10.1016/j.plipres.2008.02.003.
    1. Volek JS, Sharman MJ, Forsythe CE. Modification of lipoproteins by very low-carbohydrate diets. J Nutr. 2005;135:1339–1342. doi: 10.1093/jn/135.6.1339.
    1. Johnstone AM, Horgan GW, Murison SD, Bremner DM, Lobley GE. Effects of a high-protein ketogenic diet on hunger, appetite, and weight loss in obese men feeding ad libitum. Am J Clin Nutr. 2008;87:44–55. doi: 10.1093/ajcn/87.1.44.
    1. Yancy WS, Jr, Olsen MK, Guyton JR, Bakst RP, Westman EC. A low-carbohydrate, ketogenic diet versus a low-fat diet to treat obesity and hyperlipidemia: a randomized, controlled trial. Ann Intern Med. 2004;140:769–777. doi: 10.7326/0003-4819-140-10-200405180-00006.

Source: PubMed

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