Substituting Lean Beef for Carbohydrate in a Healthy Dietary Pattern Does Not Adversely Affect the Cardiometabolic Risk Factor Profile in Men and Women at Risk for Type 2 Diabetes

Kevin C Maki, Meredith L Wilcox, Mary R Dicklin, Mary Buggia, Orsolya M Palacios, Cathleen E Maki, Melvyn Kramer, Kevin C Maki, Meredith L Wilcox, Mary R Dicklin, Mary Buggia, Orsolya M Palacios, Cathleen E Maki, Melvyn Kramer

Abstract

Background: Observational evidence suggests that red meat intake is associated with type 2 diabetes (T2D) and cardiovascular disease incidence, but few randomized controlled trials have assessed effects of lean, unprocessed red meat intake on insulin sensitivity and other cardiometabolic risk factors.

Objective: This study compared the USDA Healthy US-Style Eating Pattern, low in saturated fat and red meat (<40 g/d red meat; USDA-CON), with a modified version with an additional 150 g/d lean beef as an isocaloric replacement for carbohydrate (USDA-LB) on insulin sensitivity and cardiometabolic risk markers.

Methods: Participants (7 men, 26 women; 44.4 y old) with overweight/obesity [BMI (kg/m2) = 31.3] and prediabetes and/or metabolic syndrome completed this randomized, crossover, controlled-feeding trial consisting of two 28-d treatments (USDA-CON and USDA-LB) separated by a ≥14-day washout. Insulin sensitivity (primary outcome variable), lipoprotein lipids, apolipoproteins (apoA-I and apoB), and high-sensitivity C-reactive protein (hs-CRP) (secondary outcome variables), in plasma or serum, and blood pressures were assessed at baseline and the end of each diet period.

Results: USDA-LB and USDA-CON did not differ significantly in effects on whole-body insulin sensitivity and other indicators of carbohydrate metabolism, lipoprotein lipids, apoA-I and apoB, hs-CRP, and blood pressures. USDA-LB produced a shift toward less cholesterol carried by smaller LDL subfractions compared with USDA-CON [least-squares geometric mean ratios for LDL1+2 cholesterol of 1.20 (P = 0.016) and LDL3+4 cholesterol of 0.89 (P = 0.044)] and increased peak LDL time versus USDA-CON (1.01; P = 0.008).

Conclusions: Substituting lean, unprocessed beef for carbohydrate in a Healthy US-Style Eating Pattern resulted in a shift toward larger, more buoyant LDL subfractions, but otherwise had no significant effects on the cardiometabolic risk factor profile in men and women with prediabetes and/or metabolic syndrome.This trial was registered at clinicaltrials.gov as NCT03202680.

Keywords: USDA; beef; carbohydrate metabolism; diet patterns; insulin sensitivity; lipoproteins; meat; metabolic syndrome; prediabetes.

Copyright © The Author(s) on behalf of the American Society for Nutrition 2020.

Figures

FIGURE 1
FIGURE 1
Flow diagram of subjects assessed for eligibility, excluded, randomized, and analyzed for the study. See Results section for a description of the subjects who terminated the study early. USDA-CON, a USDA Healthy US-Style Eating Pattern, as outlined by the 2015 Dietary Guidelines for Americans (5), containing

FIGURE 2

VAP assessment of change from…

FIGURE 2

VAP assessment of change from baseline of LDL peak time after 28-d intake…

FIGURE 2
VAP assessment of change from baseline of LDL peak time after 28-d intake of either the USDA-CON or the USDA-LB among subjects in the evaluable sample. n = 32. The line at 115.0 s represents the baseline value. Values are medians (interquartile limits). *Difference from USDA-CON from analysis of geometric mean ratios, P = 0.008. Least-squares geometric means (−1 SD, +1 SD) are 115 (113, 117) for USDA-CON and 116 (114, 118) for USDA-LB. USDA-CON, a USDA Healthy US-Style Eating Pattern, as outlined by the 2015 Dietary Guidelines for Americans (5), containing <40 g/d red meat; USDA-LB, a USDA Healthy US-Style Eating Pattern, as outlined by the 2015 Dietary Guidelines for Americans (5), modified to incorporate an additional 150 g/d of fresh/unprocessed lean beef to that of the USDA-CON diet, in place of carbohydrate, primarily refined starches; VAP, vertical auto profile.
FIGURE 2
FIGURE 2
VAP assessment of change from baseline of LDL peak time after 28-d intake of either the USDA-CON or the USDA-LB among subjects in the evaluable sample. n = 32. The line at 115.0 s represents the baseline value. Values are medians (interquartile limits). *Difference from USDA-CON from analysis of geometric mean ratios, P = 0.008. Least-squares geometric means (−1 SD, +1 SD) are 115 (113, 117) for USDA-CON and 116 (114, 118) for USDA-LB. USDA-CON, a USDA Healthy US-Style Eating Pattern, as outlined by the 2015 Dietary Guidelines for Americans (5), containing <40 g/d red meat; USDA-LB, a USDA Healthy US-Style Eating Pattern, as outlined by the 2015 Dietary Guidelines for Americans (5), modified to incorporate an additional 150 g/d of fresh/unprocessed lean beef to that of the USDA-CON diet, in place of carbohydrate, primarily refined starches; VAP, vertical auto profile.

References

    1. Reaven G. Insulin resistance and coronary heart disease in nondiabetic individuals. Arterioscler Thromb Vasc Biol. 2012;32(8):1754–9.
    1. Rader DJ. Effect of insulin resistance, dyslipidemia, and intra-abdominal adiposity on the deveopment of cardiovascular disease and diabetes mellitus. Am J Med. 2007;120(3 Suppl 1):S12–8.
    1. American Diabetes Association. 5. Prevention or delay of type 2 diabetes: standards of medical care in diabetes–2018. Diabetes Care. 2018;41(Suppl 1):S51–4.
    1. Dietary Guidelines Advisory Committee. Scientific report of the 2015 Dietary Guidelines Advisory Committee: advisory report to the Secretary of Health and Human Services and the Secretary of Agriculture. U.S. Department of Agriculture, Agricultural Research Service, Washington (DC): Office of Disease Prevention and He; alth Promotion; 2015; [Internet]. [Accessed 2019 Dec 12]. Available from: .
    1. US Department of Health and Human Services; US Department of Agriculture. 2015–2020 Dietary guidelines for Americans. 8th ed. December 2015; [Internet]. [Accessed 2019 Dec 12]. Available from: .
    1. Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Willett WC, Hu FB. Red meat consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis. Am J Clin Nutr. 2011;94(4):1088–96.
    1. Cross AJ, Leitzmann MF, Gail MH, Hollenbeck AR, Schatzkin A, Sinha R. A prospective study of red and processed meat intake in relation to cancer risk. PLoS Med. 2007;4(12):e325.
    1. Bradbury KE, Tong TYN, Key TJ. Dietary intake of high-protein foods and other major foods in meat-eaters, poultry-eaters, fish-eaters, vegetarians, and vegans in UK Bio. bank. Nutrients. 2017;9(12):1317.
    1. Papier K, Tong TY, Appleby PN, Bradbury KE, Fensom GK, Knuppel A, Perez-Cornago A, Schmidt JA, Travic RC, Key TJ. Comparison of major protein-source foods and other food groups in meat-eaters and non-meat-eaters in the EPIC-Oxford Cohort. Nutrients. 2019;11(4):824.
    1. Vernooij RWM, Zeraatkar D, Han MA, El Dib R, Zworth M, Milio K, Sit D, Lee Y, Gomaa H, Valli C et al. .. Patterns of red meat and processed meat consumption and risk for cardiometabolic and cancer outcomes: a syste. matic review and meta-analysis of cohort studies. Ann Intern Med. 2019[Epub ahead of print2019 Oct 1. doi:10.7326/M19-1583].
    1. Turner KM, Keogh JB, Clifton PM. Red meat, dairy, and insulin sensitivity: a randomized crossover intervention study. Am J Clin Nutr. 2015;101(6):1173–9.
    1. Roussell MA, Hill AM, Gaugler TL, West SG, Heuvel JP, Alaupovic P, Gillies PJ, Kris-Etherton PM. Beef in an Optimal Lean Diet study: effects on lipids, lipoproteins, and apolipoproteins. Am J Clin Nutr. 2012;95(1):9–16.
    1. Guasch-Ferr M, Satija A, Blondin SA, Janiszewski M, Emlen E, O'Connor LE, Campbell WW, Hu FB, Willett WC, Stampfer MJ. Meta-analysis of randomized controlled trials of red meat consumption in comparison with various comparison diets on cardiovascular risk factors. Circulation. 2019;139(15):1828–45.
    1. Kirkpatrick CF, Bolick JP, Kris-Etherton PM, Sikand G, Aspry KE, Soffer DE, Willard KE, Maki KC. Review of current evidence and clinical recommendations on the effects of low-carbohydrate and very-low-carbohydrate (including ketogenic) diets for the management of body weight and other cardiometabolic risk factors: a scientific statement from the National Lipid Association Nutrition and Lifestyle Task Force. J Clin Lipidol. 2019;13(5):689–711.
    1. Appel LJ, Sacks FM, Carey VJ, Obarzanek E, Swain JF, Miller ER3rd, Conlin PR, Erlinger TP, Rosner BA, Laranjo NM et al. .. Effects of protein, monounsaturated fat, and carbohydrate intake on blood pressure and serum lipids: results of the OmniHeart randomized trial. JAMA. 2005;294(19):2455–64.
    1. Gadgil MD, Appel LJ, Yeung E, Anderson CAM, Sacks FM, Miller ER III. The effects of carbohydrate, unsaturated fat, and protein intake on measures of insulin sensitivity: results from the OmniHeart trial. Diabetes Care. 2013;36(5):1132–7.
    1. World Medical Association. Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2000;284(23):3043–5.
    1. American Diabetes Association. 2. Classification and diagnosis of diabetes. Standard of medical care in diabetes–2016. Diabetes Care. 2016;39(Suppl 1):S13–22.
    1. Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WPT, Loria CM, Smith SC Jr et al. .. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(6):1640–5.
    1. Mifflin MD, St Jeor ST, Hill LA, Scott BJ, Daugherty SA, Koh YO. A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr. 1990;51(2):241–7.
    1. Blair SN, Haskell WL, Ho P, Paffenbarger RS Jr, Vranizan KM, Farquhar JW, Wood PD. Assessment of habitual physical activity by a seven-day recall in a community survey and controlled experiments. Am J Epidemiol. 1985;122(5):794–804.
    1. Kulkarni KR, Garber DW, Marcovina SM, Segrest JP. Quantification of cholesterol in all lipoprotein classes by the VAP-II method. J Lipid Res. 1994;35(1):159–68.
    1. Maki KC, Palacios OM, Lindner E, Nieman KM, Bell M, Sorce J. Replacement of refined starches and added sugars with egg protein and unsaturated fats increases insulin sensitivity and lowers triglycerides in overweight or obese adults with elevated triglycerides. J Nutr. 2017;147(7):1267–74.
    1. Trabulsi J, Schoeller DA. Evaluation of dietary assessment instruments against doubly labeled water, a biomarker of habitual energy intake. Am J Physiol Endocrinol Metab. 2001;281(5):E891–9.
    1. Chiu S, Williams PT, Dawson T, Bergman RN, Stefanovski D, Watkins SM, Krauss RM. Diets high in protein or saturated fat do not affect insulin sensitivity or plasma concentrations of lipids and lipoproteins in overweight and obese adults. J Nutr. 2014;144(11):1753–9.
    1. Vincent MJ, Allen B, Palacios OM, Haber LT, Maki KC. Meta-regression analysis of the effects of dietary cholesterol intake on LDL and HDL cholesterol. Am J Clin Nutr. 2019;109(1):7–16.
    1. O'Connor LE, Paddon-Jones D, Wright AJ, Campbell WW. A Mediterranean-style eating pattern with lean, unprocessed red meat has cardiometabolic benefits for adults who are overweight or obese in a randomized, crossover, controlled feeding trial. Am J Clin Nutr. 2018;108(1):33–40.
    1. Krauss RM, Siri PW. Metabolic abnormalities: triglyceride and low-density lipoprotein. Endocrinol Metab Clin North Am. 2004;33(2):405–15.
    1. Bergeron N, Chiu S, Williams PT, King SM, Krauss RM. Effects of red meat, white meat, and nonmeat protein sources on atherogenic lipoprotein measures in the context of low compared with high saturated fat intake: a randomized controlled trial. Am J Clin Nutr. 2019;110(1):24–33.
    1. Davidson MH, Hunninghake D, Maki KC, Kwiterovich PO Jr, Kafonek S. Comparison of the effects of lean red meat vs. lean white meat on serum lipid levels among free-living persons with hypercholesterolemia: a long-term, randomized clinical trial. Arch Intern Med. 1999;159(12):1331–8.
    1. Hunninghake DB, Maki KC, Kwiterovich PO Jr, Davidson MH, Dicklin MR, Kafonek SD. Incorporation of lean red meat into a National Cholesterol Education Program Step I diet: a long-term randomized clinical trial in free-living persons with hypercholesterolemia. J Am Coll Nutr. 2000;19(3):351–60.
    1. Anderson JW, Story L, Sieling B, Chen WJ, Petro MS, Story J. Hypocholesterolemic effects of oat-bran or bean intake for hypercholesterolemic men. Am J Clin Nutr. 1984;40(6):1146–55.
    1. National Academies of Sciences, Engineering, and Medicine; Health and Medicine Division; Food and Nutrition Board; Committee to Review the Dietary Reference Intakes for Sodium and Potassium;. Oria M, Harrison M, Stallings VA, Dietary Reference Intakes for sodium and potassium. Washington (DC): National Academies Press; 2019.

Source: PubMed

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