Effects of Low-Fat and High-Fat Meals, with and without Dietary Fiber, on Postprandial Endothelial Function, Triglyceridemia, and Glycemia in Adolescents

Corrie M Whisner, Siddhartha S Angadi, Nathan Y Weltman, Arthur Weltman, Jessica Rodriguez, James T Patrie, Glenn A Gaesser, Corrie M Whisner, Siddhartha S Angadi, Nathan Y Weltman, Arthur Weltman, Jessica Rodriguez, James T Patrie, Glenn A Gaesser

Abstract

The consumption of fiber-rich foods may negate the deleterious effects of high-fat meals on postprandial triglyceridemia and endothelial function. Despite supportive data in adults, little is known about the effects of high-fat and high-fiber foods on cardiovascular health parameters in pediatric populations. In this crossover trial, male and female adolescents (n = 10; 14.1 + 2.6 years; range 10-17 years) consumed (1) low-fat, low-fiber, (2) low-fat, high-fiber, (3) high-fat, low-fiber, and (4) high-fat, high-fiber breakfast meals in randomized order, each following an overnight fast. Baseline and 4 h post-meal blood was obtained for determination of glucose, insulin and triglyceride concentrations. Endothelial function was assessed via brachial artery flow-mediated dilation (FMD). Postprandial FMD was not significantly changed after any meal. However, regression analyses revealed a significant inverse relationship between the change in 4 h triglyceride concentration and change in 4 h FMD for the high-fat, low-fiber meal (β = -0.087; 95% CI = -0.138 to -0.037; p = 0.001) that was no longer significant in the high-fat, high-fiber meal (β = -0.044; 95% CI = -0.117 to 0.029; p = 0.227). Interpretation of these analyses must be qualified by acknowledging that between-meal comparison revealed that the two regression lines were not statistically different (p = 0.226). Addition of high-fiber cereal to the high-fat meal also reduced 4 h postprandial triglyceride increases by ~50% (p = 0.056). A high-fiber breakfast cereal did not attenuate postprandial glucose and insulin responses after consumption of a low-fat meal. While further work is needed to confirm these results in larger cohorts, our findings indicate the potential importance of cereal fiber in blunting the inverse relationship between postprandial hypertriglyceridemia and FMD after consumption of a high-fat meal in adolescents.

Keywords: cardiovascular disease; flow-mediated dilation; glycemia; insoluble fiber; insulin; pediatric; vascular; youth.

Conflict of interest statement

C.M.W. and G.A.G. serve as members of a scientific advisory board for Ardent Mills, L.L.C. G.A.G. serves as a member of the scientific advisory boards for the Wheat Foods Council and the Grain Foods Foundation.

Figures

Figure 1
Figure 1
Blood glucose concentrations over time in response to the four meals. Dashed lines represent individual subject responses. Solid line represents mean response for all subjects. See text and Table 3 for statistical comparisons.
Figure 2
Figure 2
Glycemic response as area under curve (AUC) over 4 h in response to the four meals. Boxes for each meal represent the interquartile range. Minimum and maximum values are indicated at the tips of each vertical line. The median for each meal is depicted by the horizontal line within each box. See Table 4 for statistical comparisons between meals.
Figure 3
Figure 3
Plasma insulin concentrations over time in response to four meals. Dashed lines represent individual subject responses. Solid line represents mean response for all subjects. See text and Table 5 for statistical comparisons between meals.
Figure 4
Figure 4
Plasma insulin as area under curve (AUC) over 4 h, in response to the four meals. Boxes for each meal represent the interquartile range. Minimum and maximum values are indicated at the tips of each vertical line. The median for each meal is depicted by the horizontal line within each box. See Table 6 for statistical comparisons between meals.
Figure 5
Figure 5
Plasma triglyceride responses to the four meals. Dashed lines represent individual subject responses. Solid line represents mean response for all subjects.
Figure 6
Figure 6
Change in plasma triglycerides over 4 h in response to the four meals. Minimum and maximum values are indicated at the tips of each vertical line. The median for each meal is depicted by the horizontal line within each box. See Table 7 for statistical comparisons.
Figure 7
Figure 7
Endothelial function, as measured by flow-mediated dilation (FMD), following the four meals. Dashed lines represent responses for each individual. Solid line represents the mean response (±SD). FMD was not different across time points for all meals.
Figure 8
Figure 8
Attenuating effects of including a high-fiber cereal with a high-fat, low-fiber breakfast meal on the association between the change in 4 h plasma triglyceride concentration and change in 4 h FMD. For high-fat, low-fiber: β = −0.087 (95% CI = −0.138 to −0.037; p = 0.001). For high-fat, high-fiber: β = −0.044 (95% CI = −0.117 to 0.029; p = 0.227). Direct comparison of the two regression lines indicated that the slopes were not different from one another (p = 0.226).

References

    1. Gokce N., Keaney J.F., Hunter L.M., Watkins M.T., Menzoian J.O., Vita J.A. Risk stratification for postoperative cardiovascular events via noninvasive assessment of endothelial function: A prospective study. Circulation. 2002;105:1567–1572. doi: 10.1161/01.CIR.0000012543.55874.47.
    1. Zilversmit D.B. Atherogenesis: A postprandial phenomenon. Circulation. 1979;60:473–485. doi: 10.1161/01.CIR.60.3.473.
    1. Irawati D., Mamo J.C.L., Slivkoff-Clark K.M., Soares M.J., James A.P. Dietary fat and physiological determinants of plasma chylomicron remnant homoeostasis in normolipidaemic subjects: Insight into atherogenic risk. Br. J. Nutr. 2017;117:403–412. doi: 10.1017/S0007114517000150.
    1. Langsted A., Nordestgaard B.G. Nonfasting versus fasting lipid profile for cardiovascular risk prediction. Pathology. 2019;51:131–141. doi: 10.1016/j.pathol.2018.09.062.
    1. DECODE Study Group Is the current definition for diabetes relevant to mortality risk from all causes and cardiovascular and noncardiovascular diseases? Diabetes Care. 2003;26:688–696. doi: 10.2337/diacare.26.3.688.
    1. Levitan E.B., Song Y., Ford E.S., Liu S. Is Nondiabetic Hyperglycemia a Risk Factor for Cardiovascular Disease? Arch. Intern. Med. 2004;164:2147. doi: 10.1001/archinte.164.19.2147.
    1. O’Keefe J.H., Gheewala N.M., O’Keefe J.O. Dietary Strategies for Improving Post-Prandial Glucose, Lipids, Inflammation, and Cardiovascular Health. J. Am. Coll. Cardiol. 2008;51:249–255. doi: 10.1016/j.jacc.2007.10.016.
    1. Stary H.C. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis. 1989;9:19–32.
    1. Berenson G.S., Wattigney W.A., Tracy R.E., Newman W.P., Srinivasan S.R., Webber L.S., Dalferes E.R., Strong J.P. Atherosclerosis of the aorta and coronary arteries and cardiovascular risk factors in persons aged 6 to 30 years and studied at necropsy (The Bogalusa Heart Study) Am. J. Cardiol. 1992;70:851–858. doi: 10.1016/0002-9149(92)90726-F.
    1. Thom N.J., Early A.R., Hunt B.E., Harris R.A., Herring M.P. Eating and arterial endothelial function: A meta-analysis of the acute effects of meal consumption on flow-mediated dilation. Obes. Rev. 2016;17:1080–1090. doi: 10.1111/obr.12454.
    1. Harris R.A., Nishiyama S.K., Wray D.W., Richardson R.S. Ultrasound Assessment of Flow-Mediated Dilation. Hypertension. 2010;55:1075–1085. doi: 10.1161/HYPERTENSIONAHA.110.150821.
    1. Inaba Y., Chen J.A., Bergmann S.R. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: A meta-analysis. Int. J. Cardiovasc. Imaging. 2010;26:631–640. doi: 10.1007/s10554-010-9616-1.
    1. Bae J.H., Bassenge E., Kim K.B., Kim Y.N., Kim K.S., Lee H.J., Moon K.C., Lee M.S., Park K.Y., Schwemmer M. Postprandial hypertriglyceridemia impairs endothelial function by enhanced oxidant stress. Atherosclerosis. 2001;155:517–523. doi: 10.1016/S0021-9150(00)00601-8.
    1. Vogel R.A., Corretti M.C., Plotnick G.D. Effect of a single high-fat meal on endothelial function in healthy subjects. Am. J. Cardiol. 1997;79:350–354. doi: 10.1016/S0002-9149(96)00760-6.
    1. Gaenzer H., Sturm W., Neumayr G., Kirchmair R., Ebenbichler C., Ritsch A., Föger B., Weiss G., Patsch J.R. Pronounced postprandial lipemia impairs endothelium-dependent dilation of the brachial artery in men. Cardiovasc. Res. 2001;52:509–516. doi: 10.1016/S0008-6363(01)00427-8.
    1. Williams M.J., Sutherland W.H., McCormick M.P., de Jong S.A., Walker R.J., Wilkins G.T. Impaired endothelial function following a meal rich in used cooking fat. J. Am. Coll. Cardiol. 1999;33:1050–1055. doi: 10.1016/S0735-1097(98)00681-0.
    1. Marchesi S., Lupattelli G., Schillaci G., Pirro M., Siepi D., Roscini A.R., Pasqualini L., Mannarino E. Impaired flow-mediated vasoactivity during post-prandial phase in young healthy men. Atherosclerosis. 2000;153:397–402. doi: 10.1016/S0021-9150(00)00415-9.
    1. Zhao S.P., Liu L., Gao M., Zhou Q.C., Li Y.L., Xia B. Impairment of endothelial function after a high-fat meal in patients with coronary artery disease. Coron. Artery Dis. 2001;12:561–565. doi: 10.1097/00019501-200111000-00006.
    1. Steer P., Sarabi D.M., Karlstrom B., Basu S., Berne C., Vessby B., Lind L. The effect of a mixed meal on endothelium-dependent vasodilation is dependent on fat content in healthy humans. Clin. Sci. 2003;105:81–87. doi: 10.1042/CS20020327.
    1. Loader J., Montero D., Lorenzen C., Watts R., Méziat C., Reboul C., Stewart S., Walther G. Acute Hyperglycemia Impairs Vascular Function in Healthy and Cardiometabolic Diseased Subjects: Systematic Review and Meta-Analysis. Arterioscler. Thromb. Vasc. Biol. 2015;35:2060–2072. doi: 10.1161/ATVBAHA.115.305530.
    1. Sanders T.A., Lewis F.J., Goff L.M., Chowienczyk P.J. RISCK Study Group SFAs do not impair endothelial function and arterial stiffness. Am. J. Clin. Nutr. 2013;98:677–683.
    1. Ayer J.G., Harmer J.A., Steinbeck K., Celermajer D.S. Postprandial Vascular Reactivity in Obese and Normal Weight Young Adults. Obesity. 2010;18:945–951. doi: 10.1038/oby.2009.331.
    1. Sedgwick M.J., Morris J.G., Nevill M.E., Barrett L.A. Effect of repeated sprints on postprandial endothelial function and triacylglycerol concentrations in adolescent boys. J. Sports Sci. 2015;33:806–816. doi: 10.1080/02640414.2014.964749.
    1. Sedgwick M.J., Morris J.G., Nevill M.E., Tolfrey K., Nevill A., Barrett L.A. Effect of exercise on postprandial endothelial function in adolescent boys. Br. J. Nutr. 2013;110:301–309. doi: 10.1017/S0007114512004977.
    1. Lane-Cordova A.D., Witmer J.R., Dubishar K., DuBose L.E., Chenard C.A., Siefers K.J., Myers J.E., Points L.J., Pierce G.L. High trans but not saturated fat beverage causes an acute reduction in postprandial vascular endothelial function but not arterial stiffness in humans. Vasc. Med. 2016;21:429–436. doi: 10.1177/1358863X16656063.
    1. Brock D.W., Davis C.K., Irving B.A., Rodriguez J., Barrett E.J., Weltman A., Taylor A.G., Gaesser G.A. A high-carbohydrate, high-fiber meal improves endothelial function in adults with the metabolic syndrome. Diabetes Care. 2006;29:2313–2315. doi: 10.2337/dc06-0917.
    1. Kondo K., Morino K., Nishio Y., Ishikado A., Arima H., Nakao K., Nakagawa F., Nikami F., Sekine O., Nemoto K., et al. Fiber-rich diet with brown rice improves endothelial function in type 2 diabetes mellitus: A randomized controlled trial. PLoS ONE. 2017;12:e0179869. doi: 10.1371/journal.pone.0179869.
    1. Wolk A., Manson J.E., Stampfer M.J., Colditz G.A., Hu F.B., Speizer F.E., Hennekens C.H., Willett W.C. Long-term intake of dietary fiber and decreased risk of coronary heart disease among women. JAMA. 1999;281:1998–2004. doi: 10.1001/jama.281.21.1998.
    1. Jensen M.K., Koh-Banerjee P., Hu F.B., Franz M., Sampson L., Grønbæk M., Rimm E.B. Intakes of whole grains, bran, and germ and the risk of coronary heart disease in men. Am. J. Clin. Nutr. 2004;80:1492–1499. doi: 10.1093/ajcn/80.6.1492.
    1. Hajishafiee M., Saneei P., Benisi-Kohansal S., Esmaillzadeh A. Cereal fibre intake and risk of mortality from all causes, CVD, cancer and inflammatory diseases: A systematic review and meta-analysis of prospective cohort studies. Br. J. Nutr. 2016;116:343–352. doi: 10.1017/S0007114516001938.
    1. Mateo Anson N., Aura A.M., Selinheimo E., Mattila I., Poutanen K., van den Berg R., Havenaar R., Bast A., Haenen G.R.M.M. Bioprocessing of wheat bran in whole wheat bread increases the bioavailability of phenolic acids in men and exerts antiinflammatory effects ex vivo. J. Nutr. 2011;141:137–143. doi: 10.3945/jn.110.127720.
    1. Neacsu M., Varga A., Socaciu C., Van Camp J. Analysis of antioxidant phytochemicals from Brussels sprout. Commun. Agric. Appl. Biol. Sci. 2004;69:257–260.
    1. Kern S.M., Bennett R.N., Mellon F.A., Kroon P.A., Garcia-Conesa M.T. Absorption of hydroxycinnamates in humans after high-bran cereal consumption. J. Agric. Food Chem. 2003;51:6050–6055. doi: 10.1021/jf0302299.
    1. Pérez-Jiménez J., Saura-Calixto F. Literature data may underestimate the actual antioxidant capacity of cereals. J. Agric. Food Chem. 2005;53:5036–5040. doi: 10.1021/jf050049u.
    1. Cara L., Dubois C., Borel P., Armand M., Senft M., Portugal H., Pauli A.M., Bernard P.M., Lairon D. Effects of oat bran, rice bran, wheat fiber, and wheat germ on postprandial lipemia in healthy adults. Am. J. Clin. Nutr. 1992;55:81–88. doi: 10.1093/ajcn/55.1.81.
    1. Dubois C., Cara L., Borel P., Armand M., Senft M., Portugal H., Bernard P.M., Lafont H., Lairon D. Cereal dietary fibers affect post-prandial lipoproteins in healthy human subjects. Carbohydr. Polym. 1993;21:189–194. doi: 10.1016/0144-8617(93)90017-X.
    1. Lairon D. Macronutrient intake and modulation on chylomicron production and clearance. Atheroscler. Suppl. 2008;9:45–48. doi: 10.1016/j.atherosclerosissup.2008.05.006.
    1. Bond B., Gates P.E., Jackman S.R., Corless L.M., Williams C.A., Barker A.R. Exercise intensity and the protection from postprandial vascular dysfunction in adolescents. Am. J. Physiol. Heart Circ. Physiol. 2015;308:H1443–H1450. doi: 10.1152/ajpheart.00074.2015.
    1. Metzig A.M., Schwarzenberg S.J., Fox C.K., Deering M.M., Nathan B.M., Kelly A.S. Postprandial endothelial function, inflammation, and oxidative stress in obese children and adolescents. Obesity. 2011;19:1279–1283. doi: 10.1038/oby.2010.318.
    1. Dengel D.R., Kelly A.S., Steinberger J., Sinaiko A.R. Effect of oral glucose loading on endothelial function in normal-weight and overweight children. Clin. Sci. 2007;112:493–498. doi: 10.1042/CS20060305.
    1. Herrington D.M., Fan L., Drum M., Riley W.A., Pusser B.E., Crouse J.R., Burke G.L., McBurnie M.A., Morgan T.M., Espeland M.A. Brachial flow-mediated vasodilator responses in population-based research: Methods, reproducibility and effects of age, gender and baseline diameter. J. Cardiovasc. Risk. 2001;8:319–328. doi: 10.1177/174182670100800512.
    1. Sorensen K.E., Celermajer D.S., Spiegelhalter D.J., Georgakopoulos D., Robinson J., Thomas O., Deanfield J.E. Non-invasive measurement of human endothelium dependent arterial responses: Accuracy and reproducibility. Br. Heart J. 1995;74:247–253. doi: 10.1136/hrt.74.3.247.
    1. Corretti M.C., Anderson T.J., Benjamin E.J., Celermajer D., Charbonneau F., Creager M.A., Deanfield J., Drexler H., Gerhard-Herman M., Herrington D., et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: A report of the International Brachial Artery Reactivity Task Force. J. Am. Coll. Cardiol. 2002;39:257–265. doi: 10.1016/S0735-1097(01)01746-6.
    1. Hallmark R., Patrie J.T., Liu Z., Gaesser G.A., Barrett E.J., Weltman A. The effect of exercise intensity on endothelial function in physically inactive lean and obese adults. PLoS ONE. 2014;9:e85450. doi: 10.1371/journal.pone.0085450.
    1. Mah E., Bruno R.S. Postprandial hyperglycemia on vascular endothelial function: Mechanisms and consequences. Nutr. Res. 2012;32:727–740. doi: 10.1016/j.nutres.2012.08.002.
    1. Martínez-Tomé M., Murcia M.A., Frega N., Ruggieri S., Jiménez A.M., Roses F., Parras P. Evaluation of Antioxidant Capacity of Cereal Brans. J. Agric. Food Chem. 2004;52:4690–4699. doi: 10.1021/jf049621s.
    1. Westphal S., Taneva E., Kästner S., Martens-Lobenhoffer J., Bode-Böger S., Kropf S., Dierkes J., Luley C. Endothelial dysfunction induced by postprandial lipemia is neutralized by addition of proteins to the fatty meal. Atherosclerosis. 2006;185:313–319. doi: 10.1016/j.atherosclerosis.2005.06.004.
    1. Hopping B.N., Erber E., Grandinetti A., Verheus M., Kolonel L.N., Maskarinec G. Dietary Fiber, Magnesium, and Glycemic Load Alter Risk of Type 2 Diabetes in a Multiethnic Cohort in Hawaii. J. Nutr. 2010;140:68–74. doi: 10.3945/jn.109.112441.
    1. Schulze M.B., Schulz M., Heidemann C., Schienkiewitz A., Hoffmann K., Boeing H. Fiber and Magnesium Intake and Incidence of Type 2 Diabetes. Arch. Intern. Med. 2007;167:956. doi: 10.1001/archinte.167.9.956.
    1. Bajorek S.A., Morello C.M. Effects of Dietary Fiber and Low Glycemic Index Diet on Glucose Control in Subjects with Type 2 Diabetes Mellitus. Ann. Pharmacother. 2010;44:1786–1792. doi: 10.1345/aph.1P347.
    1. Weickert M.O., Möhlig M., Schöfl C., Arafat A.M., Otto B., Viehoff H., Koebnick C., Kohl A., Spranger J., Pfeiffer A.F.H. Cereal fiber improves whole-body insulin sensitivity in overweight and obese women. Diabetes Care. 2006;29:775–780. doi: 10.2337/diacare.29.04.06.dc05-2374.
    1. Kim H., Stote K.S., Behall K.M., Spears K., Vinyard B., Conway J.M. Glucose and insulin responses to whole grain breakfasts varying in soluble fiber, beta-glucan: A dose response study in obese women with increased risk for insulin resistance. Eur. J. Nutr. 2009;48:170–175. doi: 10.1007/s00394-009-0778-3.
    1. Kranz S., Brauchla M., Slavin J.L., Miller K.B. What do we know about dietary fiber intake in children and health? The effects of fiber intake on constipation, obesity, and diabetes in children. Adv. Nutr. 2012;3:47–53. doi: 10.3945/an.111.001362.
    1. Moreno L.A., Tresaco B., Bueno G., Fleta J., Rodríguez G., Garagorri J.M., Bueno M. Psyllium fibre and the metabolic control of obese children and adolescents. J. Physiol. Biochem. 2003;59:235–242. doi: 10.1007/BF03179920.
    1. Cheng G., Karaolis-Danckert N., Libuda L., Bolzenius K., Remer T., Buyken A.E. Relation of dietary glycemic index, glycemic load, and fiber and whole-grain intakes during puberty to the concurrent development of percent body fat and body mass index. Am. J. Epidemiol. 2009;169:667–677. doi: 10.1093/aje/kwn375.
    1. Thijssen D.H.J., Black M.A., Pyke K.E., Padilla J., Atkinson G., Harris R.A., Parker B., Widlansky M.E., Tschakovsky M.E., Green D.J. Assessment of flow-mediated dilation in humans: A methodological and physiological guideline. Am. J. Physiol. Circ. Physiol. 2011;300:H2–H12. doi: 10.1152/ajpheart.00471.2010.
    1. Thijssen D.H.J., Bullens L.M., van Bemmel M.M., Dawson E.A., Hopkins N., Tinken T.M., Black M.A., Hopman M.T.E., Cable N.T., Green D.J. Does arterial shear explain the magnitude of flow-mediated dilation?: A comparison between young and older humans. Am. J. Physiol. Heart Circ. Physiol. 2009;296:H57–H64. doi: 10.1152/ajpheart.00980.2008.
    1. Walters J.F., Hampton S.M., Deanfield J.E., Donald A.E., Skene D.J., Ferns G.A.A. Circadian variation in endothelial function is attenuated in postmenopausal women. Maturitas. 2006;54:294–303. doi: 10.1016/j.maturitas.2005.12.005.
    1. Etsuda H., Takase B., Uehata A., Kusano H., Hamabe A., Kuhara R., Akima T., Matsushima Y., Arakawa K., Satomura K., et al. Morning attenuation of endothelium-dependent, flow-mediated dilation in healthy young men: Possible connection to morning peak of cardiac events? Clin. Cardiol. 1999;22:417–421. doi: 10.1002/clc.4960220610.

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