Oxidative stress and endothelial function: effects of physical exercise on results of postprandial lipemia

Krüger, Renata Lopes; Farinha, Juliano Boufleur; Teixeira, Bruno Costa; Reischak-Oliveira, Alvaro

doi:10.1590/1677-5449.01715

Renata Lopes Krüger ^**Correspondence Renata Lopes Krüger University of Calgary – UofC KNB 422, 2500, University Drive NW Calgary, Alberta, Canada T2N 1N4 Tel.: +1.403.220.3497 E-mail: renatalkruger@gmail.com

University of Calgary – UofC, Faculty of Kinesiology, Calgary, AL, Canadá.

Juliano Boufleur Farinha

Universidade Federal do Rio Grande do Sul – UFRGS, Escola de Educação Física, Laboratório de Pesquisa do Exercício, Porto Alegre, RS, Brazil.

Bruno Costa Teixeira

Universidade Federal do Rio Grande do Sul – UFRGS, Escola de Educação Física, Laboratório de Pesquisa do Exercício, Porto Alegre, RS, Brazil.

Universidade Integrada do Alto Uruguai e das Missões – URI, São Luiz Gonzaga, RS, Brazil.

Alvaro Reischak-Oliveira

Universidade Federal do Rio Grande do Sul – UFRGS, Escola de Educação Física, Laboratório de Pesquisa do Exercício, Porto Alegre, RS, Brazil.

Conflicts of interest: No conflicts of interest declared concerning the publication of this article.

*Correspondence Renata Lopes Krüger University of Calgary – UofC KNB 422, 2500, University Drive NW Calgary, Alberta, Canada T2N 1N4 Tel.: +1.403.220.3497 E-mail: renatalkruger@gmail.com

Author information RLK - MSc in Human Movement Sciences at Universidade Federal do Rio Grande do Sul (UFRGS); PhD candidate in Kinesiology at Universidade de Calgary (UofC). JBF - MSc in Physical Education from Universidade Federal de Santa Maria (UFSM); PhD candidate in Human Movement Sciences at Universidade Federal do Rio Grande do Sul (UFRGS). BCT - MSc in Human Movement Sciences; PhD candidate in Human Movement Sciences at Universidade Federal do Rio Grande do Sul (UFRGS). ARO - PhD in Physiology from Universidade Federal do Rio Grande do Sul (UFRGS).

Author contributions Conception and design: RLK, JBF, BCT, ARO Analysis and interpretation: RLK, JBF Data collection: RLK, JBF Writing the article: RLK, JBF, BCT Critical revision of the article: RLK, JBF, BCT, ARO Final approval of the article*: ARO Statistical analysis: N/A. Overall responsibility: ARO *All authors have read and approved of the final version of the article submitted to J Vasc Bras.

Figures (4)
Tables (1)

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Figure 1
Organogram illustrating manual electronic search.

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Figure 2
Normal nitric oxide production (NO) inside the vascular endothelial cell and in the postprandial lipemic state. The NO is produced from L-arginine in a reaction catalyzed by the endothelium-derived nitric oxide synthase isoform (eNOS) and is dependent on other factors, such as tetrahydrobiopterin (BH₄). Vascular NO production can be stimulated by shear forces caused by blood flow, insulin and acetylcholine (ACh). Nitric oxide maintains the blood vessel in a constant state of vasodilation. When there is an increase in postprandial lipemia, accumulated superoxide radicals (O₂^-) produced by lipid oxidation (β-oxidation) interact with NO, forming peroxynitrite (ONOO^-), and affecting vascular tone.

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Figure 3
Process of atherosclerotic plaque formation. Low density lipoprotein undergoes gradual oxidation until formation of minimally modified LDL (MM-LDL), which can contain products of lipid oxidation without protein modification. The LDL will only become oxidized LDL (ox-LDL) when the apoB protein has been modified and it loses the affinity for its receptor, when it is recognized by macrophage scavenger receptors. In inflammatory response, ox-LDL leads to activation of monocytes, which are transformed into macrophages in the subendothelial space. As the macrophages begin to phagocytose the lipids, foam cells are formed, derived from the macrophages, which contain lipids that are primarily in the form of free cholesterol.

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Figure 4
Possible benefits of exercise on postprandial oxidative stress. After eating a high fat meal, there is a rise in the levels of triglyceride-rich lipoproteins (TRLs), which stimulate production of cytokines (IL-6 and IL-8) by leukocytes and increase Krebs cycle and electron transport chain activity. In turn, polyunsaturated fatty acids supplied by the meal can react with reactive oxygen species (ROS) and reactive nitrogen species produced previously, such as superoxide (O₂^•-), hydrogen peroxide (H₂O₂), hydroxyl radical (OH^•) and peroxynitrite (ONOO^-). These ROS oxidize LDL (to ox-LDL) which, in turn, is phagocytosed by macrophages, triggering a long-term atherosclerotic process. Physical exercise can reduce the levels of TRLs and cytokines and can also prevent lipoperoxidation damage.

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Table 1
List of studies analyzing markers of oxidative stress and endothelial function selected for review.

Study	Population	Exercise protocol*	Postprandial lipemia	Oxidative stress	Endothelial function
Gill et al.¹⁵15 Gill JM, Al-Mamari A, Ferrell WR, et al. Effects of prior moderate exercise on postprandial metabolism and vascular function in lean and centrally obese men. J Am Coll Cardiol. 2004;44(12):2375-82. http://dx.doi.org/10.1016/j.jacc.2004.09.035. PMid:15607401. http://dx.doi.org/10.1016/j.jacc.2004.09...	Middle-aged, lean men (10); Middle-aged, obese men (10)	Subacute on treadmill at 50%; VO_2max - 90min	↓TG exercise vs. control ↓TG AUC exercise Obese subjects: ↑TG AUC ↑INS AUC ↑NEFA AUC	NA	microvascular function = in both groups; ACh Response 25% ↑ in exercise group
Mc Clean et al.²³23 Mc Clean CM, Mc Laughlin J, Burke G, et al. The effect of acute aerobic exercise on pulse wave velocity and oxidative stress following postprandial hypertriglyceridemia in healthy men. Eur J Appl Physiol. 2007;100(2):225-34. http://dx.doi.org/10.1007/s00421-007-0422-y. PMid:17323071. http://dx.doi.org/10.1007/s00421-007-042...	Trained men (10)	Acute on treadmill at 60% of HR_max - 1h	↑TG 2 h, 3 h and 4 h ↓TG 3 h and 4 h vs. 2 h in exercise group ↓HDL 3 h and 4 h in controls ↑HDL 3 h in exercise group = LDL	↑NOx - 4h ↓SOD 2 h and 3 h ↓SOD 3 h control vs. exercise ↑LOOH 2 h, 3 h and 4 h ↓LOOH 3 h exercise vs. control	↑PWV 1 h, 2 h, 3 h and 4 h ↓PWV 3 h and 4 h vs. 2 h in exercise group
Clegg et al.²⁴24 Clegg M, McClean C, Davison WG, et al. Exercise and postprandial lipaemia: effects on peripheral vascular function, oxidative stress and gastrointestinal transit. Lipids Health Dis. 2007;6(1):30. http://dx.doi.org/10.1186/1476-511X-6-30. PMid:17973988. http://dx.doi.org/10.1186/1476-511X-6-30...	Trained young men (8)	Acute on cycle ergometer at 60% of HR_max - 1h	= TG = HDL = LDL	↑LOOH 2 h and 4 h vs. pre	↑PWV 2 h and 4 h in controls ↓PWV 2 h and 4 h exercise vs. 2 h for controls
Silvestre et al.²⁵25 Silvestre R, Kraemer WJ, Quann EE, et al. Effects of exercise at different times on postprandial lipemia and endothelial function. Med Sci Sports Med. 2008;40(2):264-74. PMid:18202576.	Trained young men (12)	Subacute resistance and aerobic exercise for 75 min up to 450 Kcal Acute resistance and aerobic exercise for 75 min up to 450 Kcal	↓TG 2 h, 3 h and 4 h exercise vs. control ↓TG AUC exercise vs. control ↑NEFA AUC exercise vs. control ↓INS AUC subacute exercise vs. control	NA	↑Dilation 6 h in subacute (2.2%) and acute (2.8%) exercise groups ↑ BAD progressive in exercise vs. controls
Bloomer et al.²⁶26 Bloomer RJ, Cole B, Fisher-Wellman KH. Racial differences in postprandial oxidative stress with and without acute exercise. Int J Sport Nutr Exerc Metab. 2009;19(5):457-72. PMid:19910649.	African-American women (10) White women (10)	Acute on cycle ergometer at 65% HR_max - 45 min	↑TG African-American vs. white	↑MDA African-American vs. white ↑H₂O₂ African-American vs. white = XO	NA
Tyldum et al.²²22 Tyldum GA, Schjerve IE, Tjonna AE, et al. Endothelial dysfunction induced by post-prandial lipemia: complete protection afforded by high-intensity aerobic interval exercise. J Am Coll Cardiol. 2009;53(2):200-6. http://dx.doi.org/10.1016/j.jacc.2008.09.033. PMid:19130989. http://dx.doi.org/10.1016/j.jacc.2008.09...	Middle-aged men (8)	Subacute interval exercise on treadmill at 85%-90% HR_max Subacute on treadmill at 60%-70% HR_max - 47min until same energy expenditure	= TG = HDL	↓TAS 2 h and 4 h in controls ↑TAS 30 min, 2 h and 4 h in interval exercise group ↑TAS 30 min, 2 h and 4 h interval vs. control and walking ↑TAS 30 min, 2 h and 4 h walking vs. control	↑ BAD 30 min, 2 h and 4 h interval exercise group vs. controls and walking ↓FMD 2 h and 4 h in controls ↑FMD 30 min, 2 h and 4 h in interval group ↑FMD 30 min, 2 h and 4 h walking vs. control
Melton²⁷27 Melton CE, Tucker PS, Fisher-Wellman KH, Schilling BK, Bloomer RJ. Acute exercise does not attenuate postprandial oxidative stress in prediabetic women. Phys Sportsmed. 2009;37(1):27-36. http://dx.doi.org/10.3810/PSM.2009.04.1680. PMid:20048485. http://dx.doi.org/10.3810/PSM.2009.04.16...	Prediabetic women (16)	Acute at 65% of HR_reserve – 45 min	↑TG 1 h-6 h	↓TROLOX 4 h ↑H₂O₂ 1 h-6 h ↑XO 1 h-6 h ↑MDA 1 h-6 h	NA
Jenkins et al.²¹21 Jenkins NT, Landers RQ, Thakkar SR, et al. Prior endurance exercise prevents postprandial lipaemia-induced increases in reactive oxygen species in circulating CD31+ cells. J Physiol. 2011;589(22):5539-53. http://dx.doi.org/10.1113/jphysiol.2011.215277. PMid:21930598. http://dx.doi.org/10.1113/jphysiol.2011....	Trained young men (10)	Subacute on cycle ergometer at 70% VO_2max	↑TG 3 h and 4 h in controls ↓TG 1 h and 3 h exercise group vs. controls ↓TG AUC exercise vs. control	↑ROS (CD31⁺/CD14^-/CD34^-) 4 h in controls ↑LDL-Ox 4 h in controls = NO (CD31⁺/CD14^-/CD34^-)	NA
Gabriel et al.²⁰20 Gabriel B, Ratkevicius A, Gray P, Frenneaux MP, Gray SR. High-intensity exercise attenuates postprandial lipaemia and markers of oxidative stress. Clin Sci 2012;123(5):313-21. http://dx.doi.org/10.1042/CS20110600. PMid:22435779. http://dx.doi.org/10.1042/CS20110600...	Active young men (9)	Subacute on treadmill at 7 km/h - 30min Subacute interval exercise on cycle ergometer at 7.5% of the BM – 30 s x 4 min Rec	= TG = INS ↓ TG AUC interval exercise group vs. controls	↑ Carbonyls 2 h and 5 h in controls and walking ↑TBARS 2 h and 5 h ↓TBARS 2 h and 5 h interval exercise group vs. walking and control	NA
Sedgwick et al.²⁸28 Sedgwick MJ, Morris JG, Nevill ME, Tolfrey K, Nevill A, Barrett LA. Effect of exercise on postprandial endothelial function in adolescent boys. Br J Nutr. 2013;110(2):301-9. http://dx.doi.org/10.1017/S0007114512004977. PMid:23218136. http://dx.doi.org/10.1017/S0007114512004...	Adolescent boys (13)	Subacute interval exercise on treadmill at 60% VO_2max – 4 x 60 min	↑TG 1 h, 2 h, 4 h, 4h30 and 6h30 ↓TG AUC exercise group vs. controls = NS	NA	↓FMD 32% after breakfast and 24% after lunch in controls ↓FMD 6% after breakfast and 10% after lunch in exercise group
Canale et al.²⁹29 Canale RE, Farney TM, McCarthy CG, Bloomer RJ. Influence of acute exercise of varying intensity and duration on postprandial oxidative stress. Eur J Appl Physiol. 2014;114(9):1913-24. http://dx.doi.org/10.1007/s00421-014-2912-z. PMid:24907974. http://dx.doi.org/10.1007/s00421-014-291...	Trained young men (12)	Acute on cycle ergometer at 70% FC_max - 60min Acute interval exercise on cycle ergometer at 100% W_max - 60 s x 225 s Rec Acute interval exercise on cycle ergometer 200% W_max – 15 s x 116 s Rec	↑TG 2 h and 4 h	↑MDA 2h and 4h ↑H₂O₂ 2h and 4h = GPx ↓CAT 2 h and 4 h ↓SOD 2 h and 4 h ↑TAS interval exercise 15 s vs. controls and 60 min aerobic	NA
Sedgwick et al.³⁰30 Sedgwick MJ, Morris JG, Nevill ME, Barrett LA. Effect of repeated sprints on postprandial endothelial function and triacylglycerol concentrations in adolescent boys. J Sports Sci. 2015;33(8):806-16. PMid:25357120.	Active adolescents (14)	Subacute interval exercise on treadmill at 70% VO_2max - 6 x 10 min	↑TG 1 h, 3 h, 4 h, 4h30 and 6h30 ↓TG AUC exercise group vs. controls = INS	NA	↓FMD 3 h and 6h30 controls vs. exercise ↑ BAD 3 h and 6h30 ↑SR 6h30
Augustine et al.³¹31 Augustine J, Tarzia B, Kasprowicz A, Heffernan KS. Effect of a single bout of resistance exercise on arterial stiffness following a high-fat meal. Int J Sports Med. 2014;35(11):894-9. http://dx.doi.org/10.1055/s-0033-1363266. PMid:24886920. http://dx.doi.org/10.1055/s-0033-1363266...	Active young men (10)	Acute resistance training	↑ TG after meal, controls vs. exercise group = HDL	NA	↓ PWV after exercise vs. before exercise ↑ PWV after meal vs. before meal in controls

[1] Conflicts of interest: No conflicts of interest declared concerning the publication of this article.

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Oxidative stress and endothelial function: effects of physical exercise on results of postprandial lipemia

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