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Influence of mental stress and circadian cycle on postprandial lipemia^1,2,3

¹ From CERESTE, Service de Nutrition, and Service de Pharmacologie Hospitalière, CHR et U de Lille, Lille, France; INSERM U-325, INSERM CJF 95–05, and Département d'Athérosclérose, Institut Pasteur de Lille, Lille, France; CERIM, Faculté de Médecine Lille II, Lille, France; and ECCHAT, Faculté de Philosophie, Sciences Humaines, Amiens, France.

² Supported by grant 931501 from INSERM and by an unrestricted grant from GIP Cereste, Ministère de la Santé et Solidarité Nationale.

³ Address reprint requests to J Dallongeville, Institut Pasteur de Lille, 1 rue du Professeur Calmette, 59019 Lille, Cedex, France. E-mail: jean.dallongeville{at}pasteur-lille.fr.

	ABSTRACT

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Background: Mental stress produces alterations in serum lipids and lipoproteins.

Objective: The objective was to assess the effect of mental stress during the day and night on postprandial lipoproteins.

Design: Fourteen healthy subjects aged 26.6 ± 5.0 y were given randomly the same meal either at night (0100) or during the day (1300), with or without (control session) a mental stress challenge. The meal contained 40% of estimated daily energy needs. The mental task was performed on a computer and consisted of a task of choice reaction. Blood samples were drawn at baseline and hourly for 7 h after the meal.

Results: Urinary epinephrine concentrations were higher (P < 0.012) during the mental task than during the control sessions. Repeated-measures analysis of variance showed that mean postprandial triacylglycerol concentrations were significantly higher (P < 0.02) and total cholesterol (P < 0.0001) and HDL-cholesterol concentrations were significantly lower (P < 0.0001) at night than during the day. The mean postprandial VLDL-triacylglycerol concentration was significantly higher (P < 0.04) during the mental task than during the control sessions. Similarly, the VLDL-cholesterol response, calculated as the area under the postprandial curve, was significantly greater (P < 0.02) during the mental task than during the control sessions. There was no interaction between mental stress and nyctohemeral cycle on postprandial lipoprotein responses, suggesting that both indexes act independently on postprandial lipid metabolism.

Conclusions: Mental stress is associated with increased concentrations of postprandial triacylglycerol-rich lipoprotein fractions. Therefore, postprandial hyperlipidemia is one possible mechanism contributing to the higher risk of ischemic heart disease in stressed people.

Key Words: Nutrition • postprandial metabolism • cholesterol • triacylglycerol • lipoproteins • circadian cycle • mental stress • epi-nephrine • humans • men

	INTRODUCTION

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Numerous studies have shown that mental stress influences lipid and lipoprotein concentrations (1–7). In these experiments, an increase in total cholesterol, triacylglycerol, LDL cholesterol, and HDL cholesterol was generally observed (1–7). These lipid and lipoprotein changes have been attributed to the effect of epinephrine on lipoprotein lipase (8, 9), hepatic lipase (10), and hormone-sensitive lipase (11) activities. The overall effect of epinephrine action on these enzymes is to increase fatty acid efflux from adipose tissue (11), providing the liver with substrate for triacylglycerol synthesis and VLDL production. Additional investigations showed that short-term stress caused by tests results in hemoconcentration, which contributes to increases in the concentrations of circulating lipids and lipoproteins (1, 2).

Postprandial lipemia is a dynamic process characterized by increased concentrations of triacylglycerol after fat ingestion. Many conditions, such as age, physical activity, body weight, dyslipidemia, and apolipoprotein E polymorphism, affect the intensity of postprandial lipemia (12–15). The circadian cycle also influences postprandial lipid metabolism, with higher triacylglycerol concentrations after a meal eaten at night than during the day (16).

Studies to date that analyzed the effect of stress on lipoprotein metabolism were performed in fasting subjects during the day. The aim of the present study was to test the hypothesis that mental stress alters postprandial lipid and lipoprotein responses. Furthermore, because the circadian cycle also influences postprandial triacylglycerol metabolism, we assessed the possible effect of this cycle on stress-related changes in postprandial lipids.

	SUBJECTS AND METHODS

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Subjects
Fourteen healthy men aged 26.6 ± 5.0 y were recruited for the study from the University of Lille II through advertisements and posters. The mean age and body mass index (BMI; in kg/m²) were 25.6 ± 5.0 y and 22.4 ± 2.2, respectively. Exclusion criteria were as follows: obesity (BMI >27), unstable weight (change in weight >2 kg in the last 3 mo), high blood pressure, smoking, medication use that might affect the sympathetic or parasympathetic systems, night or shift work, and travel across time zones in the preceding 6 mo. All potential volunteers had a fasting blood sample drawn for screening of diabetes, hyperlipidemia, and impaired thyroid, hepatic, or renal function. Furthermore, they had to answer a questionnaire concerning their daily routines and sleep and meal schedules. Those with irregular habits were excluded. Each subject was informed about the nature and the purpose of the study and was enrolled after giving informed consent. The hospital ethics committee (CCPRB de Lille, CHR et U de Lille) approved the protocol according to the current regulations in France. During the 24 h preceding each session, the subjects were reminded to refrain from exercising and consuming alcohol.

Experimental design
The study was performed in the Centre d'Investigation Clinique of the CHR et U de Lille. Four experimental procedures took place in a randomized sequence: 2 sessions during the day (between 0730 and 2030), 1 with and 1 without a mental task, and 2 sessions at night (between 1930 and 0830), 1 with and 1 without a mental task. Between sessions, there was a minimum time span of 5 d. All subjects completed the 4 sessions within 5 wk. On arrival, participants consumed a light meal providing 20% of their theoretical energy needs (calculated as 1.5 x basal metabolic needs; 17) and stayed in the ward, reading or watching TV; they were allowed to drink water only. At 1300 and 0100, a blood sample was collected and the subjects then consumed a test meal. Heart rates were recorded with an electrocardiogram during each experiment with a Holter HELA device recorder (18).

Test meal
The test meal was a mixed meal composed of bread, butter, ham or cheese, apple marmalade, and cottage cheese. Each subject consumed exactly the same meal during the 4 sessions. The meal provided 4186 kJ and the percentage of energy derived from protein, fat, and carbohydrate was 16%, 34%, and 50%, respectively.

Mental task
The mental challenge was performed on a computer and consisted of a task of choice reaction. Briefly, the subjects were presented rapidly and simultaneously 3 geometric figures on the computer screen. They had to recognize as soon as possible the shape of the figure and indicate by pressing a key on the computer keyboard the one with bold lines. The task lasted 10 min and was presented every 30 min during the 5 h after the meal. During the control sessions, the subjects operated the computer keyboard according to the same schedule used in the experimental sessions. Between mental challenges, the subjects were allowed to watch light-entertainment movies, but were not allowed to sleep.

Blood samples
An indwelling venous canula was inserted into an antecubital vein 1 h before the test meal. The first sample was drawn before the meal was eaten and then hourly for the 7 h after the meal.

Lipid measurements
Blood was collected into dry tubes and allowed to clot for 1 h. Serum was separated by centrifugation at 3300 x g for 20 min at 4°C. Lipoproteins were separated according to standard procedures by a combination of ultracentrifugation (see below) [at a density (d) of 1.006 kg/L] and Mg²⁺-phosphotungstate precipitation. HDL cholesterol was measured after precipitation by using commercially available reagents (CHOD/PAP; Boehringer Mann- heim, Mannheim, Germany). VLDLs were separated from 0.5 mL serum by ultracentrifugation with a Beckman TL100 (Palo Alto, CA) in a single spin (d = 1.006 kg/L) (19) with modifications. Briefly, 0.5 mL of 0.9% NaCl was added to 0.5 mL serum and spun in a polycarbonate tube (400000 x g at 20°C for 2.5 h) in a Beckman 100.2 Ti rotor for 3 h. The tube was cut in 2 parts and the remaining 0.5-mL infranate was analyzed for lipids. The triacylglycerol-rich-lipoprotein (TRL) (d < 1.006 kg/L) fraction was measured by subtracting infranatant values from serum concentrations and LDL cholesterol was quantified by subtracting the HDL-cholesterol concentration from the infra-natant cholesterol concentration. Cholesterol and triacylglycerols were measured by using Boehringer Mannheim reagents (reference nos. 1.040.1839 and 1.058.550, respectively). The intra- and interseries CVs were 1% and 1.3% for cholesterol and 1.1% and 1.8% for triacylglycerol, respectively. Six-hour urine samples were collected during each session into containers containing hydrochloric acid. Urinary epinephrine concentrations were measured by HPLC with electrochemical detection as described previously (20).

Statistical analysis
Three-way analysis of variance (ANOVA) with repeated measures was performed to assess the effect of mental task (stress or no stress), mealtime (night or day), and postprandial interval (t_0h, t_1h, t_2h, t_3h, t_4h, t_5h, t_6h, or t_7h) on lipid and lipoprotein concentrations. The percentage change was calculated at each time point as follow:

(1)

where t_x varies from t_0h (baseline) to t_7h. The lipid postprandial areas under the curves (AUC) were calculated as follow:

(2)

where t_x varies from t₀ to t_7. Because of the small number of subjects in this study and to avoid the potential confounding effect of non-Gaussian distribution and outlier values, a nonparametric statistical procedure was preferred for three-way ANOVA with repeated measures (21). This procedure included a rank transformation of each variable followed by the standard ANOVA procedure (22). The level of statistical significance was set at P < 0.05.

	RESULTS

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Baseline lipid concentrations
Baseline serum cholesterol (range: 2.9–5.7 mmol/L) and triacylglycerol (0.55–1.73 mmol/L) concentrations were within the expected normal range for age and sex. Three-way ANOVA with repeated measures did not show any significant differences in baseline lipid and lipoprotein concentrations between the 4 sessions (Table 1).

View larger version (22K): [in this window] [in a new window]   FIGURE 1. Mean (±SEM) urinary epinephrine excretion of the 14 subjects during the day and at night during the mental task (stress) and control (no stress) sessions. Two-way ANOVA with repeated measures indicated a significant main effect of mealtime (P < 0.0001) and stress (P < 0.012), but no significant interaction between the 2 variables.

View larger version (23K): [in this window] [in a new window]   FIGURE 2. Mean (±SD) serum triacylglycerol (TG) and very-low-density-lipoprotein-TG (VLDL-TG) concentrations at baseline (t0) and every hour postprandially (t1 to t7) during the day and at night during the mental task (stress; triangles) and control (no stress; circles) sessions. Three-way ANOVA with repeated measures indicated a significant main effect of postprandial interval on TG (P < 0.0001) and VLDL-TG (P < 0.0001) concentrations as well as a significant interaction between mental task and postprandial interval for VLDL-TG (P < 0.04) but not for TG. n = 14.

View larger version (25K): [in this window] [in a new window]   FIGURE 3. Mean (±SD) serum LDL-cholesterol (LDL-C) and HDL-cholesterol (HDL-C) concentrations at baseline (t0) and every hour postprandially (t1 to t7) during the day and at night during the mental task (stress; closed symbols) and control (no stress; open symbols) sessions. Three-way ANOVA with repeated measures indicated a significant main effect of postprandial interval on total cholesterol (P < 0.001) and HDL-C (P < 0.0001) concentrations, but no significant interaction between mental task and postprandial interval for the 2 variables. n = 14.

Influence of mental stress on postprandial lipemia
Three-way ANOVA with repeated measures indicated a significant interaction between mental task and postprandial interval for VLDL triacylglycerol (P < 0.04). One to 2 h after the meal, mean VLDL-triacylglycerol concentrations were similar during the mental task and control sessions, but were higher (NS) during the mental task than during the control session 3 h postprandially and later. Postprandial concentrations of triacylglycerol, cholesterol, VLDL cholesterol, LDL cholesterol, and HDL cholesterol were not significantly affected by the mental task. There was, however, a nearly significant main effect of mental task for VLDL cholesterol (P < 0.075) and LDL cholesterol (P < 0.086). VLDL cholesterol and LDL cholesterol tended to be higher and lower (NS), respectively, during the mental task than during the control session.

Because baseline lipid concentrations influence postprandial lipid responses, the analyses were repeated after the values were expressed as percentage changes. Three-way ANOVA with repeated measures showed a significant interaction between mental task and postprandial interval for the percentage change in VLDL triacylglycerol from baseline (P < 0.02). The percentage increase in VLDL triacylglycerol was higher late postprandially during the mental task than during the control sessions. Postprandial changes in triacylglycerol, cholesterol, and HDL cholesterol were not significantly affected by mental task after adjustment for baseline values. There was, however, a significant main effect of stress on the percentage change in VLDL cholesterol (P < 0.05) and a nearly significant effect of stress on the percentage change in LDL cholesterol (P < 0.092).

A two-way repeated-measures ANOVA with the AUCs of triacylglycerol and the lipoproteins as dependent variables showed no evidence of a significant interaction between mealtime (night or day) and mental task (stress or no stress) for any of these variables (Figure 4). There was, however, a significant main effect of mental task on the AUC for VLDL cholesterol, but not on the AUCs for total triacylglycerol, VLDL triacylglycerol, total cholesterol, LDL cholesterol, or HDL cholesterol. The AUC for VLDL cholesterol was greater during the mental task than during the control sessions. There was also a significant main effect of nyctohemeral cycle on the AUCs for total cholesterol and HDL cholesterol, but not on the AUCs for total tri-acylglycerol, VLDL triacylglycerol, VLDL cholesterol, and LDL cholesterol. The AUCs for total cholesterol and HDL cholesterol were lower at night than during the day.

View larger version (41K): [in this window] [in a new window]   FIGURE 4. Mean (±SEM) area under the curve for total triacylglycerol (TG), very-low-density-lipoprotein-TG (VLDL-TG), VLDL-cholesterol (VLDL-C), total cholesterol, LDL-cholesterol (LDL-C), and HDL-cholesterol (HDL-C) concentrations by mealtime [day (D) or night (N)] and mental task session (+ stress). Three-way ANOVA with repeated measures indicated a significant main effect of mental task on VLDL-C (P < 0.02) and a main effect of mealtime on total cholesterol (P < 0.04) and HDL-C (P < 0.02), but not on the other variables.

	DISCUSSION

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The protocol used in the present study differed from the protocols used in other investigations. In previous studies, the stressor included the Stroop interference test, mental arithmetic calculation, motor coordination challenge, or speaking before a camera. The duration of the stress test ranged from a few to 20 min and blood sampling was performed either immediately or shortly after the stress challenge. In the present study, the stress constraint lasted 10 min and was repeated every half-hour for 5 h after the meal. This strategy was used to simulate a condition with repeated stress, such as job stress. One limitation of this strategy, however, was that the subjects were progressively accustomed to the stressors after repeated stimulation. Therefore, the magnitude of the reaction to the stress, assessed by the transient increase in heart rates during the mental task, declined during the experiment (Figure 5). However, the increase in urinary epinephrine indicated that the mental task in the present study induced a significant amount of stress. Urinary epinephrine secretion was lower at night than during the day, an observation that is compatible with a circadian cycle of epinephrine secretion (24). These lower nocturnal epinephrine concentrations did not affect the reaction to stress, suggesting independent influences of circadian rhythm and mental stress.

View larger version (23K): [in this window] [in a new window]   FIGURE 5. Heart rate of a representative subject during a mental task (stress) and control (no stress) session.

The postprandial responses of serum total cholesterol, LDL cholesterol, and HDL cholesterol were not affected by stress. This finding contrasts with the findings of studies performed in fasting subjects in whom short-term stress challenges were usually associated with increased cholesterol, LDL-cholesterol, and HDL-cholesterol concentrations (1–7). During postprandial metabolism, total cholesterol concentrations tend to decrease as the result of decreased LDL and HDL concentrations (28). This postprandial change could theoretically mask the potential increase in LDLs and HDLs resulting from stress. Overall, these findings highlight the differences in stress-related lipoprotein changes between fasting and fed conditions (29).

As in our previous study (16), we found that circadian cycle has a clear influence on postprandial lipemia. Postprandial serum triacylglycerol was higher (NS) and total cholesterol and HDL cholesterol were significantly lower at night than during the day, independent of baseline concentrations. Despite this clear influence, the intensity of the stress-related postprandial lipid response was not significantly affected by the circadian cycle. Moreover, the lower secretion of epinephrine at night than during the day was not associated with a decreased response of lipoproteins to stress, suggesting that circadian cycle and stress act independently on postprandial lipemia.

In conclusion, evidence has accumulated that postprandial dyslipidemia is a risk factor for ischemic heart disease (13–15). Increased chylomicron-remnant concentrations and decreased HDL-cholesterol concentrations have been observed in patients with angiographically verified ischemic heart disease and survivors of myocardial infarction (30, 31). In the present study, we showed that stress alters postprandial triacylglycerol metabolism. This finding suggests that postprandial dyslipidemia is one possible mechanism contributing to the higher risk of ischemic heart disease in stressed people.

	ACKNOWLEDGMENTS

 
We thank the staff of the Centre d'Investigation Clinique du CHR et U de Lille for their excellent clinical intervention.

	REFERENCES

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1. Muldoon MF, Herbert TB, Patterson SM, Kameneva M, Raible R, Manuck SB. Effects of acute psychological stress on serum lipid levels, hemoconcentration, and blood viscosity. Arch Intern Med 1995;155:615–20.[Abstract]
2. Patterson SM, Gottdiener JS, Hecht G, Vargot S, Krantz DS. Effects of acute mental stress on serum lipids: mediating effects of plasma volume. Psychosom Med 1993;55:525–32.[Abstract/Free Full Text]
3. McCann BS, Magee MS, Broyles FC, Vaughan M, Albers JJ, Knopp RH. Acute psychological stress and epinephrine infusion in normolipidemic and hyperlipidemic men: effects on plasma lipid and apoprotein concentrations. Psychosom Med 1995;57:165–76.[Abstract/Free Full Text]
4. Muldoon MF, Bachen EA, Manuck SB, Waldstein SR, Bricker PL, Bennett JA. Acute cholesterol responses to mental stress and change in posture. Arch Intern Med 1992;152:775–80.[Abstract]
5. Davis MC, Matthews KA. Cigarette smoking and oral contraceptive use influence women's lipid, lipoprotein, and cardiovascular responses during stress. Health Psychol 1990;9:717–36.[Medline]
6. Spence JD, Manuck SB, Munoz C, et al. Hemodynamic and endocrine effects of mental stress in untreated borderline hypertension. Am J Hypertens 1990;3:859–62.[Medline]
7. Lundberg U, Fredrikson M, Wallin L, Melin B, Frankenhaeuser M. Blood lipids as related to cardiovascular and neuroendocrine functions under different conditions in healthy males and females. Pharmacol Biochem Behav 1989;33:381–6.[Medline]
8. Yukht A, Davis RC, Ong JM, Ranganathan G, Kern PA. Regulation of lipoprotein lipase translation by epinephrine in 3T3-L1 cells. Importance of the 3' untranslated region. J Clin Invest 1995;96:2438–44.
9. Ong JM, Saffari B, Simsolo RB, Kern PA. Epinephrine inhibits lipoprotein lipase gene expression in rat adipocytes through multiple steps in posttranscriptional processing. Mol Endocrinol 1992;6:61–9.[Abstract]
10. Neve BP, Verhoeven AJ, Jansen H. Acute effects of adrenaline on hepatic lipase secretion by rat hepatocytes. Metabolism 1997;46:76–82.[Medline]
11. Samra JS, Simpson EJ, Clark ML, et al. Effects of epinephrine infusion on adipose tissue: interactions between blood flow and lipid metabolism. Am J Physiol 1996;271:E834–9.[Abstract/Free Full Text]
12. Dallongeville J, Fruchart JC. Postprandial dyslipidemia: a risk factor for coronary heart disease. Ann Nutr Metab 1998;42:1–11.[Medline]
13. Bergeron N, Havel RJ. Assessment of postprandial lipemia: nutritional influences. Curr Opin Lipidol 1997;8:43–52.[Medline]
14. Karpe F, Hamsten A. Postprandial lipoprotein metabolism and atherosclerosis. Curr Opin Lipidol 1995;6:123–9.[Medline]
15. Havel RJ. Postprandial hyperlipidemia and remnant lipoproteins. Curr Opin Lipidol 1994;5:102–9.[Medline]
16. Romon M, Le Fur C, Lebel P, Edmé J-L, Fruchart J-C, Dallongeville J. Circadian variation of postprandial lipemia. Am J Clin Nutr 1997;65:934–40.[Abstract/Free Full Text]
17. Schofield WN. Predicting basal metabolic rate, new standards and review of previous work. Hum Nutr Clin Nutr 1985;39:5–41.
18. Huikuri HV, Kessler KM, Terracall E, Castellanos A, Linnaluoto MK, Myerburg RJ. Reproducibility and circadian rhythm of heart rate variability in healthy subjects. Am J Cardiol 1990;65:391–3.[Medline]
19. Traber MG, Kayden HJ, Rindler MJ. Polarized secretion of newly synthesized lipoproteins by the Caco-2 human intestinal cell line. J Lipid Res 1987;28:1350–63.[Abstract]
20. Moyer TP, Jiang NS, Tyce GM, Sheps SG. Analysis for urinary catecholamines by liquid chromatography with amperometric detection: methodology and clinical interpretation of results. Clin Chem 1979;25:256–63.[Abstract/Free Full Text]
21. Conover WJ, Iman RL. Rank transformations at a bridge between parametric and nonparametric statistics. Am Statistician 1981;35:124–33.
22. Winner BJ, Brown DR, Michels KM. Statistical principles in experimental design. New York: McGraw-Hill, Inc, 1991.
23. Brown AJ, Roberts DC. The effect of fasting triacylglyceride concentration and apolipoprotein E polymorphism on postprandial lipemia. Arterioscler Thromb 1991;11:1737–44.[Abstract/Free Full Text]
24. Linsell CR, Lightman SL, Mullen PE, Brown MJ, Causon RC. Circadian rhythms of epinephrine and norepinephrine in man. J Clin Endocrinol Metab 1985;60:1210–5.[Abstract]
25. Slavin BG, Ong JM, Kern PA. Hormonal regulation of hormone-sensitive lipase activity and mRNA levels in isolated rat adipocytes. J Lipid Res 1994;35:1535–41.[Abstract]
26. Divertie GD, Jensen MD, Cryer PE, Miles JM. Lipolytic responsiveness to epinephrine in nondiabetic and diabetic humans. Am J Physiol 1997;272:E1130–5.[Abstract/Free Full Text]
27. Thomas SH, Wisher MH, Brandenburg D, Sonksen PH. Insulin action on adipocytes. Evidence that the anti-lipolytic and lipogenic effects of insulin are mediated by the same receptor. Biochem J 1979;184:355–60.[Medline]
28. Dubois C, Beaumier G, Juhel C, et al. Effects of graded amounts (0–50 g) of dietary fat on postprandial lipemia and lipoproteins in normolipidemic adults. Am J Clin Nutr 1998;67:31–8.[Abstract]
29. Brindley DN, McCann BS, Niaura R, Stoney CM, Suarez EC. Stress and lipoprotein metabolism: modulators and mechanisms. Metabolism 1993;42:3–15.[Medline]
30. Patsch JR, Miesenbock G, Hopferwieser T, et al. Relation of triglyceride metabolism and coronary artery disease. Studies in the postprandial state. Arterioscler Thromb 1992;12:1336–45.[Abstract/Free Full Text]
31. Karpe F, Steiner G, Uffelman K, Olivecrona T, Hamsten A. Postprandial lipoproteins and progression of coronary atherosclerosis. Atherosclerosis 1994;106:83–97.[Medline]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Le Fur, C. Articles by Dallongeville, J. Search for Related Content PubMed PubMed Citation Articles by Le Fur, C. Articles by Dallongeville, J. Agricola Articles by Le Fur, C. Articles by Dallongeville, J.