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Research Article| Volume 42, ISSUE 9, SUPPLEMENT 1, 3-15, September 1993

Stress and lipoprotein metabolism: Modulators and mechanisms

  • David N. Brindley
    Correspondence
    Address reprint requests to David N. Brindley, PhD, Department of Biochemistry, 332 Heritage Medical Research Centre, University of Alberta, Edmonton, T6G 2SC, Alberta, Canada.
    Affiliations
    Department of Biochemistry, University of Alberta, Edmonton, Canada

    Department of Psychiatry and Behavioral Sciences, Cardiovascular Behavioral Medicine Program, University of Washington School of Medicine, Seattle, WA USA

    Division of Behavioral Medicine, Brown University, Miriam Hospital, Providence, RI USA

    the Department of Psychiatry, Duke University Medical Center, Durham, NC USA.

    Lipid and Lipoprotein Research Group, University of Alberta, Edmonton, Canada
    Search for articles by this author
  • Barbara S. McCann
    Affiliations
    Department of Biochemistry, University of Alberta, Edmonton, Canada

    Department of Psychiatry and Behavioral Sciences, Cardiovascular Behavioral Medicine Program, University of Washington School of Medicine, Seattle, WA USA

    Division of Behavioral Medicine, Brown University, Miriam Hospital, Providence, RI USA

    the Department of Psychiatry, Duke University Medical Center, Durham, NC USA.

    Lipid and Lipoprotein Research Group, University of Alberta, Edmonton, Canada
    Search for articles by this author
  • Raymond Niaura
    Affiliations
    Department of Biochemistry, University of Alberta, Edmonton, Canada

    Department of Psychiatry and Behavioral Sciences, Cardiovascular Behavioral Medicine Program, University of Washington School of Medicine, Seattle, WA USA

    Division of Behavioral Medicine, Brown University, Miriam Hospital, Providence, RI USA

    the Department of Psychiatry, Duke University Medical Center, Durham, NC USA.

    Lipid and Lipoprotein Research Group, University of Alberta, Edmonton, Canada
    Search for articles by this author
  • Catherine M. Stoney
    Affiliations
    Department of Biochemistry, University of Alberta, Edmonton, Canada

    Department of Psychiatry and Behavioral Sciences, Cardiovascular Behavioral Medicine Program, University of Washington School of Medicine, Seattle, WA USA

    Division of Behavioral Medicine, Brown University, Miriam Hospital, Providence, RI USA

    the Department of Psychiatry, Duke University Medical Center, Durham, NC USA.

    Lipid and Lipoprotein Research Group, University of Alberta, Edmonton, Canada
    Search for articles by this author
  • Edward C. Suarez
    Affiliations
    Department of Biochemistry, University of Alberta, Edmonton, Canada

    Department of Psychiatry and Behavioral Sciences, Cardiovascular Behavioral Medicine Program, University of Washington School of Medicine, Seattle, WA USA

    Division of Behavioral Medicine, Brown University, Miriam Hospital, Providence, RI USA

    the Department of Psychiatry, Duke University Medical Center, Durham, NC USA.

    Lipid and Lipoprotein Research Group, University of Alberta, Edmonton, Canada
    Search for articles by this author
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      Abstract

      Elevated concentrations of triglycerides and low-density lipoprotein (LDL) cholesterol,1 especially in combination with low concentrations of high-density lipoprotein (HDL) cholesterol,2 are associated with an increased risk of atherosclerosis, coronary heart disease, and stroke. While several dietary and genetic factors contribute to atherogenic lipoprotein profiles,3,4 stress also contributes to unfavorable concentrations of lipoproteins that may predispose to cardiovascular disease.5,6 This report reviews the data supporting a link between stress and lipid metabolism, with particular focus on the mechanisms whereby stress could be related to increased lipid concentrations, and several factors which could modulate a relationship between stress and lipid levels. Following a brief discussion of stress, this report is divided into three main sections. First, data that support a relationship between stress and lipoprotein metabolism are considered. Data from laboratory studies, studies of episodic and chronic stress, studies on personality, and experiments from the animal literature are reviewed. The second major section discusses mechanisms that could account for stress effects on lipoprotein metabolism. This section considers the metabolic effects of stress, the effects of stress on hemoconcentration, and behavioral responses to stress that could affect lipid concentrations. The final major section reviews various modulators of the stress-lipid relationship, including intervening personality variables, gender, diet, seasonal variations in lipoprotein concentrations, and genetics and polymorphism. The concluding comments in this review address several promising areas for further research.
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      References

        • Castelli W.P.
        • Garrison R.J.
        • Wilson PWF
        • et al.
        Incidence of coronary heart disease and lipoprotein cholesterol levels: The Framingham Study.
        JAMA. 1986; 256: 2835-2838
        • Wilson P.W.F.
        • Abbott R.D.
        • Castelli W.P.
        High density lipoprotein cholesterol and mortality: The Framingham Heart Study.
        Arteriosclerosis. 1988; 8: 737-741
        • Kris-Etherton P.M.
        • Krummel D
        • Russell M.E.
        • et al.
        The effect of diet on plasma lipids, lipoproteins, and coronary heart disease.
        J Am Diet Assoc. 1988; 88: 1373-1400
        • Brown M.S.
        • Goldstein J.L.
        The hyperlipoproteinemias and other disorders of lipid metabolism.
        in: Harrison's Principles of Internal Medicine. vol 10. McGraw Hill, New York, NY1983: 547-559
        • Dimsdale J.E.
        • Herd J.A.
        Variability of plasma lipids in response to emotional arousal.
        Psychosom Med. 1982; 44: 413-430
        • Niaura R
        • Stoney C.M.
        • Herbert P.N.
        Lipids in psychological research: The last decade.
        Biol Psychol. 1992; 34: 1-43
        • Lazarus R.S.
        Emotion and Adaptation. Oxford University Press, New York, NY1991
        • Lazarus R
        • Folkman S
        Stress, Appraisal, and Coping. Springer, New York, NY1984
        • Kunihara M
        • Oshima T
        Effects of epinephrine on plasma cholesterol levels in rats.
        J Lipid Res. 1983; 24: 639-644
        • O'Donnell L
        • Owens D
        • McGee C
        • et al.
        Effects of catecholamines on serum lipoproteins of normally fed and cholesterol-fed rabbits.
        Metabolism. 1988; 37: 910-915
        • Deverey R
        • O'Donnell L
        • Tomkin G.H.
        Effect of catecholamines on the hepatic rate-limiting enzymes of cholesterol metabolism in normally fed and cholesterol-fed rabbits.
        Biochim Biophys Acta. 1986; 887: 173-181
        • Robertson R.P.
        • Smith P.H.
        Stress-induced inhibition of triglyceride secretion in vivo in sand rats (Psammomys obesus).
        Metabolism. 1976; 25: 1583-1590
        • Berger D.F.
        • Starzec J.J.
        • Mason E.B.
        • et al.
        The effects of differential psychological stress on plasma cholesterol levels in rats.
        Psychosom Med. 1980; 42: 481-492
        • Bryant H.U.
        • Story J.A.
        • Yim G.K.W.
        Assessment of endogenous opioid mediation in stress-induced hypercholestrolemia in the rat.
        Psychosom Med. 1988; 50: 576-585
        • Lang C.M.
        Effects of psychic stress on atherosclerosis in the squirrel monkey (Saimiri sciureus).
        in: Proc Soc Exp Biol Med. 126. 1967: 30-34
        • St. Clair R.W.
        • MacNitch J.W.
        • Middleton C.C.
        • et al.
        Changes in serum cholesterol levels of squirrel monkeys during importation and acclimation.
        Lab Invest. 1967; 16: 828-832
        • Kaplan J.R.
        • Manuck S.B.
        • Clarkson T.B.
        • et al.
        Social stress and atherosclerosis in normocholesterolemic monkeys.
        Science. 1983; 220: 733-735
        • Williams J.K.
        • Vita J.A.
        • Manuck S.B.
        • et al.
        Psychosocial factors impair vascular responses of coronary arteries.
        Circulation. 1991; 84: 2146-2153
        • Bramblett C.A.M.
        • Coelho A.M.
        • Mott G.E.
        Behavior and serum cholesterol in a group of Cercopithecus aethiops.
        Primates. 1981; 22: 96-102
        • Sapolsky R.M.
        • Mott G.E.
        Social subordinance in wild baboons is associated with suppressed high density lipoprotein-cholesterol concentrations: The possible role of chronic social stress.
        Endocrinology. 1987; 121: 1605-1610
        • Clarkson T.B.
        • Adams M.R.
        • Kaplan J.R.
        • et al.
        Psychosocial and reproductive influences on plasma lipids, lipoproteins, and atherosclerosis in nonhuman primates.
        J Lipid Res. 1984; 25: 1629-1634
        • Dimsdale J.E.
        • Herd J.A.
        • Hartley L.H.
        Epinephrine mediated increases in plasma cholesterol.
        Psychosom Med. 1983; 45: 227-232
        • Sane A.S.
        • Kukreti S.C.
        Effect of preoperative stress on serum cholesterol level in humans.
        Experientia. 1978; 34: 213-214
        • Taggart P
        • Carruthers M
        Endogenous hyperlipidæmia induced by emotional stress of racing driving.
        Lancet. 1971; 1: 363-366
        • Zarafonetis C.J.D.
        • Seifter J
        • Baeder D
        • et al.
        Lipid mobilization as a consequence of surgical stress.
        Am J Med Sci. 1959; 237: 418-433
        • Davis M.C.
        • Matthews K.A.
        Cigarette smoking and oral contraceptive use influence women's lipid, lipoprotein, and cardiovascular responses during stress.
        Health Psychol. 1990; 9: 717-736
        • Matthews K.A.
        • Davis M.C.
        • Stoney C.M.
        • et al.
        Does the gender relevance of the stressor influence sex differences in psychophysiological responses?.
        Health Psychol. 1991; 10: 112-120
        • Muldoon M.F.
        • Bachen E.A.
        • Manuck S.B.
        • et al.
        Acute cholesterol responses to mental stress and change in posture.
        Arch Intern Med. 1992; 152: 775-780
        • Spence J.D.
        • Manuck S.B.
        • Munoz C
        • et al.
        Hemodynamic and endocrine effects of mental stress in untreated borderline hypertension.
        Am J Hypertens. 1990; 3: 859-862
        • Stoney C.M.
        • Matthews K.A.
        • McDonald R.H.
        • et al.
        Sex differences in lipid, lipoprotein, cardiovascular, and neuroendocrine responses to acute stress.
        Psychophysiology. 1988; 25: 645-656
        • Stoney C.M.
        • Owens J.F.
        • Matthews K.A.
        • et al.
        Influences of the normal menstrual cycle on physiologic functioning during behavioral stress.
        Psychophysiology. 1990; 27: 125-135
        • Bijlani R.L.
        • Sud S
        • Gandhi B.M.
        • et al.
        Relationship of examination stress to serum lipid profile.
        Indian J Physiol Pharmacol. 1986; 30: 22-30
        • Flynn M.A.
        • Anderson A
        • Rutledge M
        • et al.
        Eggs, serum lipids, emotional stress, and blood pressure in medical students.
        Arch Environ Health. 1984; 39: 90-95
        • McCann B.S.
        • Warnick G.R.
        • Knopp R.H.
        Changes in plasma lipids and dietary intake accompanying shifts in perceived work-load and stress.
        Psychosom Med. 1990; 52: 97-108
        • Niaura R
        • Herbert P.N.
        • Saritelli A.L.
        • et al.
        Lipid and lipoprotein responses to episodic occupational and academic stress.
        Arch Intern Med. 1991; 151: 2172-2179
        • Mattiasson I
        • Lindgärde F
        • Nilsson J.A.
        • et al.
        Threat of unemployment and cardiovascular risk factors: Longitudinal study of quality of sleep and serum cholesterol concentrations in men threatened with redundancy.
        Br Med J. 1990; 301: 461-466
        • Pieper C
        • LaCroix A.Z.
        • Karasek R.A.
        The relation of psychosocial dimensions of work with coronary heart disease risk factors: A meta-analysis of five United States data bases.
        Am J Epidemiol. 1989; 129: 483-494
        • Reed D.M.
        • LaCroix A.Z.
        • Karasek R.A.
        • et al.
        Occupational strain and the incidence of coronary heart disease.
        Am J Epidemiol. 1989; 129: 495-502
        • Siegrist J
        • Matschinger H
        • Cremer P
        • et al.
        Atherogenic risk in men suffering from occupational stress.
        Atherosclerosis. 1988; 69: 211-218
        • Trevisan M
        • Celentano E
        • Meucci C
        • et al.
        Short-term effect of a natural disaster on coronary heart disease risk factors.
        Arteriosclerosis. 1986; 6: 491-494
        • Trevisan M
        • Jossa F
        • Farinaro E
        • et al.
        Earthquake and coronary heart disease risk factors: A longitudinal study.
        Am J Epidemiol. 1992; 135: 632-637
        • Brindley D.N.
        • Rolland Y
        Possible connections between stress, obesity, hypertension and altered lipoprotein metabolism that may result in atherosclerosis.
        Clin Sci. 1989; 77: 453-461
      1. Brindley DN: Mechanisms for the effects of benfluorex on the obese-diabeteic-dyslipidemic syndrome. Diabetes Metab Rev (in press)

        • Bjorntorp P
        Classification of obese patients and complications related to the distribution of surplus fat.
        Nutrition. 1990; 6: 131-137
        • Després J.-P.
        • Moorjani S
        • Lupien P.J.
        • et al.
        Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease.
        Arteriosclerosis. 1990; 10: 497-511
        • Hennes M.M.I.
        • Shrago E
        • Kissebah A.H.
        Mechanism of free fatty acid effects on hepatocyte insulin receptor binding and processing.
        Obes Res. 1993; 1: 18-28
        • Brindley D.N.
        Neuroendocrine regulation and obesity.
        Int J Obes. 1992; 16: S73-S79
        • Fain J.N.
        Hormonal regulation of lipid mobilization from adipose tissue.
        in: Biochemical Actions of Hormones. vol 7. Academic, New York, NY1980: 119-204
        • Brindley D.N.
        Phosphatidate phosphohydrolase activity in the liver.
        in: Brindley D.N. Phosphatidate Phosphohydrolase. CRC, Boca Raton, FL1988: 21-77
        • Brindley D.N.
        • Salter A.M.
        Hormonal regulation of the hepatic low density lipoprotein receptor and the catabolism of low density lipoproteins: Relationship with the secretion of very low density lipoproteins.
        Prog Lipid Res. 1991; 30: 349-360
        • Howard B.V.
        • Schneiderman N
        • Falkner B
        • et al.
        Insulin, health behaviors, and lipid metabolism.
        Metabolism. 1993; 42: 25-35
        • Martin-Sanz P
        • Vance J.E.
        • Brindley D.N.
        Stimulation of apolipoprotein secretion in very-low-density and high-density lipoproteins from cultured rat hepatocytes by dexamethasone.
        Biochem J. 1990; 271: 575-583
        • Gibbons G.F.
        Assembly and secretion of hepatic very-low-density lipoprotein.
        Biochem J. 1990; 268: 1-13
        • Howard B.V.
        Lipoprotein metabolism in diabetes mellitus.
        J Lipid Res. 1987; 28: 613-625
        • Salter A.M.
        • Fisher S.C.
        • Brindley D.N.
        Binding of low-density lipoprotein to monolayer cultures of rat hepatocytes is increased by insulin and decreased by dexamethasone.
        FEBS Lett. 1987; 220: 159-162
        • Brindley D.N.
        • Brown N.F.
        • Salter A.M.
        • et al.
        Role of insulin and counter-regulatory hormones in the control of hepatic glycero-lipid synthesis and low-density-lipoprotein catabolism in diabetes.
        Biochem Soc Trans. 1989; 17: 43-46
        • Reaven G.M.
        Role of insulin resistance in human disease.
        Diabetes. 1988; 37: 1595-1607
        • Ellwood K.C.
        • Michaelis O.E.
        • Emberland J.J.
        • et al.
        Hormonal and lipogenic and gluconeogenic enzymatic responses in Math Eq rats.
        in: Proc Soc Exp Biol Med. 179. 1985: 163-167
        • Holt S
        • York D.A.
        • Fitzsimons J.T.
        The effects of corticosterone, cold exposure and overfeeding with sucrose on brown adipose tissue of obese Zucker rats (Math Eq).
        Biochem J. 1983; 214: 215-223
        • Hauner H
        • Enternmann G
        • Wabitsch M
        • et al.
        Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium.
        J Clin Invest. 1989; 84: 1663-1670
        • Spiegelman B.M.
        • Lowell B
        • Napolitano A
        • et al.
        Adrenal glucocorticoids regulate adipsin gene expression in genetically obese mice.
        J Biol Chem. 1989; 264: 1811-1815
        • Bray G.A.
        • York D.A.
        Hypothalamic and genetic obesity in experimental animals: An autonomic and endocrine hypothesis.
        Physiol Rev. 1979; 59: 719-809
        • Baulieu E.E.
        Contragestion and other clinical applications of RU 486, an antiprogesterone at the receptor.
        Science. 1989; 245: 1351-1357
        • Langley S.C.
        • York D.A.
        Effects of antiglucocorticoid RU 486 on development of obesity in obese Math Eq Zucker rats.
        Am J Physiol. 1990; 259: R539-R544
        • Standaert M.L.
        • Farese R.V.
        • Cooper DR
        • et al.
        Insulin-induced glycerolipid mediators and the stimulation of glucose transport in BC3H-1 myocytes.
        J Biol Chem. 1988; 263: 8696-8705
        • Newsholme E.A.
        • Challiss R.A.J.
        • Leighton B
        • et al.
        A possible mechanism for defective thermogenesis and insulin resistance in obesity.
        in: Berry E.M. Blondheim S.H. Eliahou H.E. Recent Advances in Obesity Research. Libbey, London, England1987: 144-150
        • Steiner G
        • Poapst M.E.
        • Shumak S.L.
        • et al.
        Metabolism of the apolipoprotein B-containing lipoproteins.
        Methods Enzymol. 1986; 129: 395-440
        • Dalderup L.M.
        Effects of posture and exertion on levels of serum cholesterol and lactic acid.
        Am Heart J. 1967; 73: 160-164
        • Hagan D.R.
        • Upton S.J.
        • Avakian E.V.
        • et al.
        Increases in serum lipid and lipoprotein levels with movement form the supine to standing position in adult men and women.
        Prev Med. 1986; 15: 18-27
        • Howes L.G.
        • Krum H
        • Louis W.J.
        Increase in plasma cholesterol on subjects' standing correlates with the increase in plasma norepinephrine.
        Clin Chem. 1988; 34: 988
        • Stoker D.J.
        • Wynn V
        Effect of posture on the plasma cholesterol level.
        Br Med J. 1966; 1: 336-338
        • Tan M.H.
        • Wilmshrust E.G.
        • Gleason R.E.
        • et al.
        Effect of posture on serum lipids.
        N Engl J Med. 1973; 289: 416-419
        • Dill D.B.
        • Costill D.L.
        Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration.
        J Appl Physiol. 1974; 37: 247-248
        • Mattiason I
        • Lindgärde F
        • Nilsson JÅ
        • et al.
        Threat of unemployment and cardiovascular risk factors: Longitudinal study of quality of sleep and serum cholesterol concentrations in men threatened with redundancy.
        BMJ. 1990; 301: 461-466
        • Kiyohara Y
        • Ueda K
        • Hasuo Y
        • et al.
        Hematocrit as a risk factor of cerebral infarction: Long-term prospective population survey in a Japanese rural community.
        Stroke. 1986; 17: 687-692
        • Sorlie P.D.
        • Garcia-Palmieri M.R.
        • Costas R
        • et al.
        Hematocrit and risk of coronary heart disease: The Puerto Rico Heart Health Program.
        Am Heart J. 1981; 101: 456-461
        • Robbins T.W.
        • Fray P.J.
        Stress-induced eating: Fact, fiction or misunderstanding?.
        Appetite. 1980; 1: 103-133
        • Robbins T.W.
        • Everitt B.J.
        • Sahakian B.J.
        Stress-induced eating in animals.
        in: Cioffi L.A. James W.P.T. Van Etallie T.B. The Body Weight Regulatory System: Normal and Disturbed Mechanisms. Raven, New York, NY1981: 289-297
        • Bradley P.J.
        Conditions recalled to have been associated with weight gain in adulthood.
        Appetite. 1985; 6: 235-241
        • Sternberg B
        Relapse in weight control: definitions, processes, and prevention strategies.
        in: Marlatt G.A. Gordon J.R. Relapse Prevention: Maintenance Strategies in the Treatment of Addictive Behaviors. Guilford, New York, NY1985: 521-545
        • Lipinski B.G.
        Life change events as correlates of weight gain.
        in: Howard A Recent Advances in Obesity Research: I. Proceedings of the First International Congress on Obesity. Newman, London, England1975: 210-212
        • Rookus M.A.
        • Burema J
        • Frijters J.E.R.
        Changes in body mass index in young adults in relation to number of life events experienced.
        Int J Obes. 1988; 12: 29-39
        • White W.B.
        Utilizing ambulatory blood pressure recordings to evaluate antihypertensive drug therapy.
        Am J Cardiol. 1992; 69: 8E-12E
        • Morris J.K.
        • Cook D.G.
        • Shaper A.G.
        Non-employment and changes in smoking, drinking, and body weight.
        BMJ. 1992; 304: 536-541
        • Conway T.L.
        • Vickers Jr., R.R.
        • Ward H.W.
        • et al.
        Occupational stress and variation in cigarette, coffee, and alcohol consumption.
        J Health Soc Behav. 1981; 22: 155-165
        • Craig W.Y.
        • Palomaki G.E.
        • Haddow J.E.
        Cigarette smoking and serum lipid and lipoprotein concentrations: An analysis of published data.
        BMJ. 1989; 298: 784-788
        • Dwyer J.H.
        • Rieger-Ndakorerwa G.E.
        • Semmer N.K.
        • et al.
        Low-level cigarette smoking and longitudinal change in serum cholesterol among adolescents. The Berlin-Bremen study.
        JAMA. 1988; 259: 2857-2862
        • Moffatt R.J.
        Effects of cessation of smoking on serum lipids and high density lipoprotein-cholesterol.
        Atherosclerosis. 1988; 74: 85-89
        • Stubbe I
        • Eskilsson J
        • Nilsson Ehle P
        High-density lipoprotein concentrations increase after stopping smoking.
        Br Med J (Clin Res Ed). 1982; 284: 1511-1513
        • Brischetto C.S.
        • Connor W.E.
        • Connor S.L.
        • et al.
        Plasma lipid and lipoprotein profiles of cigarette smokers from randomly selected families: Enhancement of hyperlipidemia and depression of high-density lipoprotein.
        Am J Cardiol. 1983; 52: 675-680
        • Mjos O.D.
        • Tromso M.D.
        Lipid effects of smoking.
        Am Heart J. 1988; 115: 272-275
        • Barrett Connor E
        • Khaw K.T.
        Cigarette smoking and increased central adiposity.
        Ann Intern Med. 1989; 111: 783-787
        • Muscat J.E.
        • Harris R.E.
        • Haley N.J.
        • et al.
        Cigarette smoking and plasma cholesterol.
        Am Heart J. 1991; 121: 141-147
        • Shimokata H
        • Muller D.C.
        • Andres R
        Studies in the distribution of body fat. III. Effects of cigarette smoking.
        JAMA. 1989; 261: 1169-1173
        • Winternitz W.W.
        • Quillen D
        Acute hormonal response to cigarette smoking.
        J Clin Pharmacol. 1987; 17: 389-397
        • Kirschbaum C
        • Wust S
        • Strasburger C.J.
        ‘Normal’ cigarette smoking increases free cortisol in habitual smokers.
        Life Sci. 1992; 50: 435-442
        • Cohen S
        • Lichtenstein E
        Perceived stress, quitting smoking, and smoking relapse.
        Health Psychol. 1990; 9: 466-478
        • Scherwitz L.W.
        • Perkins L.L.
        • Chesney M.A.
        • et al.
        Hostility and health behaviors in young adults: The CARDIA study.
        Am J Epidemiol. 1992; 136: 136-145
        • Hietanen E
        Regulation of Serum Lipids by Physical Exercise. CRC, Boca Raton, FL1982
        • Wood P.D.
        • Stefanik M.L.
        Exercise, fitness, and atherosclerosis.
        in: Bouchard C Shepard R.J. Stephens T Exercise, Fitness, and Health: A Consensus of Current Knowledge. Human Kinetic Books, Champaign, IL1990: 409-423
        • Thompson P.D.
        • Cullinane E.M.
        • Sady S.P.
        • et al.
        Modest changes in high-density lipoprotein concentration and metabolism with prolonged exercise training.
        Circulation. 1988; 78: 25-34
        • Kantor MA
        • Cullinane EM
        • Sady SP
        • et al.
        Exercise acutely increases high density lipoprotein-cholesterol and lipoprotein lipase activity in trained and untrained men.
        Metabolism. 1987; 36: 188-192
        • Sady SP
        • Thompson PD
        • Cullinane EM
        • et al.
        Prolonged exercise augments plasma triglyceride clearance.
        JAMA. 1986; 256: 2552-2555
        • Jorgensen RS
        • Nash JK
        • Lasser NL
        • et al.
        Heart rate acceleration and its relationship to total serum cholesterol, triglycerides, and blood pressure reactivity in men with mild hypertension.
        Psychophysiology. 1988; 25: 39-44
        • Fredrikson M
        • Blumenthal JA
        Lipids, catecholamines, and cardiovascular responses to stress in patients recovering from myocardial infarction.
        J Cardiopulm Rehabil. 1988; 12: 513-517
        • Fredrikson M
        • Blumenthal JA
        Serum lipid levels and ambulatory blood pressure.
        J Ambulatory Monitor. 1990; 3: 113-118
        • Suarez EC
        • Williams Jr, RB
        • Kuhn CM
        • et al.
        Biobehavioral basis of coronary-prone behavior in middle-aged men. Part II: Serum cholesterol, the type A behavior pattern, and hostility as interactive modulators of physiological reactivity.
        Psychosom Med. 1991; 53: 528-537
        • Schwertner HA
        • Troxler RG
        • Uhl GS
        • et al.
        Relationship between cortisol and cholesterol in men with coronary artery disease and type A behavior.
        Arteriosclerosis. 1984; 4: 59-64
        • Friedman M
        • Byers SO
        • Rosenman RH
        Plasma ACTH and cortisol concentration of coronary-prone subjects.
        in: Proc Soc Exp Biol Med. 140. 1972: 681-684
        • Friedman M
        • Rosenman RH
        Association of specific overt behavior pattern with blood and cardiovascular findings.
        JAMA. 1959; 169: 1286-1296
        • Rosenman RH
        • Friedman M
        Association of specific behavior pattern in women with blood and cardiovascular findings.
        Circulation. 1961; 24: 1173-1184
        • Friedman M
        • Byers SO
        • Rosenman RH
        • et al.
        Coronaryprone individuals (type A behavior pattern): Some biochemical characteristics.
        JAMA. 1970; 212: 1030-1037
        • Cohen JB
        • Reed D
        The type A behavior pattern and coronary heart disease among Japanese men in Hawaii.
        J Behav Med. 1985; 8: 343-352
        • Howard JH
        • Cunningham DA
        • Rechnitzer PA
        Health patterns associated with type a behavior: A managerial population.
        J Hum Stress. 1976; 2: 24-31
        • Dujovne VF
        • Houston BK
        • Dujovne CA
        Type A behavior, anger expression, and plasma lipids levels: A preliminary study.
        Coronary Artery Dis. 1992; 3: 1171-1176
        • Hubert HB
        • Eaker ED
        • Garrison RJ
        • et al.
        Life-style correlates of risk factor change in young adults: An eight-year study of coronary heart disease risk factors in the Framingham offspring.
        Am J Epidemiol. 1987; 125 (erratum in Am J Epidemiol 126:559, 1987): 812-831
        • Rigotti NA
        • Stoto MA
        • Bierer MF
        • et al.
        Retail stores' compliance with a city no-smoking law.
        Am J Public Health. 1993; 83: 227-232
        • Lovallo WR
        • Pishkin V
        A psychophysiological comparison of type A and B men exposed to failure and uncontrolled noise.
        Psychophysiology. 1980; 17: 29-36
        • Lundberg U
        • Hedman M
        • Melin B
        • et al.
        Type A behavior in healthy males and females as related to physiological reactivity and blood lipids.
        Psychosom Med. 1989; 51: 113-122
        • Orth-Gomer K
        • Unden AL
        Type A behavior, social support, and coronary risk: Interaction and significance for mortality in cardiac patients.
        Psychosom Med. 1990; 52: 59-72
        • Shekelle RB
        • Schoenberger JA
        • Stamler J
        Correlates of the JAS type A behavior pattern score.
        J Chron Dis. 1976; 29: 381-394
        • Sprafka JM
        • Folsom AR
        • Burke GL
        • et al.
        Type A behavior and its association with cardiovascular disease prevalence in blacks and whites: The Minnesota Heart Survey.
        J Behav Med. 1990; 13: 1-13
        • van Doornen LPJ
        The coronary risk personality: Psychological and psychophysiological aspects.
        Psychother Psychosom. 1980; 34: 204-215
        • Watkins PL
        • Fisher EB
        • Southard DR
        • et al.
        Assessing the relationship of type a beliefs to cardiovascular disease risk and psychosocial distress.
        J Psychopath Behav Assess. 1989; 11: 113-125
        • Chesney MA
        • Sevelius G
        • Black GW
        • et al.
        Work environment, type A behavior, and coronary heart disease risk factors.
        J Occup Med. 1981; 23: 551-555
        • Eaker ED
        • Abbott RD
        • Kannel WB
        Frequency of uncomplicated angina pectoris in type A compared with type B persons (the Framingham Study).
        Am J Cardiol. 1989; 63: 1042-1045
        • Friedman EH
        • Hellerstein HK
        • Easiwood GL
        • et al.
        Behavior patterns and serum cholesterol in two groups of normal males.
        Am J Med Sci. 1968; 255: 237-244
        • Gallacher JE
        • Yarnell JW
        • Butland BK
        Type A behaviour and prevalent heart disease in the Caerphilly study: Increase in risk or symptom reporting?.
        J Epidemiol Commun Health. 1988; 42: 226-231
        • Garrity TF
        • Kotchen JM
        • McKean HE
        • et al.
        The association between type A behavior and change in coronary risk factors among young adults.
        Am J Public Health. 1990; 80: 1354-1357
        • Hendrix WH
        • Ovalle NK
        • Troxler R
        Behavioral and physiological consequences of stress and its antecedent factors.
        J Appl Psychol. 1985; 70: 188-201
        • Keith RA
        • Lown B
        • Stare FJ
        Coronary heart disease and behavior patterns.
        Psychosom Med. 1965; 27: 424-434
        • Kornitzer M
        • Dramaix M
        • DeBacker G
        • et al.
        The Belgian multifactor preventive trial in CVD (II): Cholesterolemia and psycho-socio-biological variables.
        Heart Bull. 1977; 8: 147-154
        • van Doornen LJ
        • van Blokland RW
        The relation of type A behavior and vital exhaustion with physiological reactions to real life stress.
        J Psychosom Res. 1989; 33: 715-725
        • Harlan W
        • Oberman A
        • Mitchell R
        • et al.
        Constitutional and environmental factors related to serum lipid and lipoprotein levels.
        Ann Intern Med. 1967; 66: 540-555
        • Jenkins CD
        • Hames CG
        • Zyzanski SJ
        • et al.
        Psychological traits and serum lipids.
        Psychosom Med. 1969; 31: 115-128
        • Cook WW
        • Medley DM
        Proposed hostility and pharisaic-virtue scores for the MMPI.
        J Appl Psychol. 1954; 38: 414-418
        • Smith TW
        • Allred KD
        Blood-pressure responses during social interaction in high- and low-cynically hostile males.
        J Behav Med. 1989; 12: 135-143
        • Suarez EC
        • Williams RBJ
        Situational determinants of cardiovascular and emotional reactivity in high and low hostile men.
        Psychosom Med. 1989; 51: 404-418
        • Weidner G
        • Sexton G
        • McLellarn R
        • et al.
        The role of type A behavior and hostility in an elevation of plasma lipids in adult women and men.
        Psychosom Med. 1987; 49: 136-145
        • Dujovne VF
        • Houston BK
        Hostility-related variables and plasma lipid levels.
        J Behav Med. 1991; 14: 555-565
        • Suarez EC
        • Harlan E
        • Tyrey M
        The relationship between anger expression and serum lipids in women.
        Ann Behav Med. 1993; 15 (suppl, abstr): S79
        • Spielberger CD
        • Johnson E
        • Russell S
        • et al.
        The experience and expression of anger: construction and validation of an anger expression scale.
        in: Chesney MA Rosenman RH Anger and Hostility in Cardiovascular and Behavioral Disorders. Hemisphere Publishing, Washington, DC1985: 5-30
        • Engebretson TO
        • Stoney CM
        Cynical hostility and anger expression: Relationships to plasma lipid concentrations.
        Psychosom Med. 1993; 55 (abstr): 121-122
        • van Doornen LJ
        • van Blokland R
        Serum-cholesterol: Sex specific psychological correlates during rest and stress.
        J Psychosom Res. 1987; 31: 239-249
        • Lundberg U
        • Fredrikson M
        • Wallin L
        • et al.
        Blood lipids as related to cardiovascular and neuroendocrine functions under different conditions in healthy males and females.
        Pharmacol Biochem Behav. 1989; 33: 381-386
        • Istvan J
        • Zavela K
        • Weidner G
        Body weight and psychological distress in NHANES I.
        Int J Obes. 1992; 16: 999-1003
        • Van Strien T
        • Rookus MA
        • Bergers GPA
        • et al.
        Life events, emotional eating and change in body mass index.
        Int J Obes. 1986; 10: 29-35
        • Oscarsson J
        • Olofsson SO
        • Bondjers G
        • et al.
        Differential effects of continuous versus intermittent administration of growth hormone to hypophysectomized female rats on serum lipoproteins and their apoproteins.
        Endocrinology. 1989; 125: 1638-1649
        • Shively CA
        • Knox SS
        • Sherwin BB
        • et al.
        Sex steroids, psychosocial factors, and lipid metabolism.
        Metabolism. 1993; 42: 16-24
        • Hülsmann WC
        Abnormal stress eractions after feeding diets rich in (very) long-chain fatty acids: high levels of corticosterone and testosterone.
        Mol Cel Endocrinol. 1978; 12: 1-8
        • Yagamuchi K
        • Goko H
        • Takashima S
        • et al.
        Abnormalities of insulin secretory and lipolytic response to epinephrine produced by a high fat diet and electric stress in rats.
        Endokrinologie. 1981; 78: 253-261
        • Brindley DN
        • Cooling J
        • Glenny HP
        • et al.
        Effects of chronic modification of dietary fat and carbohydrate on the insulin, corticosterone and metabolic responses of rats fed acutely with glucose, fructose or ethanol.
        Biochem J. 1981; 200: 275-283
        • Tannenbaum BM
        • Brindley DN
        • Dallman MF
        • et al.
        Hypothalamic-pituitary dysregulation associated with a high fat diet.
        in: Society for Neuroscience Annual Meeting. 2. 1992: 1540 (abstr)
        • Brindley DN
        • Saxton J
        • Shahidullah H
        • et al.
        Possible relationships between changes in body weight set-point and stress metabolism after treating rats chronically with d-fenfluramine. Effects of feeding rats acutely with fructose on the metabolism of corticosterone, glucose, fatty acids, glycerol and triacylglycerol.
        Biochem Pharmacol. 1985; 34: 1265-1271
        • Brindley DN
        • Akester H
        • Derrick GP
        • et al.
        Effects of chronic administration of benfluorex to rats on the metabolism of corticosterone, glucose, triacylglycerols, glycerol and fatty acid.
        Biochem Pharmacol. 1988; 37: 695-705
        • Sessions VA
        • Martin A
        • Gomez-Muñoz A
        • et al.
        Cholesterol feeding induces hypertriglyceridemia in hamsters and increases the activity of the Mg2+-dependent phosphatidate phosphohydrolase in the liver.
        Biochim Biophys Acta. 1993; 1166: 238-263
        • Frayn KN
        • Coppack SW
        Insulin resistance, adipose tissue and coronary heart disease.
        Clin Sci. 1992; 82 (editorial): 1-8
        • Rippey RM
        Overview: seasonal variations in cholesterol.
        Prev Med. 1981; 10: 655-659
        • Gordon DJ
        • Hyde J
        • Trost DC
        • et al.
        Cyclic seasonal variation in plasma lipid and lipoprotein levels: The Lipid Research Clinics Coronary Primary Prevention Trial Placebo group.
        J Clin Epidemiol. 1988; 41: 679-689
        • Robinson D
        • Bevan EA
        • Hinohara S
        • et al.
        Seasonal variation in serum cholesterol levels—Evidence from the UK and Japan.
        Atherosclerosis. 1992; 95: 15-24
        • Fager G
        • Wiklund O
        • Olofsson S-O
        • et al.
        Seasonal variations in serum lipid and apolipoprotein levels evaluated by periodic regression analysis.
        J Chron Dis. 1982; 35: 643-648
        • Davignon J
        • Gregg RE
        • Sing CF
        Apolipoprotein E polymorphism and atherosclerosis.
        Arteriosclerosis. 1988; 8: 1-21
        • Soria LF
        • Ludwig EH
        • Clarke HR
        • et al.
        Association between a specific apolipoprotein B mutation and familial defective apolipoprotein B-100.
        in: Proc Natl Acad Sci USA. 86. 1989: 587-591
        • Young SG
        • Linton MF
        Genetic abnormalities in apolipoprotein B.
        Trends Cardiovasc Med. 1991; 1: 59-65
        • Utermann G
        The mysteries of lipoprotein(a).
        Science. 1989; 246: 904-910
        • McCranie EW
        • Simpson ME
        • Stevens JS
        Type A behavior, field dependence, and serum lipids.
        Psychosom Med. 1981; 43: 107-116
        • Salter AM
        • Hayashi R
        • al Seeni M
        • et al.
        Effects of hypothyroidism and high-fat feeding on mRNA concentrations for the low-density-lipoprotein receptor and on acyl-CoA:cholesterol acyltransferase activities in rat liver.
        Biochem J. 1991; 276: 825-832
        • Spady DK
        • Turley SD
        • Dietschy JM
        Rates of low density lipoprotein uptake and cholesterol synthesis are regulated independently in the liver.
        J Lipid Res. 1985; 26: 465-472
        • Steinberg D
        • Witztum JL
        Lipoproteins and atherogenesis. Current concepts.
        JAMA. 1990; 264: 3047-3052
        • Muller JE
        • Tofler GH
        Introduction (symposium review).
        in: Am J Cardiol. 6. 1990: 1G-6G
        • Kaplan JR
        • Manuck SB
        • Adams MR
        Plaque changes and arterial enlargement in atherosclerotic monkeys after manipulation of diet and social environment.
        Arterioscler Thromb. 1993; 26: 151-162
        • Troxler RG
        • Sprague EA
        • Albanese RA
        • et al.
        The association of elevated plasma cortisol and early atherosclerosis as demonstrated by coronary angiography.
        Atherosclerosis. 1977; 26: 151-162
        • Haynes SG
        • Feinlieb M
        • Kannel WB
        The relationship of psychological factors to coronary heart disease in the Framingham Study: III. Eight-year incidence of coronary heart disease.
        Am J Epidemiol. 1980; 111: 37-58
      2. McEwen BS, Stellar E: Stress and the individual: Mechanisms leading to disease. Arch Intern Med (in press)