Metabolic syndrome: links to social stress and socioeconomic status

Socioeconomic stress associated with financial and psychosocial stress is widespread in society. A comprehensive body of research indicates that low socioeconomic status and social stress is associated with a broad spectrum of health risks. This paper reviews epidemiological evidence demonstrating the association between chronic social stress and development of obesity and symptoms leading to metabolic syndrome. The cumulative effects of socioeconomic stress on health and well being are evident throughout the lifespan, affecting children, adolescents, and adults. While the links between stress and metabolic disease are documented, the mechanisms remain less well understood. Animal models are well established and have provided opportunities to systematically investigate contributing mechanisms that may be targeted to develop treatment and prevention strategies against metabolic disorders arising from exposure to chronic social stress.

[1]  H. Simon,et al.  Prenatal Stress Increases the Hypothalamo‐Pituitary‐Adrenal Axis Response in Young and Adult Rats , 1994, Journal of neuroendocrinology.

[2]  P. Bossuyt,et al.  The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-gamma2 gene on glucose/insulin metabolism interact with prenatal exposure to famine. , 2006, Diabetes care.

[3]  T. Bale,et al.  Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity , 2006, Physiology & Behavior.

[4]  M. Solomon,et al.  Social defeat and footshock increase body mass and adiposity in male Syrian hamsters. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[5]  G. Elmer,et al.  Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia , 2005, Behavioural Brain Research.

[6]  F. Frey,et al.  Epigenetic regulation of 11β-hydroxysteroid dehydrogenase type 2 expression , 2004 .

[7]  J. Seckl.  Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms , 2001, Molecular and Cellular Endocrinology.

[8]  R. Sakai,et al.  Androgenic influences on behavior, body weight, and body composition in a model of chronic social stress. , 2007, Endocrinology.

[9]  S. Woods,et al.  Social stress and recovery: implications for body weight and body composition. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[10]  P. Plotsky,et al.  Chronic maternal stress inhibits the capacity to up-regulate placental 11beta-hydroxysteroid dehydrogenase type 2 activity. , 2005, The Journal of endocrinology.

[11]  E Susser,et al.  Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. , 1999, JAMA.

[12]  P. Gluckman,et al.  Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life , 2008, BJOG : an international journal of obstetrics and gynaecology.

[13]  T. Bale,et al.  Sex-specificity in transgenerational epigenetic programming , 2011, Hormones and Behavior.

[14]  C. Russell,et al.  Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men. , 1993, The Journal of clinical investigation.

[15]  T. Moran,et al.  Prenatal Stress or High-Fat Diet Increases Susceptibility to Diet-Induced Obesity in Rat Offspring , 2009, Diabetes.

[16]  J. Seckl,et al.  Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 b -hydroxysteroid dehydrogenase inhibitor carbenoxolone , 1996, Diabetologia.

[17]  J. A. Markham,et al.  Prenatal stress: Role in psychotic and depressive diseases , 2011, Psychopharmacology.

[18]  F. Frey,et al.  Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression. , 2004, The Journal of clinical investigation.

[19]  D. Blanchard,et al.  Behavioral correlates of chronic dominance-subordination relationships of male rats in a seminatural situation , 1990, Neuroscience & Biobehavioral Reviews.

[20]  N. Kalin,et al.  PROLONGED STRESS-INDUCED ELEVATION IN PLASMA CORTICOSTERONE DURING PREGNANCY IN THE RAT: IMPLICATIONS FOR PRENATAL STRESS STUDIES , 1998, Psychoneuroendocrinology.

[21]  E. Susser,et al.  Schizophrenia after prenatal famine. Further evidence. , 1996, Archives of general psychiatry.

[22]  Christina Thaller,et al.  Enhanced anxiety and stress-induced corticosterone release are associated with increased Crh expression in a mouse model of Rett syndrome , 2006, Proceedings of the National Academy of Sciences.

[23]  K. Shiota,et al.  Expression of the peroxisome proliferator activated receptor γ gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes , 2009, BMC Biology.

[24]  V. Willour,et al.  Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. , 2010, Endocrinology.

[25]  T. Bale,et al.  Maternal high-fat diet effects on third-generation female body size via the paternal lineage. , 2011, Endocrinology.

[26]  C. Shively,et al.  Regional obesity and coronary artery atherosclerosis in females: a non-human primate model. , 2009, Acta medica Scandinavica. Supplementum.

[27]  A. Convit,et al.  Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes , 2007, Diabetologia.

[28]  T. Bale,et al.  Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy , 2008, The Journal of Neuroscience.

[29]  M. Nyirenda,et al.  Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. , 1998, The Journal of clinical investigation.

[30]  S. Woods,et al.  Dynamic body weight and body composition changes in response to subordination stress , 2007, Physiology & Behavior.

[31]  S. Ozanne,et al.  Early programming of glucose–insulin metabolism , 2002, Trends in Endocrinology & Metabolism.

[32]  Robert L. Spencer,et al.  Visible burrow system as a model of chronic social stress: Behavioral and neuroendocrine correlates , 1995, Psychoneuroendocrinology.

[33]  S. Woods,et al.  Metabolic and endocrine consequences of social stress in a visible burrow system , 2004, Physiology & Behavior.

[34]  C. Shively,et al.  The unique value of primate models in translational research , 2009, American journal of primatology.

[35]  E. Finkelstein,et al.  Annual medical spending attributable to obesity: payer-and service-specific estimates. , 2009, Health affairs.

[36]  M A Hanson,et al.  Animal models and programming of the metabolic syndrome. , 2001, British medical bulletin.

[37]  E. Krause,et al.  Dominant rats are natural risk takers and display increased motivation for food reward , 2009, Neuroscience.

[38]  R. Sakai,et al.  Social stress: From rodents to primates , 2005, Frontiers in Neuroendocrinology.

[39]  Shelley E. Taylor,et al.  Relationship of Early Life Stress and Psychological Functioning to Adult C-Reactive Protein in the Coronary Artery Risk Development in Young Adults Study , 2006, Biological Psychiatry.

[40]  F. Milagro,et al.  High fat diet-induced obesity modifies the methylation pattern of leptin promoter in rats , 2009, Journal of Physiology and Biochemistry.

[41]  R. Stöger.  Epigenetics and obesity. , 2008, Pharmacogenomics.

[42]  J. Kral,et al.  Early-Life Stress and the Development of Obesity and Insulin Resistance in Juvenile Bonnet Macaques , 2007, Diabetes.

[43]  M. Hanson,et al.  Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. , 2005, The Journal of nutrition.

[44]  D. Pfaff,et al.  Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. , 2010, Endocrinology.

[45]  E. Susser,et al.  Increased Risk of Affective Disorders in Males after Second Trimester Prenatal Exposure to the Dutch Hunger Winter of 1944–45 , 1995, British Journal of Psychiatry.

[46]  W. Yeaton,et al.  Young Children's Weight Trajectories and Associated Risk Factors: Results from the Early Childhood Longitudinal Study–Birth Cohort , 2011, American journal of health promotion : AJHP.

[47]  E. Sijbrands,et al.  Genetic Variant in the IGF2BP2 Gene May Interact With Fetal Malnutrition to Affect Glucose Metabolism , 2009, Diabetes.

[48]  Childhood obesity in the United States , 2011, AAP News.

[49]  D. Laber,et al.  11 { beta }-hydroxysteroid dehydrogenase type 1 regulates glucocorticoid-induced insulin resistance in skeletal muscle , 2011 .

[50]  Michael J Meaney,et al.  Epigenetic programming by maternal behavior , 2004, Nature Neuroscience.

[51]  P. Bossuyt,et al.  The metabolic syndrome in adults prenatally exposed to the Dutch famine. , 2007, The American journal of clinical nutrition.

[52]  Tarani Chandola,et al.  Chronic stress at work and the metabolic syndrome: prospective study , 2006, BMJ : British Medical Journal.

[53]  J. Seckl,et al.  Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. , 1996, Neuroendocrinology.

[54]  Ian Janssen,et al.  Vascular Risks and Management of Obesity in Children and Adolescents , 2006, Vascular health and risk management.

[55]  A. Russell,et al.  Redistribution of glucose from skeletal muscle to adipose tissue during catch-up fat: a link between catch-up growth and later metabolic syndrome. , 2005, Diabetes.

[56]  R. Gitau,et al.  Fetal exposure to maternal cortisol , 1998, The Lancet.

[57]  P. Björntorp.  Adipose tissue distribution and function. , 1991, International journal of obesity.

[58]  B. Rolls,et al.  Changes in Food Intake in Response to Stress in Men and Women: Psychological Factors , 1997, Appetite.

[59]  R. Sakai,et al.  Chronic social stress in a changing dietary environment , 2006, Physiology & Behavior.

[60]  J. Tepperman,et al.  Meal frequency--a possible factor in human pathology. , 1970, The American journal of clinical nutrition.

[61]  F. Milagro,et al.  Individuality and epigenetics in obesity , 2009, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[62]  K. S. Vimaleswaran,et al.  Progress in the genetics of common obesity and type 2 diabetes , 2010, Expert Reviews in Molecular Medicine.

[63]  M. Le Moal,et al.  Prenatal Stress Induces High Anxiety and Postnatal Handling Induces Low Anxiety in Adult Offspring: Correlation with Stress-Induced Corticosterone Secretion , 1997, The Journal of Neuroscience.

[64]  Shelley E. Taylor,et al.  Relation of Childhood Socioeconomic Status and Family Environment to Adult Metabolic Functioning in the CARDIA Study , 2005, Psychosomatic medicine.

[65]  M. Hetherington,et al.  Emotions and eating. Self-reported and experimentally induced changes in food intake under stress , 2009, Appetite.

[66]  K. Flegal,et al.  Prevalence of overweight and obesity in the United States, 1999-2004. , 2006, JAMA.

[67]  B. A. Ardekani,et al.  Preliminary evidence for brain complications in obese adolescents with type 2 diabetes mellitus , 2010, Diabetologia.

[68]  A. Convit,et al.  Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[69]  M. Solomon,et al.  Social defeat increases food intake, body mass, and adiposity in Syrian hamsters. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[70]  J. van Os.  Schizophrenia after prenatal famine. , 1997, Archives of general psychiatry.

[71]  S. Woods,et al.  Meal patterns and hypothalamic NPY expression during chronic social stress and recovery. , 2010, American journal of physiology. Regulatory, integrative and comparative physiology.

[72]  L. Gathercole,et al.  Glucocorticoid modulation of insulin signaling in human subcutaneous adipose tissue. , 2007, The Journal of clinical endocrinology and metabolism.

[73]  M. Wabitsch,et al.  Leptin Gene Expression in Human Preadipocytes Is Switched on by Maturation-induced Demethylation of Distinct CpGs in Its Proximal Promoter* , 2002, The Journal of Biological Chemistry.

[74]  R. Rosmond.  Role of stress in the pathogenesis of the metabolic syndrome , 2005, Psychoneuroendocrinology.

[75]  Jason U Tilan,et al.  Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome , 2007, Nature Medicine.

[76]  J. Newell-Price,et al.  The CpG island promoter of the human proopiomelanocortin gene is methylated in nonexpressing normal tissue and tumors and represses expression. , 2001, Molecular endocrinology.

[77]  T. Onaya,et al.  DNA demethylation during the differentiation of 3T3-L1 cells affects the expression of the mouse GLUT4 gene. , 1999, Diabetes.