Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-13T01:55:34.379Z Has data issue: false hasContentIssue false
  • English
  • Français

Relationship between adiposity, emotional status and eating behaviour in obese women: role of inflammation

Published online by Cambridge University Press:  20 October 2010

L. Capuron ,
C. Poitou ,
D. Machaux-Tholliez ,
V. Frochot ,
J.-L. Bouillot ,
A. Basdevant ,
S. Layé  and
K. Clément
L. Capuron*
Affiliation:
Laboratory of Psychoneuroimmunology, Nutrition and Genetics (PSYNUGEN), University Victor Segalen Bordeaux 2, INRA 1286, CNRS 5226, 146 rue Léo Saignat, Bordeaux, F-33076 France
C. Poitou
Affiliation:
Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Nutrition and Endocrinology Department, CRNH-Ile de France, Paris, F-75013 France INSERM, U872, Nutriomique team 7, Paris, F-75006 France; Université Pierre et Marie Curie-Paris 6, Centre de Recherche des Cordeliers, UMR S 872, Paris, F-75006 France; Université Paris Descartes, UMR S 872, Paris, F-75006 France
D. Machaux-Tholliez
Affiliation:
Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Nutrition and Endocrinology Department, CRNH-Ile de France, Paris, F-75013 France
V. Frochot
Affiliation:
Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Endocrinology and Oncology Biochemistry Department, Paris, F-75013 France
J.-L. Bouillot
Affiliation:
Assistance Publique-Hôpitaux de Paris, Hotel-Dieu Hospital, Surgery Department, Paris, F-75013 France
A. Basdevant
Affiliation:
Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Nutrition and Endocrinology Department, CRNH-Ile de France, Paris, F-75013 France INSERM, U872, Nutriomique team 7, Paris, F-75006 France; Université Pierre et Marie Curie-Paris 6, Centre de Recherche des Cordeliers, UMR S 872, Paris, F-75006 France; Université Paris Descartes, UMR S 872, Paris, F-75006 France
S. Layé
Affiliation:
Laboratory of Psychoneuroimmunology, Nutrition and Genetics (PSYNUGEN), University Victor Segalen Bordeaux 2, INRA 1286, CNRS 5226, 146 rue Léo Saignat, Bordeaux, F-33076 France
K. Clément
Affiliation:
Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Nutrition and Endocrinology Department, CRNH-Ile de France, Paris, F-75013 France INSERM, U872, Nutriomique team 7, Paris, F-75006 France; Université Pierre et Marie Curie-Paris 6, Centre de Recherche des Cordeliers, UMR S 872, Paris, F-75006 France; Université Paris Descartes, UMR S 872, Paris, F-75006 France
*
*Address for correspondence: L. Capuron, Ph.D., Laboratory of Psychoneuroimmunology, Nutrition and Genetics (PSYNUGEN), University Victor Segalen Bordeaux 2, INRA 1286, CNRS 5226, 146 rue Léo Saignat, Bordeaux, F-33076 France. (Email: lucile.capuron@bordeaux.inra.fr)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Obesity is characterized by chronic low-grade inflammation that may lead to emotional distress and behavioural symptoms. This study assessed the relationship between adiposity, low-grade inflammation, eating behaviour and emotional status in obese women awaiting gastric surgery and investigated the effects of surgery-induced weight loss on this relationship.

Method

A total of 101 women with severe or morbid obesity awaiting gastric surgery were recruited. Assessments were performed before and at 1 year post-surgery and included the measurement of neuroticism and extraversion using the revised Neuroticism–Extraversion–Openness personality inventory (NEO-PI-R) and eating behaviour using the Three-Factor Eating Questionnaire (TFEQ). Blood samples were collected for the measurement of serum inflammatory markers [interleukin-6 (IL-6), high-sensitive C-reactive protein (hsCRP)] and adipokines (leptin, adiponectin).

Results

At baseline, body mass index (BMI) was positively correlated with inflammatory markers and adipokines. Regression analyses adjusting for age and diabetes revealed that baseline concentrations of IL-6 and hsCRP were associated with the depression and anxiety facets of neuroticism, with higher inflammation predicting higher anxiety and depression. This association remained significant after adjusting for BMI. Gastric surgery induced significant weight loss, which correlated with reduced inflammation. After controlling for BMI variations, decreases in inflammatory markers, notably hsCRP, were associated with reduced anxiety and TFEQ-cognitive restraint scores.

Conclusions

These findings indicate strong associations between adiposity, inflammation and affectivity in obese subjects and show that surgery-induced weight loss is associated concomitantly with reduced inflammation and adipokines and with significant improvement in emotional status and eating behaviour. Inflammatory status appears to represent an important mediator of emotional distress and psychological characteristics of obese individuals.

Keywords

Eating behaviourinflammationneuroticismobesitypsychological characteristicsweight loss
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 7 , July 2011 , pp. 1517 - 1528
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bankier, B, Barajas, J, Martinez-Rumayor, A, Januzzi, JL (2008). Association between C-reactive protein and generalized anxiety disorder in stable coronary heart disease patients. European Heart Journal 29, 2212–2217.CrossRefGoogle ScholarPubMed
Baron, RM, Kenny, DA (1986). The moderator–mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology 51, 1173–1182.CrossRefGoogle ScholarPubMed
Bastard, JP, Jardel, C, Bruckert, E, Blondy, P, Capeau, J, Laville, M, Vidal, H, Hainque, B (2000). Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. Journal of Clinical Endocrinology and Metabolism 85, 3338–3342.Google ScholarPubMed
Bastard, JP, Jardel, C, Delattre, J, Hainque, B, Bruckert, E, Oberlin, F (1999). Evidence for a link between adipose tissue interleukin-6 content and serum C-reactive protein concentrations in obese subjects. Circulation 99, 2221–2222.CrossRefGoogle ScholarPubMed
Bastard, JP, Maachi, M, Lagathu, C, Kim, MJ, Caron, M, Vidal, H, Capeau, J, Feve, B (2006). Recent advances in the relationship between obesity, inflammation, and insulin resistance. European Cytokine Network 17, 4–12.Google ScholarPubMed
Bean, MK, Stewart, K, Olbrisch, ME (2008). Obesity in America: implications for clinical and health psychologists. Journal of Clinical Psychology in Medical Settings 15, 214–224.CrossRefGoogle ScholarPubMed
Bellisle, F, Clement, K, Le Barzic, M, Le Gall, A, Guy-Grand, B, Basdevant, A (2004). The Eating Inventory and body adiposity from leanness to massive obesity: a study of 2509 adults. Obesity Research 12, 2023–2030.CrossRefGoogle ScholarPubMed
Cancello, R, Clement, K (2006). Is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue. British Journal of Obstetrics and Gynaecology 113, 1141–1147.CrossRefGoogle ScholarPubMed
Cancello, R, Henegar, C, Viguerie, N, Taleb, S, Poitou, C, Rouault, C, Coupaye, M, Pelloux, V, Hugol, D, Bouillot, JL, Bouloumie, A, Barbatelli, G, Cinti, S, Svensson, PA, Barsh, GS, Zucker, JD, Basdevant, A, Langin, D, Clement, K (2005). Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 54, 2277–2286.CrossRefGoogle ScholarPubMed
Canetti, L, Berry, EM, Elizur, Y (2009). Psychosocial predictors of weight loss and psychological adjustment following bariatric surgery and a weight-loss program: the mediating role of emotional eating. International Journal of Eating Disorders 42, 109–117.CrossRefGoogle Scholar
Capuron, L, Bluthe, RM, Dantzer, R (2001). Cytokines in clinical psychiatry. American Journal of Psychiatry 158, 1163–1164.CrossRefGoogle ScholarPubMed
Capuron, L, Gumnick, JF, Musselman, DL, Lawson, DH, Reemsnyder, A, Nemeroff, CB, Miller, AH (2002). Neurobehavioral effects of interferon-α in cancer patients: phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology 26, 643–652.CrossRefGoogle ScholarPubMed
Capuron, L, Miller, AH (2004). Cytokines and psychopathology: lessons from interferon-α. Biological Psychiatry 56, 819–824.CrossRefGoogle ScholarPubMed
Capuron, L, Pagnoni, G, Demetrashvili, M, Woolwine, BJ, Nemeroff, CB, Berns, GS, Miller, AH (2005). Anterior cingulate activation and error processing during interferon-α treatment. Biological Psychiatry 58, 190–196.CrossRefGoogle ScholarPubMed
Capuron, L, Su, S, Miller, AH, Bremner, JD, Goldberg, J, Vogt, GJ, Maisano, C, Jones, L, Murrah, NV, Vaccarino, V (2008). Depressive symptoms and metabolic syndrome: is inflammation the underlying link? Biological Psychiatry 64, 896–900.CrossRefGoogle ScholarPubMed
Charles, SC (1987). Psychiatric evaluation of morbidly obese patients. Gastroenterology Clinics of North America 16, 415–432.CrossRefGoogle ScholarPubMed
Clement, K, Viguerie, N, Poitou, C, Carette, C, Pelloux, V, Curat, CA, Sicard, A, Rome, S, Benis, A, Zucker, JD, Vidal, H, Laville, M, Barsh, GS, Basdevant, A, Stich, V, Cancello, R, Langin, D (2004). Weight loss regulates inflammation-related genes in white adipose tissue of obese subjects. FASEB Journal 18, 1657–1669.CrossRefGoogle ScholarPubMed
Costa, P Jr., McCrae, R (1998). NEO-PI-R Inventaire de Personnalité-Revisé [NEO-PI-R Personality Inventory – Revised]. French adaptation (ed. Rolland, J. P.). Les Editions du Centre de Psychologie Appliquée: Paris.Google Scholar
Costa, PT, McCrae, RR (1985). The NEO Personality Inventory Manual. Psychological Assessment Resources, Inc.: Odessa, FL.Google Scholar
Dantzer, R, Wollman, EE, Yirmiya, R (1999). Cytokines, Stress and Depression. Kluwer Academic: New York.CrossRefGoogle ScholarPubMed
de Zwaan, M, Mitchell, JE, Howell, LM, Monson, N, Swan-Kremeier, L, Crosby, RD, Seim, HC (2003). Characteristics of morbidly obese patients before gastric bypass surgery. Comprehensive Psychiatry 44, 428–434.CrossRefGoogle ScholarPubMed
Dixon, JB, Dixon, ME, O'Brien, PE (2003). Depression in association with severe obesity: changes with weight loss. Archives of Internal Medicine 163, 2058–2065.CrossRefGoogle ScholarPubMed
Evans, DL, Charney, DS, Lewis, L, Golden, RN, Gorman, JM, Krishnan, KR, Nemeroff, CB, Bremner, JD, Carney, RM, Coyne, JC, Delong, MR, Frasure-Smith, N, Glassman, AH, Gold, PW, Grant, I, Gwyther, L, Ironson, G, Johnson, RL, Kanner, AM, Katon, WJ, Kaufmann, PG, Keefe, FJ, Ketter, T, Laughren, TP, Leserman, J, Lyketsos, CG, McDonald, WM, McEwen, BS, Miller, AH, Musselman, D, O'Connor, C, Petitto, JM, Pollock, BG, Robinson, RG, Roose, SP, Rowland, J, Sheline, Y, Sheps, DS, Simon, G, Spiegel, D, Stunkard, A, Sunderland, T, Tibbits, P Jr., Valvo, WJ (2005). Mood disorders in the medically ill: scientific review and recommendations. Biological Psychiatry 58, 175–189.CrossRefGoogle Scholar
Faith, MS, Flint, J, Fairburn, CG, Goodwin, GM, Allison, DB (2001). Gender differences in the relationship between personality dimensions and relative body weight. Obesity Research 9, 647–650.CrossRefGoogle ScholarPubMed
Forsythe, LK, Wallace, JM, Livingstone, MB (2008). Obesity and inflammation: the effects of weight loss. Nutrition Research Reviews 21, 117–133.CrossRefGoogle ScholarPubMed
Gibson, EL (2006). Emotional influences on food choice: sensory, physiological and psychological pathways. Physiology and Behavior 89, 53–61.CrossRefGoogle ScholarPubMed
Herva, A, Laitinen, J, Miettunen, J, Veijola, J, Karvonen, JT, Laksy, K, Joukamaa, M (2006). Obesity and depression: results from the longitudinal Northern Finland 1966 Birth Cohort Study. International Journal of Obesity 30, 520–527.CrossRefGoogle ScholarPubMed
Hsu, LK, Mulliken, B, McDonagh, B, Krupa Das, S, Rand, W, Fairburn, CG, Rolls, B, McCrory, MA, Saltzman, E, Shikora, S, Dwyer, J, Roberts, S (2002). Binge eating disorder in extreme obesity. International Journal of Obesity and Related Metabolism Disorders 26, 1398–1403.CrossRefGoogle ScholarPubMed
Jylha, P, Isometsa, E (2006). The relationship of neuroticism and extraversion to symptoms of anxiety and depression in the general population. Depression and Anxiety 23, 281–289.CrossRefGoogle ScholarPubMed
Karlsson, J, Persson, LO, Sjostrom, L, Sullivan, M (2000). Psychometric properties and factor structure of the Three-Factor Eating Questionnaire (TFEQ) in obese men and women. Results from the Swedish Obese Subjects (SOS) study. International Journal of Obesity and Related Metabolism Disorders 24, 1715–1725.CrossRefGoogle ScholarPubMed
Katz, A, Nambi, SS, Mather, K, Baron, AD, Follmann, DA, Sullivan, G, Quon, MJ (2000). Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. Journal of Clinical Endocrinology and Metabolism 85, 2402–2410.CrossRefGoogle ScholarPubMed
Kendler, KS, Gardner, CO, Gatz, M, Pedersen, NL (2007). The sources of co-morbidity between major depression and generalized anxiety disorder in a Swedish national twin sample. Psychological Medicine 37, 453–462.CrossRefGoogle Scholar
Kendler, KS, Gatz, M, Gardner, CO, Pedersen, NL (2006). Personality and major depression: a Swedish longitudinal, population-based twin study. Archives of General Psychiatry 63, 1113–1120.CrossRefGoogle ScholarPubMed
Konsman, JP, Parnet, P, Dantzer, R (2002). Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neuroscience 25, 154–159.CrossRefGoogle ScholarPubMed
Lluch, A (1995). Identification of eating patterns by nutritional and psychometric approaches. Implications for the prevention and treatment of human obesity. Doctoral thesis, Université Henri Poincaré: Nancy, France.Google Scholar
Lykouras, L (2008). Psychological profile of obese patients. Digestive Diseases 26, 36–39.CrossRefGoogle ScholarPubMed
Musselman, DL, Lawson, DH, Gumnick, JF, Manatunga, AK, Penna, S, Goodkin, RS, Greiner, K, Nemeroff, CB, Miller, AH (2001). Paroxetine for the prevention of depression induced by high-dose interferon α. New England Journal of Medicine 344, 961–966.CrossRefGoogle Scholar
O'Rourke, RW (2009). Inflammation in obesity-related diseases. Surgery 145, 255–259.CrossRefGoogle ScholarPubMed
Plotkin, SR, Banks, WA, Kastin, AJ (1996). Comparison of saturable transport and extracellular pathways in the passage of interleukin-1 α across the blood–brain barrier. Journal of Neuroimmunology 67, 41–47.Google ScholarPubMed
Poitou, C, Coussieu, C, Rouault, C, Coupaye, M, Cancello, R, Bedel, JF, Gouillon, M, Bouillot, JL, Oppert, JM, Basdevant, A, Clement, K (2006). Serum amyloid A: a marker of adiposity-induced low-grade inflammation but not of metabolic status. Obesity (Silver Spring) 14, 309–318.CrossRefGoogle Scholar
Poitou, C, Divoux, A, Faty, A, Tordjman, J, Hugol, D, Aissat, A, Keophiphath, M, Henegar, C, Commans, S, Clement, K (2009). Role of serum amyloid α in adipocyte–macrophage cross talk and adipocyte cholesterol efflux. Journal of Clinical Endocrinology and Metabolism 94, 1810–1817.CrossRefGoogle ScholarPubMed
Provencher, V, Begin, C, Gagnon-Girouard, MP, Tremblay, A, Boivin, S, Lemieux, S (2008). Personality traits in overweight and obese women: associations with BMI and eating behaviors. Eating Behaviors 9, 294–302.CrossRefGoogle ScholarPubMed
Rabe, K, Lehrke, M, Parhofer, KG, Broedl, UC (2008). Adipokines and insulin resistance. Molecular Medicine 14, 741–751.CrossRefGoogle ScholarPubMed
Raison, CL, Capuron, L, Miller, AH (2006). Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends in Immunology 27, 24–31.CrossRefGoogle ScholarPubMed
Rivest, S, Lacroix, S, Vallieres, L, Nadeau, S, Zhang, J, Laflamme, N (2000). How the blood talks to the brain parenchyma and the paraventricular nucleus of the hypothalamus during systemic inflammatory and infectious stimuli. Proceedings of the Society for Experimental Biology and Medicine 223, 22–38.Google Scholar
Roberts, SB, Kendler, KS (1999). Neuroticism and self-esteem as indices of the vulnerability to major depression in women. Psychological Medicine 29, 1101–1109.CrossRefGoogle ScholarPubMed
Rolland, JP (1998). Psychometric qualities of the French translation of the personality inventory NEO PI R [in French]. Revue Française de Psychiatry et de Psychologie Médicale 18, 139–144.Google Scholar
Watkins, LR, Goehler, LE, Relton, JK, Tartaglia, N, Silbert, L, Martin, D, Maier, SF (1995). Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune–brain communication. Neuroscience Letters 183, 27–31.CrossRefGoogle ScholarPubMed
Wellen, KE, Hotamisligil, GS (2003). Obesity-induced inflammatory changes in adipose tissue. Journal of Clinical Investigation 112, 1785–1788.CrossRefGoogle ScholarPubMed
Wilberg, T, Karterud, S, Pedersen, G, Urnes, O, Costa, PT (2009). Nineteen-month stability of Revised NEO Personality Inventory domain and facet scores in patients with personality disorders. Journal of Nervous and Mental Disease 197, 187–195.CrossRefGoogle ScholarPubMed
Wolfe, BL, Terry, ML (2006). Expectations and outcomes with gastric bypass surgery. Obesity Surgery 16, 1622–1629.CrossRefGoogle ScholarPubMed
WHO (2007). The Challenge of Obesity in the WHO European Region and the Strategies for Response (ed. Branca, F., Nikogosian, H. and Lobstein, T.). WHO Regional Office for Europe: Copenhagen.Google Scholar