Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-30T05:54:32.891Z Has data issue: false hasContentIssue false

Peer problems are associated with elevated serum leptin levels in children

Published online by Cambridge University Press:  08 April 2013

G. Kohlboeck*
Affiliation:
Helmholtz Zentrum Muenchen, German Research Center for Environmental Health, Institute of Epidemiology I, Neuherberg, Germany
M. Romanos
Affiliation:
Department of Child and Adolescent Psychiatry and Psychotherapy, University Hospital Wuerzburg, Germany
C. Tiesler
Affiliation:
Helmholtz Zentrum Muenchen, German Research Center for Environmental Health, Institute of Epidemiology I, Neuherberg, Germany Dr von Hauner Children's Hospital, Ludwig-Maximilians-University of Munich, Germany
S. Koletzko
Affiliation:
Dr von Hauner Children's Hospital, Ludwig-Maximilians-University of Munich, Germany
J. Kratzsch
Affiliation:
University Leipzig, Institute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, Germany
J. Thiery
Affiliation:
University Leipzig, Institute of Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, Germany
C.-P. Bauer
Affiliation:
Department of Pediatrics, Technical University of Munich, Germany
A. von Berg
Affiliation:
Department of Pediatrics, Marien-Hospital Wesel, Germany
D. Berdel
Affiliation:
Department of Pediatrics, Marien-Hospital Wesel, Germany
B. Hoffmann
Affiliation:
Leibniz Research Institute for Environmental Medicine, University of Düsseldorf, Germany
B. Schaaf
Affiliation:
Medical Practice for Pediatrics, Bad Honnef, Germany
I. Lehmann
Affiliation:
UFZ-Center for Environmental Research, Leipzig, Germany
O. Herbarth
Affiliation:
University Leipzig, Faculty of Medicine, Environmental Medicine and Hygiene, Leipzig, Germany
J. Heinrich
Affiliation:
Helmholtz Zentrum Muenchen, German Research Center for Environmental Health, Institute of Epidemiology I, Neuherberg, Germany
*
* Address for correspondence: G. Kohlboeck, Ph.D., Helmholtz Zentrum München, Institut für Epidemiologie, Ingolstädter Landstr. 1, D-85764 Neuherberg, Germany. (Email: [email protected])

Abstract

Background

Leptin is thought to act as an important mediator in stress reactions. To date, no study has examined the association between psychological stress and leptin levels in children. This study aimed to assess the association between emotional symptoms and peer problems and serum leptin levels in children aged 10 years of the two population-based GINI-plus and LISA-plus birth cohorts.

Method

Cross-sectional data from 2827 children aged 10 years were assessed with regard to leptin concentrations in serum and behavioral problems using the parent-reported Strengths and Difficulties Questionnaire (SDQ). Linear regression modeling was applied to determine the likelihood of elevated leptin levels in children with emotional symptoms and peer problems, controlling for socio-economic status (SES), body mass index (BMI), fasting serum leptin levels, pubertal development and sex hormones.

Results

We found that increases in emotional symptoms (exp βadj = 1.03, s.e. = 0.02, p < 0.04) and peer problems (exp βadj = 1.05, s.e. = 0.01, p = 0.0001) were significantly associated with higher serum leptin levels controlled for BMI and sociodemographic factors. Similar results were found when the fasting serum leptin sample was examined (exp βadj = 1.08, s.e. = 0.04, p = 0.0294). Gender-stratified analyses showed a significant relationship between serum leptin and peer problems in girls (exp βadj = 1.05, s.e. = 0.02, p = 0.03), and a borderline significant association in boys (exp βadj = 1.04, s.e. = 0.02, p = 0.05).

Conclusions

Children with peer problems have higher stress and eat more, acquire a higher body fat mass and thus, through increased leptin resistance, exhibit higher leptin levels.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2013 

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

Ankarberg-Lindgren, C, Dahlgren, J, Carlsson, B, Rosberg, S, Carlsson, L, Wikland, KA, Norjavaara, E (2001). Leptin levels show diurnal variation throughout puberty in healthy children, and follow a gender-specific pattern. European Journal of Endocrinology 145, 4351.Google Scholar
Antonijevic, IA, Murck, H, Frieboes, RM, Horn, R, Brabant, G, Steiger, A (1998). Elevated nocturnal profiles of serum leptin in patients with depression. Journal of Psychiatric Research 32, 403410.Google Scholar
Auwerx, J, Staels, B (1998). Leptin. Lancet 351, 737742.Google Scholar
Baumeister, RF, Leary, MR (1995). The need to belong: desire for interpersonal attachments as a fundamental human motivation. Psychological Bulletin 117, 497529.Google Scholar
Birketvedt, GS, Florholmen, J, Sundsfjord, J, Osterud, B, Dinges, D, Bilker, W, Stunkard, A (1999). Behavioral and neuroendocrine characteristics of the night-eating syndrome. Journal of the American Medical Association 282, 657663.CrossRefGoogle ScholarPubMed
Bjorntorp, P (2001). Do stress reactions cause abdominal obesity and comorbidities? Obesity Reviews 2, 7386.Google Scholar
Blum, WF, Englaro, P, Hanitsch, S, Juul, A, Hertel, NT, Müller, J, Skakkebæk, NE, Heiman, ML, Birkett, M, Attanasio, AM, Kiess, W, Rascher, W (1997). Plasma leptin levels in healthy children and adolescents: dependence on body mass index, body fat mass, gender, pubertal stage, and testosterone. Journal of Clinical Endocrinology and Metabolism 82, 29042910.Google Scholar
Boneberger, A, von Kries, R, Milde-Busch, A, Bolte, G, Rochat, MK, Ruckinger, S (2009). Association between peer relationship problems and childhood overweight/obesity. Acta Paediatrica 98, 19501955.Google Scholar
Brannian, JD, Schmidt, SM, Kreger, DO, Hansen, KA (2001). Baseline non-fasting serum leptin concentration to body mass index ratio is predictive of IVF outcomes. Human Reproduction 16, 18191826.CrossRefGoogle ScholarPubMed
Brennan, AM, Fargnoli, JL, Williams, CJ, Li, T, Willett, W, Kawachi, I, Qi, L, Hu, FB, Mantzoros, CS (2009). Phobic anxiety is associated with higher serum concentrations of adipokines and cytokines in women with diabetes. Diabetes Care 32, 926931.Google Scholar
Brydon, L, Wright, CE, O'Donnell, K, Zachary, I, Wardle, J, Steptoe, A (2007). Stress-induced cytokine responses and central adiposity in young women. International Journal of Obesity 32, 443450.CrossRefGoogle ScholarPubMed
Casanueva, FF, Dieguez, C, Popovic, V, Peino, R, Considine, RV, Caro, JF (1997). Serum immunoreactive leptin concentrations in patients with anorexia nervosa before and after partial weight recovery. Biochemical and Molecular Medicine 60, 116120.Google Scholar
Considine, RV, Sinha, MK, Heiman, ML, Kriauciunas, A, Stephens, TW, Nyce, MR, Ohannesian, JP, Marco, CC, McKee, LJ, Bauer, TL, Caro, JF (1996). Serum immunoreactive-leptin concentrations in normal-weight and obese humans. New England Journal of Medicine 334, 292295.Google Scholar
Demerath, EW, Towne, B, Wisemandle, W, Blangero, J, Chumlea, WC, Siervogel, RM (1999). Serum leptin concentration, body composition, and gonadal hormones during puberty. International Journal of Obesity and Related Metabolic Disorders 23, 678685.Google Scholar
Drukker, M, Wojciechowski, F, Feron, FJM, Mengelers, R, van Os, J (2009). A community study of psychosocial functioning and weight in young children and adolescents. International Journal of Pediatric Obesity 4, 9197.Google Scholar
Erikson, EH (1959). Identity and the Life Cycle. International Universities Press: New York.Google Scholar
Esel, E, Ozsoy, S, Tutus, A, Sofuoglu, S, Kartalci, S, Bayram, F, Kokbudak, Z, Kula, M (2005). Effects of antidepressant treatment and of gender on serum leptin levels in patients with major depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry 29, 565570.Google Scholar
Filipiak, B, Zutavern, A, Koletzko, S, von Berg, A, Brockow, I, Grubl, A, Berdel, D, Reinhardt, D, Bauer, CP, Wichmann, HE, Heinrich, J (2007). Solid food introduction in relation to eczema: results from a four-year prospective birth cohort study. Journal of Pediatrics 151, 352358.Google Scholar
Flinn, MV (1999). Family environment, stress and health during childhood. In Hormones, Health and Behavior: A Socio-ecological and Lifespan Perspective (ed. Panter-Brick, C. and Worthman, C. M.), pp. 105138. Cambridge University Press: Cambridge.Google Scholar
Flinn, MV, England, BG (1995). Childhood stress and family environment. Current Anthropology 36, 854866.CrossRefGoogle Scholar
Focker, M, Timmesfeld, N, Scherag, S, Buhren, K, Langkamp, M, Dempfle, A, Sheridan, EM, de Zwaan, M, Fleischhaker, C, Herzog, W, Egberts, K, Zipfel, S, Herpertz-Dahlmann, B, Hebebrand, J (2011). Screening for anorexia nervosa via measurement of serum leptin levels. Journal of Neural Transmission 118, 571578.Google Scholar
Garcia-Mayor, RV, Andrade, MA, Rios, M, Lage, M, Dieguez, C, Casanueva, FF (1997). Serum leptin levels in normal children: relationship to age, gender, body mass index, pituitary-gonadal hormones, and pubertal stage. Journal of Clinical Endocrinology and Metabolism 82, 28492855.Google ScholarPubMed
Goodman, R (1997). The Strengths and Difficulties Questionnaire: a research note. Journal of Child Psychology and Psychiatry 38, 581586.Google Scholar
Gunnar, MR, Sebanc, AM, Tout, K, Donzella, B, van Dulmen, MM (2003). Peer rejection, temperament, and cortisol activity in preschoolers. Developmental Psychobiology 43, 346358.Google Scholar
Häfner, S, Zierer, A, Emeny, RT, Thorand, B, Herder, C, Koenig, W, Rupprecht, R, Ladwig, KH (2011). Social isolation and depressed mood are associated with elevated serum leptin levels in men but not in women. Psychoneuroendocrinology 36, 200209.Google Scholar
Hancox, RJ, Landhuis, CE (2011). Correlation between measures of insulin resistance in fasting and nonfasting blood. Diabetology and Metabolic Syndrome 3, 23.Google Scholar
Hassink, SG, Sheslow, DV, de Lancey, E, Opentanova, I, Considine, RV, Caro, JF (1996). Serum leptin in children with obesity: relationship to gender and development. Pediatrics 98, 201203.Google Scholar
Hauser, R (1988). Adequacy and Poverty Among the Retired. Ageing Working Paper (AWP) No. 3.2. Organization for Economic Co-operation and Development (OECD): Paris.Google Scholar
Hebebrand, J, Albayrak, O (2012). Leptin treatment of patients with anorexia nervosa? The urgent need for initiation of clinical studies. European Child and Adolescent Psychiatry 21, 6366.Google Scholar
Hebebrand, J, van der Heyden, J, Devos, R, Köpp, W, Herpertz, S, Remschmidt, H, Herzog, W (1995). Plasma concentrations of obese protein in anorexia nervosa. Lancet 346, 16241625.Google Scholar
Heinrich, J, Bolte, G, Holscher, B, Douwes, J, Lehmann, I, Fahlbusch, B, Bischof, W, Weiss, M, Borte, M, Wichmann, HE (2002). Allergens and endotoxin on mothers’ mattresses and total immunoglobulin E in cord blood of neonates. European Respiratory Journal 20, 617623.CrossRefGoogle ScholarPubMed
Herpertz-Dahlmann, B, Buhren, K, Seitz, J (2011). Anorexia nervosa in childhood and adolescence: course and significance for adulthood [in German]. Nervenarzt 82, 10931099.Google Scholar
Houseknecht, KL, Spurlock, ME (2003). Leptin regulation of lipid homeostasis: dietary and metabolic implications. Nutrition Research Reviews 16, 8396.Google Scholar
Howe, LD, Galobardes, B, Sattar, N, Hingorani, AD, Deanfield, J, Ness, AR, Davey-Smith, G, Lawlor, DA (2010). Are there socioeconomic inequalities in cardiovascular risk factors in childhood, and are they mediated by adiposity? Findings from a prospective cohort study. International Journal of Obesity 34, 11491159.Google Scholar
Jow, GM, Yang, TT, Chen, CL (2006). Leptin and cholesterol levels are low in major depressive disorder, but high in schizophrenia. Journal of Affective Disorders 90, 2127.Google Scholar
Khafaji, HA, Bener, A, Osman, M, Al Merri, A, Al Suwaidi, J (2012). The impact of diurnal fasting during Ramadan on the lipid profile, hs-CRP, and serum leptin in stable cardiac patients. Vascular Health and Risk Management 8, 714.Google Scholar
Kopp, W, Blum, WF, Ziegler, A, Mathiak, K, Lubbert, H, Herpertz, S, Deter, HC, Hebebrand, J (1998). Serum leptin and body weight in females with anorexia and bulimia nervosa. Hormone and Metabolic Research 30, 272275.Google Scholar
Kraus, T, Haack, M, Schuld, A, Hinze-Selch, D, Pollmacher, T (2001). Low leptin levels but normal body mass indices in patients with depression or schizophrenia. Neuroendocrinology 73, 243247.Google Scholar
Lawson, EA, Miller, KK, Blum, JI, Meenaghan, E, Misra, M, Eddy, KT, Herzog, DB, Klibanski, A (2011). Leptin levels are associated with decreased depressive symptoms in women across the weight spectrum, independent of body fat. Clinical Endocrinology 6, 520525.Google Scholar
Lazarus, RS, Folkman, S (eds) (1984). Stress, Appraisal, and Coping. Springer: New York, NY.Google Scholar
Liao, SC, Lee, MB, Lee, YJ, Huang, TS (2004). Hyperleptinemia in subjects with persistent partial posttraumatic stress disorder after a major earthquake. Psychosomatic Medicine 66, 2328.CrossRefGoogle ScholarPubMed
Lumeng, JC, Forrest, P, Appugliese, DP, Kaciroti, N, Corwyn, RF, Bradley, RH (2010). Weight status as a predictor of being bullied in third through sixth grades. Pediatrics 125, 13011307.Google Scholar
Margetic, S, Gazzola, C, Pegg, GG, Hill, RA (2002). Leptin: a review of its peripheral actions and interactions. International Journal of Obesity and Related Metabolic Disorders 26, 14071433.Google Scholar
Narita, K, Murata, T, Hamada, T, Kosaka, H, Sudo, S, Mizukami, K, Yoshida, H, Wada, Y (2008). Associations between trait anxiety, insulin resistance, and atherosclerosis in the elderly: a pilot cross-sectional study. Psychoneuroendocrinology 33, 305312.CrossRefGoogle ScholarPubMed
Otsuka, R, Yatsuya, H, Tamakoshi, K, Matsushita, K, Wada, K, Toyoshima, H (2006). Perceived psychological stress and serum leptin concentrations in Japanese men. Obesity 14, 18321838.Google Scholar
Pasco, JA, Jacka, FN, Williams, LJ, Henry, MJ, Nicholson, GC, Kotowicz, MA, Berk, M (2008). Leptin in depressed women: cross-sectional and longitudinal data from an epidemiologic study. Journal of Affective Disorders 107, 221225.Google Scholar
Peters, E, Riksen-Walraven, J, Cillessen, A, de Weerth, C (2011). Peer rejection and HPA activity in middle childhood: friendship makes a difference. Child Development 82, 19061920.Google Scholar
Petersen, AC, Crockett, L, Richards, M, Boxer, A (1988). A self-report measure of pubertal status: reliability, validity, and initial norms. Journal of Youth and Adolescence 17, 117133.CrossRefGoogle ScholarPubMed
Pitrou, I, Shojaei, T, Wazana, A, Gilbert, F, Kovess-Masfety, V (2010). Child overweight, associated psychopathology, and social functioning: a French school-based survey in 6- to 11-year-old children. Obesity 18, 809817.CrossRefGoogle ScholarPubMed
Raison, CL, Capuron, L, Miller, AH (2006). Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends in Immunology 27, 2431.Google Scholar
Rosenbaum, M, Nicholson, M, Hirsch, J, Heymsfield, SB, Gallagher, D, Chu, F, Leibel, RL (1996). Effects of gender, body composition, and menopause on plasma concentrations of leptin. Journal of Clinical Endocrinology and Metabolism 81, 34243427.Google Scholar
Rubin, RT, Rhodes, ME, Czambel, RK (2002). Sexual diergism of baseline plasma leptin and leptin suppression by arginine vasopressin in major depressives and matched controls. Psychiatry Research 113, 255268.CrossRefGoogle ScholarPubMed
Sausenthaler, S, Kompauer, I, Mielck, A, Borte, M, Herbarth, O, Schaaf, B, von Berg, A, Heinrich, J (2007). Impact of parental education and income inequality on children's food intake. Public Health Nutrition 10, 2433.Google Scholar
Schnabel, E, Sausenthaler, S, Schaaf, B, Schafer, T, Lehmann, I, Behrendt, H, Herbarth, O, Borte, M, Kramer, U, von Berg, A, Wichmann, HE, Heinrich, J (2010). Prospective association between food sensitization and food allergy: results of the LISA birth cohort study. Clinical and Experimental Allergy 40, 450457.CrossRefGoogle ScholarPubMed
Schoeller, DA, Cella, LK, Sinha, MK, Caro, JF (1997). Entrainment of the diurnal rhythm of plasma leptin to meal timing. Journal of Clinical Investigation 100, 18821887.CrossRefGoogle ScholarPubMed
Sontag, LM, Graber, JA, Brooks-Gunn, J, Warren, MP (2008). Coping with social stress: implications for psychopathology in young adolescent girls. Journal of Abnormal Child Psychology 36, 11591174.Google Scholar
Speakman, JR, Stubbs, RJ, Mercer, JG (2002). Does body mass play a role in the regulation of food intake? Proceedings of the Nutrition Society 61, 473487.Google Scholar
Stiegler, P, Sausenthaler, S, Buyken, AE, Rzehak, P, Czech, D, Linseisen, J, Kroke, A, Gedrich, K, Robertson, C, Heinrich, J (2010). A new FFQ designed to measure the intake of fatty acids and antioxidants in children. Public Health Nutrition 13, 3846.Google Scholar
Sumner, AE, Falkner, B, Kushner, H, Considine, RV (1998). Relationship of leptin concentration to gender, menopause, age, diabetes, and fat mass in African Americans. Obesity Research 6, 128133.CrossRefGoogle ScholarPubMed
Vaillancourt, T, Duku, E, Decatanzaro, D, Macmillan, H, Muir, C, Schmidt, LA (2008). Variation in hypothalamic-pituitary-adrenal axis activity among bullied and non-bullied children. Aggressive Behavior 34, 294305.Google Scholar
van Aggel-Leijssen, DP, van Baak, MA, Tenenbaum, R, Campfield, LA, Saris, WH (1999). Regulation of average 24 h human plasma leptin level; the influence of exercise and physiological changes in energy balance. International Journal of Obesity and Related Metabolic Disorders 23, 151158.CrossRefGoogle Scholar
von Berg, A, Koletzko, S, Filipiak-Pittroff, B, Laubereau, B, Grubl, A, Wichmann, HE, Bauer, CP, Reinhardt, D, Berdel, D (2007). Certain hydrolyzed formulas reduce the incidence of atopic dermatitis but not that of asthma: three-year results of the German Infant Nutritional Intervention Study. Journal of Allergy and Clinical Immunology 119, 718725.Google Scholar
Watzlawik, M (2009). The acquisition of puberty status using the Pubertal Development Scale. First steps in the evaluation of a German translation [in German]. Diagnostica 55, 5565.Google Scholar
Woerner, W, Becker, A, Rothenberger, A (2004). Normative data and scale properties of the German parent SDQ. European Child and Adolescent Psychiatry 13, 310.Google Scholar
Wolthers, OD, Heuck, C, Skjaerbaek, C (1999). Diurnal rhythm in serum leptin. Journal of Pediatric Endocrinology and Metabolism 12, 863866.CrossRefGoogle ScholarPubMed
Yang, K, Xie, G, Zhang, Z, Wang, C, Li, W, Zhou, W, Tang, Y (2007). Levels of serum interleukin (IL)-6, IL-1β, tumour necrosis factor-α and leptin and their correlation in depression. Australian and New Zealand Journal of Psychiatry 41, 266273.Google Scholar