Catch-up growth during infancy and childhood is increasingly recognized as a major risk factor for later development of insulin-related complications and chronic diseases, namely abdominal obesity, type 2 diabetes and cardiovascular disease. As catch-up growth per se is characterized by insulin resistance, hyperinsulinaemia and an accelerated rate of fat storage (i.e., catch-up fat) even in the absence of hyperphagia, the possibility arises that suppressed thermogenesis in certain organs/tissues – for the purpose of enhancing the efficiency of catch-up fat – also plays a role in the pathophysiological consequences of catch-up growth. Here, the evidence for the existence of an adipose-specific control of thermogenesis, the suppression of which contributes to catch-up fat, is reviewed. Recent findings suggest that such suppression of thermogenesis is accompanied by hyperinsulinaemia, insulin resistance in skeletal muscle and insulin hyperresponsiveness in adipose tissue, all of which precede the appearance of excess body fat, central fat distribution and elevations in intramyocellular triglyceride or circulating lipid concentrations. These findings underscore a role for suppressed thermogenesis per se as an early event in the pathophysiology of catch-up growth. It is proposed that, in its evolutionary adaptive role to spare glucose for the rapid rebuilding of an adequate fat reserve (for optimal survival capacity during intermittent famine), suppressed thermogenesis in skeletal muscle constitutes a thrifty phenotype that confers to the phase of catch-up growth its high sensitivity to the development of insulin resistance and hyperinsulinaemia. In the context of the complex interactions between earlier reprogramming and a modern lifestyle characterized by nutritional abundance and low physical activity, this thrifty ‘catch-up fat phenotype’ is a central event that predisposes individuals with catch-up growth to abdominal obesity, type 2 diabetes and cardiovascular disease.

1.
Eriksson JG, Forsen T, Tuomilehto J, Winter PD, Osmond C, Barker DJ: Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ 1999;318:427–431.
2.
Cianfarani S, Germani D, Branca F: Low birthweight and adult insulin resistance: the ‘catch-up growth’ hypothesis. Arch Dis Child Fetal Neonatal Ed 1999;81:F71–F73.
3.
Huxley RR, Shiell AW, Law CM: The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. J Hypertens 2000;18:815–831.
4.
Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB: Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 2000;320:967–971.
5.
Levy-Marchal C, Jaquet D, Czernichow P: Long-term metabolic consequences of being born small for gestational age. Semin Neonatol 2004;9:67–74.
6.
Hales CN, Barker DJ: The thrifty phenotype hypothesis. Br Med Bull 2001;60:5–20.
7.
Young JB: Programming of sympathoadrenal function. Trends Endocrinol Metab 2002;13:381–385.
8.
Colle E, Schiff D, Andrew G, Bauer CB, Fitzhardinge P: Insulin responses during catch-up growth of infants who were small for gestational age. Pediatrics 1976;57:363–371.
9.
Ong KK, Dunger DB: Birth weight, infant growth and insulin resistance. Eur J Endocrinol 2004;151(suppl 3):U131–U139.
10.
Soto N, Bazaes RA, Pena V, Salazar T, Avila A, Iniguez G, Ong KK, Dunger DB, Mericq MV: Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort. J Clin Endocrinol Metab 2003;88:3645–3650.
11.
Dulloo AG, Jacquet J, Montani JP: Pathways from weight fluctuations to metabolic diseases: focus on maladaptive thermogenesis during catch-up fat. Int J Obes Relat Metab Disord 2002;26(suppl 2):S46–S57.
12.
Kornfeld W, Schüller H: Pattern of lean tissue deposition in free-living children recovering from tuberculosis. Z Kinder Jugendpsychiatrie 1931;51:349–362.
13.
Debray C, Zarakovitch M, Ranson B, Jacquemin J, Robert J, Sirage M: Contribution to the study on the pathology of the deportees. Sem Hôpital Paris 1946;22:863–870.
14.
Keys A, Borizek J, Henschel A, Mickelson O, Taylor HL: The Biology of Human Starvation. Minneapolis, University of Minnesota Press, 1950.
15.
Weyer C, Walford RL, Harper IT, Milner M, MacCallum T, Tataranni PA, Ravussin E: Energy metabolism after 2 y of energy restriction: the biosphere 2 experiment. Am J Clin Nutr 2000;72:946–953.
16.
Forbes GB, Kreipe RE, Lipinski BA, Hodgman CH: Body composition changes during recovery from anorexia nervosa: comparison of two dietary regimes. Am J Clin Nutr 1984;40:1137–1145.
17.
Mitchell PB, Truswell AS: Body composition in anorexia nervosa and starvation; in Beamont PJV, Burrows GD, Casper RC (eds): Handbook of Eating Disorders. I. Anorexia and Bulimia Nervosa. Amsterdam, Elsevier, 1987, pp 981–991.
18.
Barac-Nieto M, Spurr GB, Lotero H, Maksud MG, Dahners HW: Body composition during nutritional repletion of severely undernourished men. Am J Clin Nutr 1979;32:981–991.
19.
Ashworth A: Metabolic rates during recovery from protein-calorie malnutrition: the need for a new concept of specific dynamic action. Nature 1969;223:407–409.
20.
MacLean WC Jr, Graham GG: The effect of energy intake on nitrogen content of weight gained by recovering malnourished infants. Am J Clin Nutr 1980;33:903–909.
21.
Castilla-Serna L, Perez-Ortiz B, Cravioto J: Patterns of muscle and fat mass repair during recovery from advanced infantile protein-energy malnutrition. Eur J Clin Nutr 1996;50:392–397.
22.
van Eys J: Nutrition and cancer: physiological interrelationships. Annu Rev Nutr 1985;5:435–461.
23.
Streat SJ, Beddoe AH, Hill GL: Aggressive nutritional support does not prevent protein loss despite fat gain in septic intensive care patients. J Trauma 1987;27:262–266.
24.
Kotler DP, Tierney AR, Culpepper-Morgan JA, Wang J, Pierson RN Jr: Effect of home total parenteral nutrition on body composition in patients with acquired immunodeficiency syndrome. J Parenter Enteral Nutr 1990;14:454–458.
25.
Jornayvaz FR, Selz R, Tappy L, Theintz GE: Metabolism of oral glucose in children born small for gestational age: evidence for an impaired whole body glucose oxidation. Metabolism 2004;53:847–851.
26.
Eriksson J, Forsen T, Tuomilehto J, Osmond C, Barker D: Size at birth, fat-free mass and resting metabolic rate in adult life. Horm Metab Res 2002;34:72–76.
27.
Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, Pilgaard K, Schou JH, Madsbad S, Astrup A, Vaag A: Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care 2005;28:151–153.
28.
Hermann TS, Rask-Madsen C, Ihlemann N, Dominguez H, Jensen CB, Storgaard H, Vaag AA, Kober L, Torp-Pedersen C: Normal insulin-stimulated endothelial function and impaired insulin-stimulated muscle glucose uptake in young adults with low birth weight. J Clin Endocrinol Metab 2003;88:1252–1257.
29.
Ozanne SE, Jensen CB, Tingey KJ, Storgaard H, Madsbad S, Vaag AA: Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 2005;48:547–552.
30.
Dulloo AG, Antic V, Montani JP: Ectopic fat stores: housekeepers that can overspill into weapons of lean body mass destruction. Int J Obes Relat Metab Disord 2004;28(suppl 4):S1–S2.
31.
Dulloo AG, Jacquet J: Adaptive reduction in basal metabolic rate in response to food deprivation in humans: a role for feedback signals from fat stores. Am J Clin Nutr 1998;68:599–606.
32.
Dulloo AG, Jacquet J: An adipose-specific control of thermogenesis in body weight regulation. Int J Obes Relat Metab Disord 2001;25(suppl 5):S22–S29.
33.
Dulloo AG, Girardier L: Adaptive role of energy expenditure in modulating body fat and protein deposition during catch-up growth after early undernutrition. Am J Clin Nutr 1993;58:614–621.
34.
Crescenzo R, Samec S, Antic V, Rohner-Jeanrenaud F, Seydoux J, Montani JP, Dulloo AG: A role for suppressed thermogenesis favoring catch-up fat in the pathophysiology of catch-up growth. Diabetes 2003;52:1090–1097.
35.
Cettour-Rose P, Samec S, Russell AP, Summermatter S, Mainieri D, Carrillo-Theander C, Montani JP, Seydoux J, Rohner-Jeanrenaud F, Dulloo AG: Redistribution of glucose from skeletal muscle to adipose tissue during catch-up fat: a link between catch-up growth and later metabolic syndrome. Diabetes 2005;54:751–756.
36.
Dulloo AG: A role for suppressed skeletal muscle thermogenesis in pathways from weight fluctuations to the insulin resistance syndrome. Acta Physiol Scand 2005;184:295–307.
37.
Dulloo AG, Gubler M, Montani JP, Seydoux J, Solinas G: Substrate cycling between de novo lipogenesis and lipid oxidation: a thermogenic mechanism against skeletal muscle lipotoxicity and glucolipotoxicity. Int J Obes Relat Metab Disord 2004;28(suppl 4):S29–S37.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.