Journal of Physiology and Biochemistry

, Volume 75, Issue 3, pp 311–319 | Cite as

Has the adipokine profile an influence on the catch-up growth type in small for gestational age infants?

  • A. Léniz
  • M. P. Portillo
  • Alfredo Fernández-QuintelaEmail author
  • M. T. Macarulla
  • A. Sarasua-Miranda
  • M. del Hoyo
  • I. Díez-López


Infants born small for gestational age (SGA) are at increased risk of perinatal morbidity, persistent short stature, and metabolic alterations in later life. Moreover, the post-natal growth pattern of SGA infants may be an important contributor to health outcomes later in life, which can be influenced by adipokines. The aims of this study were to compare plasma adipokine profiles (leptin, adiponectin, vaspin, chemerin, and nephroblastoma overexpressed (NOV/CCN3)) among SGA newborns aged 3 months, with low, normal, or high catch-up, to search for potential differences between males and females and to analyze the evolution of several adipokines in plasma from SGA newborns between 3 and 24 months. This prospective, longitudinal study was addressed in SGA Caucasian subjects at Hospital Universitario de Álava-Txagorritxu. We observed that infants with fast catch-up showed significantly lower birth weight than the other two groups. As far as adipokines are concerned, they could have an influence on catch-up type because differences among the three experimental groups were found. It may be proposed that health prognoses in infants with slow and fast catch-up are opposite, not only in adulthood but also during their first months. Finally, adipokine evolution patterns during the first 24 months of age differ, depending on the adipokine, and 24-month-old males show lower levels of leptin, adiponectin, and omentin than females.


SGA Catch-up Leptin Adiponectin Omentin Chemerin Vaspin NOV/CCN3 


Funding information

This work was supported by grants from Pfizer International (2012/13), Government of the Basque Country (IT-572-13), and Instituto de Salud Carlos III (CIBERobn).

Compliance with ethical standards

Ethical approval

The study protocol has been approved by the Ethical Committee of the Hospital Universitario de Álava-Txagorritxu (HUA) (Ref. 2012-050). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Parents of all subjects have given their written informed consent to take part in the study. Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Ahima RS, Flier JS (2000) Adipose tissue as an endocrine organ. Trends Endocrinol Metab 11:327–332CrossRefGoogle Scholar
  2. 2.
    Ahima RS, Qi Y, Singhal NS, Jackson MB, Scherer PE (2006) Brain adipocytokine action and metabolic regulation. Diabetes 55(Suppl 2):S145–S154CrossRefPubMedGoogle Scholar
  3. 3.
    Akcay A, Akar M, Demirel G, Canpolat FE, Erdeve O, Dilmen U (2013) Umbilical cord and fifth-day serum vaspin concentrations in small-, appropriate-, and large-for-gestational age neonates. J Pediatr Endocrinol Metab 26:635–638CrossRefPubMedGoogle Scholar
  4. 4.
    Albertsson-Wikland K, Boguszewski M, Karlberg J (1998) Children born small-for-gestational age: postnatal growth and hormonal status. Horm Res Paediatr 49(suppl 2):7–13CrossRefGoogle Scholar
  5. 5.
    Amador-Licona N, Martinez-Cordero C, Guizar-Mendoza JM, Malacara JM, Hernandez J, Alcala JF (2007) Catch-up growth in infants born small for gestational age - a longitudinal study. J Pediatr Endocrinol Metab 20:379–386. CrossRefPubMedGoogle Scholar
  6. 6.
    Blüher M (2012) Vaspin in obesity and diabetes: pathophysiological and clinical significance. Endocrine 41:176–182CrossRefPubMedGoogle Scholar
  7. 7.
    Boersma B, Wit JM (1997) Catch-up growth. Endocr Rev 18:646–661CrossRefPubMedGoogle Scholar
  8. 8.
    Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, Walder K, Segal D (2007) Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 148:4687–4694CrossRefPubMedGoogle Scholar
  9. 9.
    Bozaoglu K, Segal D, Shields KA, Cummings N, Curran JE, Comuzzie AG, Mahaney MC, Rainwater DL, VandeBerg JL, MacCluer JW, Collier G, Blangero J, Walder K, Jowett JBM (2009) Chemerin is associated with metabolic syndrome phenotypes in a Mexican-American population. J Clin Endocrinol Metab 94:3085–3088CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Bozzola E, Meazza C, Arvigo M, Travaglino P, Pagani S, Stronati M, Gasparoni A, Bianco C, Bozzola M (2010) Role of adiponectin and leptin on body development in infants during the first year of life. Ital J Pediatr 36:26CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Briffa JF, McAinch AJ, Romano T, Wlodek ME, Hryciw DH (2015) Leptin in pregnancy and development: a contributor to adulthood disease? Am J Physiol Endocrinol Metab 308:E335–E350CrossRefPubMedGoogle Scholar
  12. 12.
    Britt C, Sven C, Ove A (2005) Preterm and term births of small for gestational age infants: a population-based study of risk factors among nulliparous women. Br J Obstet Gynaecol 105:1011–1017Google Scholar
  13. 13.
    Buyukinan M, Atar M, Can U, Pirgon O, Guzelant A, Deniz I (2018) The association between serum vaspin and omentin-1 levels in obese children with metabolic syndrome. Metab Syndr Relat Disord 16(2):76–81CrossRefPubMedGoogle Scholar
  14. 14.
    Carling SJ, Demment MM, Kjolhede CL, Olson CM (2015) Breastfeeding duration and weight gain trajectory in infancy. Pediatrics 135:111–119CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Carrascosa A, Fernández JM, Ferrández A, López-Siguero JP, López D, Sánchez E (2010) Estudios españoles de crecimiento. Available from: Last Accessed April 2019
  16. 16.
    Cheng G, Bolzenius K, Joslowski G, Günther AL, Kroke A, Heinrich J, Buyken AE (2015) Velocities of weight, height and fat mass gain during potentially critical periods of growth are decisive for adult body composition. Eur J Clin Nutr 69:262–268CrossRefPubMedGoogle Scholar
  17. 17.
    Cho WK, Suh BK (2016) Catch-up growth and catch-up fat in children born small for gestational age. Korean J Pediatr 59(1):1–7CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    de Kroon ML, Renders CM, van Wouwe JP, van Buuren S, Hirasing RA (2010) The Terneuzen birth cohort: BMI change between 2 and 6 years is most predictive of adult cardiometabolic risk. PLoS One 5(11):e13966CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Dos Santos E, Duval F, Vialard F, Dieudonné MN (2015) The roles of leptin and adiponectin at the fetal-maternal interface in humans. Horm Mol Biol Clin Invest 24:47–63Google Scholar
  20. 20.
    D'souza AM, Neumann UH, Glavas MM, Kieffer TJ (2017) The glucoregulatory actions of leptin. Mol Metab 6(9):1052–1065CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    El-Mesallamy HO, Kassem DH, El-Demerdash E, Amin AI (2011) Vaspin and visfatin/Nampt are interesting interrelated adipokines playing a role in the pathogenesis of type 2 diabetes mellitus. Metabolism 60:63–70CrossRefPubMedGoogle Scholar
  22. 22.
    Escoté X, Gómez-Zorita S, López-Yoldi M, Milton-Laskibar I, Ferández-Quintela A, Martínez AJ, Moreno-Aliaga J, Portillo MP (2017) Role of omentin, vaspin, cardiotrophin-1, TWEAK and NOV/CCN3 in obesity and diabetes development. Int J Mol Sci 18Google Scholar
  23. 23.
    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRefPubMedGoogle Scholar
  24. 24.
    Giapros V, Vavva E, Siomou E, Kolios G, Tsabouri S, Cholevas V, Bairaktari E, Tzoufi M, Challa A (2017) Low-birth-weight, but not catch-up growth, correlates with insulin resistance and resistin level in SGA infants at 12 months. J Matern Fetal Neonatal Med 30:1771–1776CrossRefPubMedGoogle Scholar
  25. 25.
    Heiker JT (2014) Vaspin (serpinA12) in obesity, insulin resistance, and inflammation. J Pept Sci 20(5):299–306CrossRefPubMedGoogle Scholar
  26. 26.
    Helfer G, Wu Q (2018) Chemerin: a multifaceted adipokine involved in metabolic disorders. J Endocrinol 238:R79–R94CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Hokken-Koelega AC, De Ridder MA, Lemmen RJ, Den Hartog H, De Muinck Keizer-Schrama SM, Drop SL (1995) Children born small for gestational age: do they catch up? Pediatr Res 38:267–271CrossRefPubMedGoogle Scholar
  28. 28.
    Hovi P, Andersson S, Eriksson JG, Järvenpää AL, Strang-Karlsson S, Mäkitie O, Kajantie E (2007) Glucose regulation in young adults with very low birth weight. N Engl J Med 356:2053–2063CrossRefPubMedGoogle Scholar
  29. 29.
    Huang Y, Li Y, Chen Q, Chen H, Ma H, Su Z, Du M (2015) Low serum adiponectin levels are associated with reduced insulin sensitivity and lipid disturbances in short children born small for gestational age. Clin Endocrinol 83:78–84CrossRefGoogle Scholar
  30. 30.
    Iñiguez G, Soto N, Avila A, Salazar T, Ong K, Dunger D, Mericq V (2004) Adiponectin levels in the first two years of life in a prospective cohort: relations with weight gain, leptin levels and insulin sensitivity. J Clin Endocrinol Metab 89:5500–5503CrossRefPubMedGoogle Scholar
  31. 31.
    Jornayvaz FR, Vollenweider P, Bochud M, Mooser V, Waeber G, Marques-Vidal P (2016) Low birth weight leads to obesity, diabetes and increased leptin levels in adults: the CoLaus study. Cardiovasc Diabetol 15:73CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Karlberg JP, Albertsson-Wikland K, Kwan EY, Lam BC, Low LC (1997) The timing of early postnatal catch-up growth in normal, full-term infants born short for gestational age. Horm Res 48(Suppl 1):17–24CrossRefPubMedGoogle Scholar
  33. 33.
    Kistner A, Vanpée M, Hall K (2013) Leptin may enhance hepatic insulin sensitivity in children and women born small for gestational age. Endocr Connect 2:38–49CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lee PA, Chernausek SD, Hokken-Koelega A, Czernichow P (2003) International small for gestational age advisory board consensus development conference statement: management of short children born small for gestational age, April 24-October 1, 2001. Pediatrics 111:1253–1261CrossRefPubMedGoogle Scholar
  35. 35.
    Lei X, Chen Y, Ye J, Ouyang F, Jiang F, Zhang J (2015) The optimal postnatal growth trajectory for term small for gestational age babies: a prospective cohort study. J Pediatr 166:54–58CrossRefPubMedGoogle Scholar
  36. 36.
    Levy-Marchal C, Jaquet D (2004) Long-term metabolic consequences of being born small for gestational age. Pediatr Diabetes 5:147–153CrossRefPubMedGoogle Scholar
  37. 37.
    Maeyama K, Morioka I, Iwatani S, Fukushima S, Kurokawa D, Yamana K, Nishida K, Ohyama S, Fujioka K, Awano H, Taniguchi-Ikeda M, Nozu K, Nagase H, Nishimura N, Shirai C, Iijima K (2016) Gestational age-dependency of height and body mass index trajectories during the first 3 years in Japanese small-for-gestational age children. Sci Rep 6:38659CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Martin A, Connelly A, Bland RM, Reilly JJ (2017) Health impact of catch-up growth in low-birth weight infants: systematic review, evidence appraisal, and meta-analysis. Matern Child Nutr 13(1):
  39. 39.
    Martinerie C, Garcia M, Do TT, Antoine B, Moldes M, Dorothee G, Kazazian C, Auclair M, Buyse M, Ledent T, Marchal PO, Fesatidou M, Beisseiche A, Koseki H, Hiraoka S, Chadjichristos CE, Blondeau B, Denis RG, Luquet S, Feve B (2016) NOV/CCN3: a new adipocytokine involved in obesity-associated insulin resistance. Diabetes 65(9):2502–2515CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Mazaki-Tovi S, Kasher-Meron M, Hemi R, Haas J, Gat I, Lantsberg D, Hendler I, Kanety H (2012) Chemerin is present in human cord blood and is positively correlated with birthweight. Am J Obstet Gynecol 207:412.e1–412.10CrossRefGoogle Scholar
  41. 41.
    Meek TH, Morton GJ (2016) The role of leptin in diabetes: metabolic effects. Diabetologia 59(5):928–932CrossRefPubMedGoogle Scholar
  42. 42.
    Ong KKL, Ahmed ML, Emmett PM, Preece MA, Dunger DB (2000) Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 320:967–971CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Parikh NI, Hwang S, Ingelsson E, Benjamin EJ, Fox CS, Vasan RS, Murabito JM (2009) Breastfeeding in infancy and adult cardiovascular disease risk factors. Am J Med 122:656–663CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Rolland-Cachera MF, Deheeger M, Maillot M, Bellisle F (2006) Early adiposity rebound: causes and consequences for obesity in children and adults. Int J Obes 30(Suppl 4):S11–S17CrossRefGoogle Scholar
  45. 45.
    Yang R-Z, Lee M-J, Hu H, Pray J, Hai-Bin W, Hansen BC, Shuldiner AR, Fried SK, McLenithan JC, Gong D-W (2006) Identification of omentin as a novel depot-specific adipokine in human adipose tissue: possible role in modulating insulin action. Am J Physiol Endocrinol Metab 290:E1253–E1261CrossRefPubMedGoogle Scholar
  46. 46.
    Saenger P, Czernichow P, Hughes I, Reiter EO (2007) Small for gestational age: short stature and beyond. Endocr Rev 28:219–251CrossRefPubMedGoogle Scholar
  47. 47.
    Saggese G, Fanos M, Simi F (2013) SGA children: auxological and metabolic outcomes - the role of GH treatment. J Matern Fetal Neonatal Med 26(Suppl 2):64–67CrossRefPubMedGoogle Scholar
  48. 48.
    Singhal A (2017) Long-term adverse effects of early growth acceleration or catch-up growth. Ann Nutr Metab 70(3):236–240CrossRefPubMedGoogle Scholar
  49. 49.
    Tannenbaum GS, Gurd W, Lapointe M (1998) Leptin is a potent stimulator of spontaneous pulsatile growth hormone (GH) secretion and the GH response to GH-releasing hormone. Endocrinology 139:3871–3875CrossRefPubMedGoogle Scholar
  50. 50.
    Xiao X, Zhang Z, Li W, Feng K, Sun Q, Cohen HJ, Xu T, Wang H, Liu A, Gong X, Shen Y, Yi Z (2010) Low birth weight is associated with components of the metabolic syndrome. Metabolism 59:1282–1286CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Zhu X, Jiang Y, Shan PF, Shen J, Liang QH, Cui RR, Liu Y, Liu GY, Wu SS, Lu Q, Xie H, Liu YS, Yuan LQ, Liao EY (2013) Vaspin attenuates the apoptosis of human osteoblasts through ERK signaling pathway. Amino Acids 44(3):961–968CrossRefPubMedGoogle Scholar
  52. 52.
    Zieger K, Weiner J, Krause K, Schwarz M, Kohn M, Stumvoll M, Bluher M, Heiker JT (2018) Vaspin suppresses cytokine-induced inflammation in 3T3-L1 adipocytes via inhibition of NFkappaB pathway. Mol Cell Endocrinol 460:181–188CrossRefPubMedGoogle Scholar

Copyright information

© University of Navarra 2019

Authors and Affiliations

  • A. Léniz
    • 1
    • 2
  • M. P. Portillo
    • 1
    • 3
    • 4
  • Alfredo Fernández-Quintela
    • 1
    • 3
    • 4
    Email author
  • M. T. Macarulla
    • 1
    • 3
    • 4
  • A. Sarasua-Miranda
    • 5
  • M. del Hoyo
    • 5
  • I. Díez-López
    • 5
  1. 1.Nutrition and Obesity GroupUniversity of the Basque Country (UPV/EHU) and Lucio Lascaray Research InstituteVitoriaSpain
  2. 2.Araba Integrated Health Care OrganizationBasque Health Service (Osakidetza)VitoriaSpain
  3. 3.CIBERobn Physiopathology of Obesity and NutritionInstitute of Health Carlos IIIVitoriaSpain
  4. 4.Department Nutrition and Food Sciences, University of the Basque CountryPaseo de la UniversidadVitoriaSpain
  5. 5.Pediatric Endocrinology Unit, HU Araba Vitoria. Department of PediatricUniversity of the Basque Country (UPV/EHU)LeioaSpain

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