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Children with metabolically healthy obesity have a worse metabolic profile compared to normal-weight peers: a cross-sectional study

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Abstract

Purpose

A phenotype of metabolically healthy obesity (MHO) has been described in youth with obesity, but data are still scarce in this age group. The aim of the current study was to describe and compare clinical and laboratory parameters related to obesity among three different groups of youth, namely youth with normal weight (NW), with MHO, and with metabolically unhealthy obesity (MUO).

Methods

One hundred and three youngsters with obesity were divided according to 2018 consensus-based criteria into those with MHO [n = 49, age (±SD): 10.9 ± 2.9 years] and those with MUO [n = 54, 11.5 ± 2.7 years] and were compared to age-, sex- and Tanner-matched NW [n = 69, 11.3 ± 2.9 years]. Several obesity-related parameters were investigated for all three groups of children. Comparisons were made by analysis of variance (ANOVA) followed by the Fisher’s PLSD test.

Results

Youth with MHO had lower systolic (p < 0.001) and diastolic (p < 0.01) blood pressure z-score and triglycerides (p < 0.01), but higher HDL-C (p < 0.001), total cholesterol (p < 0.05), and apo-A1 (p < 0.05) compared to those with MUO. Compared to controls, both children with MHO and MUO showed higher fasting insulin (p < 0.05), HOMA-IR (p < 0.05), and QUICKI (p < 0.001). Similarly, both groups had higher hsCRP, fibrinogen, uric acid, and leptin compared to controls (for all, p < 0.001), while their adiponectin was lower (p < 0.05). Visfatin was higher in children with MUO compared to controls (p < 0.01), and it showed a trend to be lower in children with MHO compared to those with MUO (p = 0.1).

Conclusion

This study provides evidence that children identified as having MHO by the consensus-based criteria had better metabolic profiles than youth with MUO, but worse than NW. Further research is needed in pediatric populations both regarding MHO criteria and the nature of the MHO phenotype per se.

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References

  1. J. Bentham, M. Di Cesare, V. Bilano, et al. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet. 390: 2627–2642 (2017)

  2. R. Lakshman, C.E. Elks, K.K. Ong, Childhood obesity. Circulation 126, 1770–1779 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  3. S.J. Olshansky, D.J. Passaro, R.C. Hershow et al. A potential decline in life expectancy in the united states in the 21st century. N. Engl. J. Med. 352, 1138–1145 (2005)

    Article  CAS  PubMed  Google Scholar 

  4. A. Tsatsoulis, S.A. Paschou, Metabolically healthy obesity: criteria, epidemiology, controversies, and consequences. Curr. Obes. Rep. 9, 109–120 (2020)

    Article  PubMed  Google Scholar 

  5. H. Lin, L. Zhang, R. Zheng et al. The prevalence, metabolic risk and effects of lifestyle intervention for metabolically healthy obesity: a systematic review and meta-analysis. Medicine 96, e8838 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  6. R.L. Prince, J.L. Kuk, K.A. Ambler et al. Predictors of metabolically healthy obesity in children. Diabetes Care 37, 1462–1468 (2014)

    Article  CAS  PubMed  Google Scholar 

  7. D.Y. Yoon, Y.A. Lee, J. Lee et al. Prevalence and clinical characteristics of metabolically healthy obesity in Korean children and adolescents: data from the Korea National Health and Nutrition Examination Survey. J. Korean Med. Sci. 32, 1840–1847 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. R. Vukovic, T.J. Dos Santos, M. Ybarra et al. Children with metabolically healthy obesity: a review. Front. Endocrinol. 10, 865 (2019)

    Article  Google Scholar 

  9. R. Weiss, S.E. Taksali, S. Dufour et al. The “Obese insulin-sensitive” adolescent: Importance of adiponectin and lipid partitioning. J. Clin. Endocrinol. Metab. 90, 3731–3737 (2005)

    Article  CAS  PubMed  Google Scholar 

  10. R. Vukovic, T. Milenkovic, K. Mitrovic et al. Preserved insulin sensitivity predicts metabolically healthy obese phenotype in children and adolescents. Eur. J. Pediatr. 174, 1649–1655 (2015)

    Article  CAS  PubMed  Google Scholar 

  11. D. Weghuber, S. Zelzer, I. Stelzer et al. High risk vs “metabolically healthy” phenotype in juvenile obesity—neck subcutaneous adipose tissue and serum uric acid are clinically relevant. Exp. Clin. Endocrinol. Diabetes 121, 384–390 (2013)

    Article  CAS  PubMed  Google Scholar 

  12. L. Bervoets, G. Massa, Classification and clinical characterization of metabolically “healthy” obese children and adolescents. J. Pediatr. Endocrinol. Metab. 29, 553–560 (2016)

    Article  CAS  PubMed  Google Scholar 

  13. C. Cadenas-Sanchez, J.R. Ruiz, I. Labayen et al. Prevalence of metabolically healthy but overweight/obese phenotype and its association with sedentary time, physical activity, and fitness. J. Adolesc. Heal. 61, 107–114 (2017)

    Article  Google Scholar 

  14. M.L. Evia-Viscarra, R. Guardado-Mendoza. Comparison between metabolically healthy obesity and metabolically unhealthy obesity by different definitions among Mexican children. J. Pediatr. Endocrinol. Metab. 33, 215–222 (2020)

    Article  CAS  PubMed  Google Scholar 

  15. S. Damanhoury, A.S. Newton, M. Rashid et al. Defining metabolically healthy obesity in children: a scoping review. Obes. Rev. 19, 1476–1491 (2018)

    Article  CAS  PubMed  Google Scholar 

  16. F. Magkos, Metabolically healthy obesity: what’s in a name? Am. J. Clin. Nutr. 110, 533–537 (2019)

    Article  PubMed  Google Scholar 

  17. R. Caleyachetty, G.N. Thomas, K.A. Toulis et al. Metabolically healthy obese and incident cardiovascular disease events among 3.5 million men and women. J. Am. Coll. Cardiol. 70, 1429–1437 (2017)

    Article  PubMed  Google Scholar 

  18. M. Blüher, Obesity: the myth of innocent obesity. Nat. Rev. Endocrinol. 13, 691–692 (2017)

    Article  PubMed  Google Scholar 

  19. K.D. Tambalis, D.B. Panagiotakos, G. Arnaoutis et al. Establishing cross-sectional curves for height, weight, body mass index and waist circumference for 4- to 18-year-old Greek children, using the Lambda Mu and Sigma (LMS) statistical method. Hippokratia 19, 239–248 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  20. B. Falkner, S.R. Daniels. Summary of the fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Hypertension 44, 387–388 (2004)

    Article  CAS  PubMed  Google Scholar 

  21. W.A. Marshall, J.M. Tanner, Variations in the pattern of pubertal changes in boys. Arch. Dis. Child 45, 13–23 (1970)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. W.A. Marshall, J.M. Tanner, Variations in pattern of pubertal changes in girls. Arch. Dis. Child 44, 291–303 (1969)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. D.R. Matthews, J.P. Hosker, A.S. Rudenski et al. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419 (1985)

    Article  CAS  PubMed  Google Scholar 

  24. A. Katz, S.S. Nambi, K. Mather et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J. Clin. Endocrinol. Metab. 85, 2402–2410 (2000)

    Article  CAS  PubMed  Google Scholar 

  25. W.T. Friedewald, R.I. Levy, D.S. Fredrickson. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18, 499–502 (1972)

    Article  CAS  PubMed  Google Scholar 

  26. U. Lausten-Thomsen, M. Christiansen, C.E. Fonvig et al. Reference values for serum total adiponectin in healthy non-obese children and adolescents. Clin. Chim. Acta 450, 11–14 (2015)

    Article  CAS  PubMed  Google Scholar 

  27. M.B. Horlick, M. Rosenbaum, M. Nicolson et al. Effect of puberty on the relationship between circulating leptin and body composition. J. Clin. Endocrinol. Metab. 85, 2509–2518 (2000)

    CAS  PubMed  Google Scholar 

  28. D. Taşkesen, B. Kirel, T. Us. Serum visfatin levels, adiposity and glucose metabolism in obese adolescents. J. Clin. Res. Pediatr. Endocrinol. 4, 76–81 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  29. U. Sack, U. Burkhardt, M. Borte et al. Age-dependent levels of select immunological mediators in sera of healthy children. Clin. Diagn. Lab. Immunol. 5, 28–32 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. D. Altman, Sample size, in Practical Statistics for Medical Research (Chapman & Hall, London, 1994), pp. 456–60

  31. G. O’Malley, N. Santoro, V. Northrup et al. High normal fasting glucose level in obese youth: a marker for insulin resistance and beta cell dysregulation. Diabetologia 53, 1199–1209 (2010)

    Article  PubMed  CAS  Google Scholar 

  32. E. Hagman, T. Reinehr, J. Kowalski et al. Impaired fasting glucose prevalence in two nationwide cohorts of obese children and adolescents. Int. J. Obes. 38, 40–45 (2014)

    Article  CAS  Google Scholar 

  33. K.A. Christou, G.A. Christou, A. Karamoutsios et al. Metabolically healthy obesity is characterized by a proinflammatory phenotype of circulating monocyte subsets. Metab. Syndr. Relat. Disord. 17, 259–265 (2019)

    Article  CAS  PubMed  Google Scholar 

  34. S. Genovesi, L. Antolini, A. Orlando, et al. Cardiovascular risk factors associated with the metabolically healthy obese (MHO) phenotype compared to the metabolically unhealthy obese (MUO) phenotype in children. Front. Endocrinol. (Lausanne) 11, 27–35 (2020)

    Article  Google Scholar 

  35. J. Fu, Y. Li, I.C. Esangbedo et al. Circulating osteonectin and adipokine profiles in relation to metabolically healthy obesity in Chinese children: Findings from BCAMS. J. Am. Heart Assoc. 7, e009169 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  36. W. Ding, H. Cheng, F. Chen et al. Adipokines are associated with hypertension in metabolically healthy obese (MHO) children and adolescents: a prospective population-based cohort study. J. Epidemiol. 28, 19–26 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  37. G. Labruna, F. Pasanisi, C. Nardelli, et al. High leptin/adiponectin ratio and serum triglycerides are associated with an at-risk phenotype in young severely obese patients. Obesity (Silver Spring) 19, 1492–1496 (2011)

    Article  CAS  Google Scholar 

  38. I. Aldhoon-Hainerová, H. Zamrazilová, M. Hill et al. Insulin sensitivity and its relation to hormones in adolescent boys and girls. Metabolism 67, 90–98 (2017)

    Article  PubMed  CAS  Google Scholar 

  39. M.B. Vos, S.H. Abrams, S.E. Barlow et al. NASPGHAN clinical practice guideline for the diagnosis and treatment of nonalcoholic fatty liver disease in children: recommendations from the expert committee on NAFLD (ECON) and the North American society of pediatric gastroenterology, hepatology and nutrition (NASPGHAN). J. Pediatr. Gastroenterol. Nutr. 64, 319–334 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  40. Y. Kim, Y. Chang, Y.K. Cho, et al. Metabolically healthy versus unhealthy obesity and risk of fibrosis progression in non-alcoholic fatty liver disease. Liver Int. 39, 1884–1894 (2019)

    Article  CAS  PubMed  Google Scholar 

  41. P.K.C. Selvakumar, M.N. Kabbany, R. Lopez et al. Prevalence and risk factors of nonalcoholic fatty liver disease in metabolically healthy obese adolescents in the United States: an analysis of national health and nutrition examination survey data. J. Hepatol. 66, S587–S588 (2017)

    Google Scholar 

  42. A. Lonardo, A. Mantovani, S. Lugari et al. Epidemiology and pathophysiology of the association between NAFLD and metabolically healthy or metabolically unhealthy obesity. Ann. Hepatol. 19, 359–366 (2020)

    Article  CAS  PubMed  Google Scholar 

  43. M. Blüher, Metabolically healthy obesity. Endocr. Rev. 41, 405–420 (2020)

    Article  Google Scholar 

  44. G. Farello, A. Antenucci, S. Stagi et al. Metabolically healthy and metabolically unhealthy obese children both have increased carotid intima-media thickness: a case control study. BMC Cardiovasc. Disord. 18, 140–146 (2018)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. M. Zhao, A. López-Bermejo, C.A. Caserta et al. Metabolically healthy obesity and high carotid intima-media thickness in children and adolescents: international childhood vascular structure evaluation Consortium. Diabetes Care 42, 119–125 (2019)

    Article  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Child Health Department, School of Health Sciences, Faculty of Medicine, University of Ioannina, Ioannina, Greece

    Anastasios Serbis, Vasilieios Giapros & Ekaterini Siomou

  2. Division of Endocrinology, Diabetes and Metabolism, Department of Clinical Therapeutics, Alexandra Hospital, School of Medicine, National and Kapodistrian University of Athens, Athens, Greece

    Stavroula A. Paschou

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  1. Anastasios Serbis
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  3. Stavroula A. Paschou
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  4. Ekaterini Siomou
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Contributions

VG and AS contributed to the study conception and design. Material preparation and data collection were performed by AS and ES. Data analysis was performed by VG and SP. The first draft of the manuscript was written by AS and VG. ES and SP made substantial contributions to the final version of the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Anastasios Serbis.

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The authors declare no competing interests.

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Approved by the Institutional Scientific Review Board at Ioannina University Hospital.

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Written informed consent and each child’s assent were obtained from all participants and their parents of all groups for participating in the study.

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Written informed consent and each child’s assent were obtained from all participants and their parents of all groups for publishing the study’s results.

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Serbis, A., Giapros, V., Paschou, S.A. et al. Children with metabolically healthy obesity have a worse metabolic profile compared to normal-weight peers: a cross-sectional study. Endocrine 73, 580–587 (2021). https://doi.org/10.1007/s12020-021-02762-6

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  • DOI: https://doi.org/10.1007/s12020-021-02762-6

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