Impact of a group-based treatment program on adipocytokines, oxidative status, inflammatory cytokines and arterial stiffness in obese children and adolescents
-
Jeerunda Santiprabhob
, Kawewan Limprayoon
, Prapun Aanpreung , Ratiya Charoensakdi , Ruchaneekorn W. Kalpravidh , Benjaluck Phonrat und Rungsunn Tungtrongchitr
Abstract
Background
Dysregulation of adipocytokines, inflammatory cytokines and oxidative stress are associated with the pathogenesis of obesity-related complications. This study aimed to evaluate the effect of a group-based lifestyle modification program on adipocytokines, inflammatory cytokines, oxidative status and arterial stiffness in obese youth.
Methods
A 1-year weight-reduction program was conducted. The program consisted of initial hospitalization and five outpatient group-based sessions held at 1, 2, 3, 6 and 9 months. Pre- and post-intervention measurements included anthropometric data, blood tests, body composition and brachial-ankle pulse wave velocity (ba-PWV).
Results
A total of 126 obese youths were recruited, and 115 of those completed the study. Twenty-four participants had increased percentage weight for height at the end of the study (group A), 30 had minimal reduction (group B) and 61 had substantial reduction (group C). Lean mass significantly increased in all three groups (all p<0.001). A significant decrease in leptin (group A, p=0.021; group B, p=0.005; group C, p<0.001), interleukin-6 (IL-6) (group A, p=0.019; group B, p=0.004; group C, p<0.001) and ba-PWV (group A, p=0.031; group B, p=0.015; group C, p<0.001) was also observed. No significant change in the oxidative status was found among the groups. Reduction in ba-PWV was correlated with decreases in plasma malondialdehyde (pMDA) (r=0.233, p=0.036) and homeostasis model assessment of insulin resistance (HOMA-IR) (r=0.253, p=0.025).
Conclusions
A group-based healthy lifestyle program for obese youths had beneficial effects on adipocytokines, inflammatory cytokines and arterial stiffness. Participants without change in weight status also benefited. These improvements may reduce the risk of obese youths developing atherosclerosis.
Acknowledgments
The authors gratefully acknowledge the young people and their families who participated in this study. We would also like to thank Dr. Supawadee Likitmaskul, pediatric endocrinologist; Dr. Chanin Leewanun, rehabilitation physician; Mrs. Renu Wongarn, nutritionist; Ms. Pornpimol Kiattisakthavee, diabetes nurse; Ms. Praewvarin Weerakulwattana, researcher; Ms. Sunattra Nunloi, scientist; Mrs. Katharee Chaichanwattanakul, scientist; Ms. Amornrat Pipatsathiant, research assistant; and, Ms. Suwanee Weraviriyapitak, project coordinator for their invaluable support for this study. Finally, we would like to thank Ms. Atchara Suwannakin, rehabilitation nurse, for performing pulse wave velocity measurement, and Dr. Chulaluk Komoltri of the Department of Research and Development, Faculty of Medicine Siriraj Hospital for her assistance with statistical analysis.
Author contributions: JS: Study conception and design, conducting the study, acquisition of data, analysis and interpretation of data, drafting of manuscript. KL, PA: Study conception and design, conducting the study, reviewing the manuscript, final approval of the manuscript. RC: Acquisition, analysis and interpretation of oxidative status data, reviewing the manuscript, final approval of the manuscript. RWK: Study conception and design, analysis and interpretation of oxidative status data, reviewing the manuscript, final approval of the manuscript. BP: Acquisition, analysis, and interpretation of adipocytokines and inflammatory cytokines data, reviewing the manuscript, final approval of the manuscript. RT: Study conception and design, acquisition, analysis and interpretation of adipocytokines and inflammatory cytokines data, reviewing the manuscript, final approval of the manuscript. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: This study was supported by the Siriraj Routine to Research Management Fund (grant no. R2R.031/07).
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 2006;17:4–12.Suche in Google Scholar
2. Hutcheson R, Rocic P. The metabolic syndrome, oxidative stress, environment, and cardiovascular disease: the great exploration. Exp Diabetes Res 2012. doi: 10.1155/2012/271028.10.1155/2012/271028Suche in Google Scholar
3. Koerner A, Kratzsch J, Kiess W. Adipocytokines: leptin – the classical, resistin – the controversical, adiponectin – the promising, and more to come. Best Pract Res Clin Endocrinol Metab 2005;19:525–46.10.1016/j.beem.2005.07.008Suche in Google Scholar
4. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011;11:85–97.10.1038/nri2921Suche in Google Scholar
5. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996;334:292–5.10.1056/NEJM199602013340503Suche in Google Scholar
6. Murdolo G, Nowotny B, Celi F, Donati M, Bini V, et al. Inflammatory adipokines, high molecular weight adiponectin, and insulin resistance: a population-based survey in prepubertal schoolchildren. PLoS One 2011;6:e17264.10.1371/journal.pone.0017264Suche in Google Scholar
7. Xu L, Li M, Yin J, Cheng H, Yu M, et al. Change of body composition and adipokines and their relationship with insulin resistance across pubertal development in obese and nonobese Chinese children: the BCAMS study. Int J Endocrinol 2012. doi: 10.1155/2012/389108.10.1155/2012/389108Suche in Google Scholar
8. Spranger J, Kroke A, Mohlig M, Bergmann MM, Ristow M, et al. Adiponectin and protection against type 2 diabetes mellitus. Lancet 2003;361:226–8.10.1016/S0140-6736(03)12255-6Suche in Google Scholar
9. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. J Am Med Assoc 2001;286:327–34.10.1001/jama.286.3.327Suche in Google Scholar
10. Yudkin JS, Kumari M, Humphries SE, Mohamed-Ali V. Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 2000;148:209–14.10.1016/S0021-9150(99)00463-3Suche in Google Scholar
11. Montero D, Walther G, Perez-Martin A, Roche E, Vinet A. Endothelial dysfunction, inflammation, and oxidative stress in obese children and adolescents: markers and effect of lifestyle intervention. Obes Rev 2012;13:441–55.10.1111/j.1467-789X.2011.00956.xSuche in Google Scholar PubMed
12. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006;440:944–8.10.1038/nature04634Suche in Google Scholar
13. Herouvi D, Karanasios E, Karayianni C, Karavanaki K. Cardiovascular disease in childhood: the role of obesity. Eur J Pediatr 2013;172:721–32.10.1007/s00431-013-1932-8Suche in Google Scholar
14. Cote AT, Harris KC, Panagiotopoulos C, Sandor GG, Devlin AM. Childhood obesity and cardiovascular dysfunction. J Am Coll Cardiol 2013;62:1309–19.10.1016/j.jacc.2013.07.042Suche in Google Scholar
15. Alp H, Eklioglu BS, Atabek ME, Karaarslan S, Baysal T, et al. Evaluation of epicardial adipose tissue, carotid intima- media thickness and ventricular functions in obese children and adolescents. J Pediatr Endocrinol Metab 2014;27: 827–35.10.1515/jpem-2013-0306Suche in Google Scholar
16. Celik N, Cinaz P, Bideci A, Derinkuyu B, Emeksiz HC, et al. Endoglin and obestatin levels, cardiometabolic risk factors and subclinical atherosclerosis in children aged 10–18 years. J Pediatr Endocrinol Metab 2016;29:1173–80.10.1515/jpem-2016-0024Suche in Google Scholar
17. Cote AT, Phillips AA, Harris KC, Sandor GG, Panagiotopoulos C, et al. Obesity and arterial stiffness in children: systematic review and meta-analysis. Arterioscler Thromb Vasc Biol 2015;35:1038–44.10.1161/ATVBAHA.114.305062Suche in Google Scholar
18. Santiprabhob J, Leewanun C, Limprayoon K, Kiattisakthavee P, Wongarn R, et al. Outcomes of group-based treatment program with parental involvement for the management of childhood and adolescent obesity. Patient Educ Couns 2014;97:67–74.10.1016/j.pec.2014.07.002Suche in Google Scholar
19. Tanner JM. Growth and maturation during adolescence. Nutr Rev 1981;39:43–55.10.1111/j.1753-4887.1981.tb06734.xSuche in Google Scholar
20. Winterbourn CC, Hawkins RE, Brian M, Carrell RW. The estimation of red cell superoxide dismutase activity. J Lab Clin Med 1975;85:337–41.Suche in Google Scholar
21. Beutler E. Red cell metabolism: a manual of biochemical methods. London: Grune&Stratton, 1984:74–6.Suche in Google Scholar
22. Agarwal R, Chase SD. Rapid, fluorimetric-liquid chromatographic determination of malondialdehyde in biological samples. J Chromatogr B Analyt Technol Biomed Life Sci 2002; 775:121–6.10.1016/S1570-0232(02)00273-8Suche in Google Scholar
23. Murer SB, Knopfli BH, Aeberli I, Jung A, Wildhaber J, et al. Baseline leptin and leptin reduction predict improvements in metabolic variables and long-term fat loss in obese children and adolescents: a prospective study of an inpatient weight-loss program. Am J Clin Nutr 2011;93:695–702.10.3945/ajcn.110.002212Suche in Google Scholar PubMed
24. Izadpanah A, Barnard RJ, Almeda AJ, Baldwin GC, Bridges SA, et al. A short-term diet and exercise intervention ameliorates inflammation and markers of metabolic health in overweight/obese children. Am J Physiol Endocrinol Metab 2012;303: E542–50.10.1152/ajpendo.00190.2012Suche in Google Scholar PubMed PubMed Central
25. Roth CL, Kratz M, Ralston MM, Reinehr T. Changes in adipose-derived inflammatory cytokines and chemokines after successful lifestyle intervention in obese children. Metabolism 2011;60:445–52.10.1016/j.metabol.2010.03.023Suche in Google Scholar PubMed
26. Cambuli VM, Musiu MC, Incani M, Paderi M, Serpe R, et al. Assessment of adiponectin and leptin as biomarkers of positive metabolic outcomes after lifestyle intervention in overweight and obese children. J Clin Endocrinol Metab 2008;93:3051–7.10.1210/jc.2008-0476Suche in Google Scholar PubMed
27. Utsal L, Tillmann V, Zilmer M, Maestu J, Purge P, et al. Elevated serum IL-6, IL-8, MCP-1, CRP, and IFN-gamma levels in 10- to 11-year-old boys with increased BMI. Horm Res Paediatr 2012;78:31–9.10.1159/000339831Suche in Google Scholar PubMed
28. Galcheva SV, Iotova VM, Yotov YT, Bernasconi S, Street ME. Circulating proinflammatory peptides related to abdominal adiposity and cardiometabolic risk factors in healthy prepubertal children. Eur J Endocrinol 2011;164:553–8.10.1530/EJE-10-1124Suche in Google Scholar PubMed
29. Caminiti C, Armeno M, Mazza CS. Waist-to-height ratio as a marker of low-grade inflammation in obese children and adolescents. J Pediatr Endocrinol Metab 2016;29:543–51.10.1515/jpem-2014-0526Suche in Google Scholar PubMed
30. Lausten-Thomsen U, Gamborg M, Bojsoe C, Hedley PL, Hagen CM, et al. Longitudinal changes in C-reactive protein, proform of eosinophil major basic protein, and pregnancy-associated plasma protein-A during weight changes in obese children. J Pediatr Endocrinol Metab 2015;28:393–8.10.1515/jpem-2014-0249Suche in Google Scholar PubMed
31. Santos MG, Pegoraro M, Sandrini F, Macuco EC. Risk factors for the development of atherosclerosis in childhood and adolescence. Arq Bras Cardiol 2008;90:276–83.10.1590/S0066-782X2008000400012Suche in Google Scholar
32. Balagopal P, George D, Patton N, Yarandi H, Roberts WL, et al. Lifestyle-only intervention attenuates the inflammatory state associated with obesity: a randomized controlled study in adolescents. J Pediatr 2005;146:342–8.10.1016/j.jpeds.2004.11.033Suche in Google Scholar PubMed
33. Reinehr T, Stoffel-Wagner B, Roth CL, Andler W. High-sensitive C-reactive protein, tumor necrosis factor alpha, and cardiovascular risk factors before and after weight loss in obese children. Metabolism 2005;54:1155–61.10.1016/j.metabol.2005.03.022Suche in Google Scholar PubMed
34. Landgraf K, Rockstroh D, Wagner IV, Weise S, Tauscher R, et al. Evidence of early alterations in adipose tissue biology and function and its association with obesity-related inflammation and insulin resistance in children. Diabetes 2015;64: 1249–61.10.2337/db14-0744Suche in Google Scholar PubMed
35. Canas JA, Sweeten S, Balagopal PB. Biomarkers for cardiovascular risk in children. Curr Opin Cardiol 2013;28:103–14.10.1097/HCO.0b013e32835dd0ceSuche in Google Scholar PubMed
36. Mohn A, Catino M, Capanna R, Giannini C, Marcovecchio M, et al. Increased oxidative stress in prepubertal severely obese children: effect of a dietary restriction-weight loss program. J Clin Endocrinol Metab 2005;90:2653–8.10.1210/jc.2004-2178Suche in Google Scholar PubMed
37. Woo J, Shin KO, Yoo JH, Park S, Kang S. The effects of detraining on blood adipokines and antioxidant enzyme in Korean overweight children. Eur J Pediatr 2012;171:235–43.10.1007/s00431-011-1518-2Suche in Google Scholar PubMed
38. Meyer AA, Kundt G, Lenschow U, Schuff-Werner P, Kienast W. Improvement of early vascular changes and cardiovascular risk factors in obese children after a six-month exercise program. J Am Coll Cardiol 2006;48:1865–70.10.1016/j.jacc.2006.07.035Suche in Google Scholar PubMed
39. Woo KS, Chook P, Yu CW, Sung RY, Qiao M, et al. Effects of diet and exercise on obesity-related vascular dysfunction in children. Circulation 2004;109:1981–6.10.1161/01.CIR.0000126599.47470.BESuche in Google Scholar PubMed
40. Maeda S, Miyaki A, Kumagai H, Eto M, So R, et al. Lifestyle modification decreases arterial stiffness and plasma asymmetric dimethylarginine level in overweight and obese men. Coron Artery Dis 2013;24:583–8.10.1097/MCA.0b013e3283647a99Suche in Google Scholar PubMed
41. Hvidt KN, Olsen MH, Ibsen H, Holm JC. Weight reduction and aortic stiffness in obese children and adolescents: a 1-year follow-up study. J Hum Hypertens 2015;29: 535–40.10.1038/jhh.2014.127Suche in Google Scholar PubMed
42. Lee YH, Song YW, Kim HS, Lee SY, Jeong HS, et al. The effects of an exercise program on anthropometric, metabolic, and cardiovascular parameters in obese children. Korean Circ J 2010;40:179–84.10.4070/kcj.2010.40.4.179Suche in Google Scholar PubMed PubMed Central
43. Kim OY, Paik JK, Lee JY, Lee SH, Lee JH. Follow-ups of metabolic, inflammatory and oxidative stress markers, and brachial-ankle pulse wave velocity in middle-aged subjects without metabolic syndrome. Clin Exp Hypertens 2013;35:382–8.10.3109/10641963.2012.739232Suche in Google Scholar PubMed PubMed Central
44. Muniyappa R, Iantorno M, Quon MJ. An integrated view of insulin resistance and endothelial dysfunction. Endocrinol Metab Clin N Am 2008;37:685–711.10.1016/j.ecl.2008.06.001Suche in Google Scholar PubMed PubMed Central
Article note
This work was conducted at the Department of Pediatrics, Faculty of Medicine Siriraj Hospital, Mahidol University 2 Wanglang Road, Bangkoknoi, Bangkok 10700, Thailand. This work was presented at the 55th Annual European Society for Paediatric Endocrinology (ESPE) Meeting, 10–12 September 2016, Paris, France.
©2018 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Review
- Prevalence of cranial MRI findings in girls with central precocious puberty: a systematic review and meta-analysis
- Original Articles
- Can having a sibling with type 1 diabetes cause disordered eating behaviors?
- Wrist circumference as a novel predictor of obesity in children and adolescents: the CASPIAN-IV study
- Evaluation of Mn-superoxide dismutase and catalase gene expression in childhood obesity: its association with insulin resistance
- Impact of a group-based treatment program on adipocytokines, oxidative status, inflammatory cytokines and arterial stiffness in obese children and adolescents
- Clinical management of childhood hyperthyroidism with and without Down syndrome: a longitudinal study at a single center
- Detection of distant metastasis at the time of ablation in children with differentiated thyroid cancer: the value of pre-ablation stimulated thyroglobulin
- Random serum free cortisol and total cortisol measurements in pediatric septic shock
- Self-assessment of pubertal development in a puberty cohort
- Growth, the Mediterranean diet and the buying power of adolescents in Greece
- Clinical and molecular genetic characterization of two patients with mutations in the phosphoglucomutase 1 (PGM1) gene
- Genetic analysis of three families with X-linked dominant hypophosphatemic rickets
- Clinical heterogeneity and molecular profile of triple A syndrome: a study of seven cases
- No central adrenal insufficiency found in patients with Prader-Willi syndrome with an overnight metyrapone test
- Case Reports
- A novel mutation in the proopiomelanocortin (POMC) gene of a Hispanic child: metformin treatment shows a beneficial impact on the body mass index
- Hypertriglyceridemia thalassemia syndrome
- Severe consumptive hypothyroidism caused by multiple infantile hepatic haemangiomas
Artikel in diesem Heft
- Frontmatter
- Review
- Prevalence of cranial MRI findings in girls with central precocious puberty: a systematic review and meta-analysis
- Original Articles
- Can having a sibling with type 1 diabetes cause disordered eating behaviors?
- Wrist circumference as a novel predictor of obesity in children and adolescents: the CASPIAN-IV study
- Evaluation of Mn-superoxide dismutase and catalase gene expression in childhood obesity: its association with insulin resistance
- Impact of a group-based treatment program on adipocytokines, oxidative status, inflammatory cytokines and arterial stiffness in obese children and adolescents
- Clinical management of childhood hyperthyroidism with and without Down syndrome: a longitudinal study at a single center
- Detection of distant metastasis at the time of ablation in children with differentiated thyroid cancer: the value of pre-ablation stimulated thyroglobulin
- Random serum free cortisol and total cortisol measurements in pediatric septic shock
- Self-assessment of pubertal development in a puberty cohort
- Growth, the Mediterranean diet and the buying power of adolescents in Greece
- Clinical and molecular genetic characterization of two patients with mutations in the phosphoglucomutase 1 (PGM1) gene
- Genetic analysis of three families with X-linked dominant hypophosphatemic rickets
- Clinical heterogeneity and molecular profile of triple A syndrome: a study of seven cases
- No central adrenal insufficiency found in patients with Prader-Willi syndrome with an overnight metyrapone test
- Case Reports
- A novel mutation in the proopiomelanocortin (POMC) gene of a Hispanic child: metformin treatment shows a beneficial impact on the body mass index
- Hypertriglyceridemia thalassemia syndrome
- Severe consumptive hypothyroidism caused by multiple infantile hepatic haemangiomas