Synergy Between Adiposity, Insulin Resistance, Metabolic Risk Factors, and Inflammation in Adolescents
Open accessAbstract
OBJECTIVE: The purpose of this study was to investigate relationships between inflammatory markers and components of a metabolic syndrome cluster in adolescents. RESEARCH DESIGN AND METHODS: This was a cross-sectional analysis of an Australian childhood cohort (n = 1,377) aged 14 years. Cluster analysis defined a “high-risk” group similar to adults with metabolic syndrome. Relevant measures were anthropometry, fasting insulin, glucose, lipids, inflammatory markers, liver function, and blood pressure. RESULTS: Of the children, 29% fell into a high-risk metabolic cluster group compared with 2% by a pediatric metabolic syndrome definition. Relative to the “low-risk” cluster, they had higher BMI (95% CI 19.5–19.8 vs. 24.5–25.4), waist circumference (centimeters) (95% CI 71.0–71.8 vs. 83.4–85.8), insulin (units per liter) (95% CI 1.7–1.8 vs. 3.5–3.9), homeostasis model assessment (95% CI 1.7–1.8 vs. 3.5–3.9), systolic blood pressure (millimeters of mercury) (95% CI 110.8–112.1 vs. 116.7–118.9), and triglycerides (millimoles per liter) (95% CI 0.78–0.80 vs. 1.25–1.35) and lower HDL cholesterol (millimoles per liter) (95% CI 1.44–1.48 vs. 1.20–1.26). Inflammatory and liver function markers were higher in the high-risk group: C-reactive protein (CRP) (P < 0.001), uric acid (P < 0.001), alanine aminotransferase (ALT) (P < 0.001), and γ-glutamyl transferase (GGT) (P < 0.001). The highest CRP, GGT, and ALT levels were restricted to overweight children in the high-risk group. CONCLUSIONS: Cluster analysis revealed a strikingly high proportion of 14 year olds at risk of cardiovascular disease–related metabolic disorders. Adiposity and the metabolic syndrome cluster are synergistic in the pathogenesis of inflammation. Systemic and liver inflammation in the high-risk cluster is likely to predict diabetes, cardiovascular disease, and nonalcoholic fatty liver disease.
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Unhealthy eating contributes to obesity and associated health issues among adolescents such as growth retardation, impaired organ development, micronutrient deficiencies, and later in life can lead to non-communicable diseases (NCDs) including cardiovascular diseases, diabetes mellitus, and hypertension.
“Unhealthy eating contributes to obesity and associated health issues among adolescents such as growth retardation, impaired organ development, micronutrient deficiencies, and later in life can lead to non-communicable diseases (NCDs) including cardiovascular diseases, diabetes mellitus, and hypertension [3–7].”
From School-based healthy eating interventions for adolescents aged 10–19 years: an umbrella review (2024) · cites this paper as [6]
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“observed that serum GGT concentrations were elevated in a high metabolic risk overweight group of adolescents (21).”
BackgroundHart, R. J., Doherty, D. A., Mori, T. A., Adams, L. A., Huang, R. C., Minaee, N. S., Handelsman, D. J., McLachlan, R. I., Norman, R. J., Dickinson, J. E., et al. (2018) · Human Reproduction · doi:10.1093/humrep/dey371 · Cited by 31 · see citing works
“This 228 approach was used previously to identify those Raine study participants within a high risk metabolic 229 cluster at 17 years of age (13).”
BackgroundMethodInfluentialSelf-citationOptimisation of a metabotype approach to deliver targeted dietary advice
Hillesheim, E., Ryan, M. F., Gibney, E. R., Roche, H. M., & Brennan, L. (2020) · Nutrition & Metabolism · doi:10.1186/s12986-020-00499-z · Cited by 30 · see citing works
Huang, R., Mori, T. A., & Beilin, L. J. (2012) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2012.05746.x · Cited by 30 · see citing works
“Because there is no consensus as to how to define metabolic syndrome in childhood,(17) the Raine study 8, 14 and 17 year reviews used two-step cluster analysis(18) to define high and low metabolic risk groups.(10,19) Cluster analysis does not apply uncertain arbitrary cut-off points to define metabolic syndrome and ha…”
BackgroundSelf-citationMetabolic syndrome in children with chronic kidney disease and after renal transplantation
Litwin, M., & Niemirska, A. (2013) · Pediatric nephrology (Berlin, West) · doi:10.1007/s00467-013-2500-1 · Cited by 27 · see citing works
“These findings indicate strong synergy between visceral obesity/altered body composition, IR, oxidative stress, and inflammatory activation [22].”
BackgroundBlack, L. J., Burrows, S., Jacoby, P., Oddy, W. H., Beilin, L. J., Ping‐Delfos, W. C. S., Marshall, C. E., Holt, P. G., Hart, P. H., & Mori, T. A. (2014) · British Journal Of Nutrition · doi:10.1017/s000711451400186x · Cited by 29 · see citing works
“Therefore, the remaining cohort is more representative of the general Western Australian population than the original cohort((38,39)).”
BackgroundSelf-citationO’Sullivan, T. A., Lyons‐Wall, P., Bremner, A., Ambrosini, G. L., Huang, R., Beilin, L. J., Mori, T. A., Blair, E. M., & Oddy, W. H. (2010) · Diabetic Medicine · doi:10.1111/j.1464-5491.2010.03021.x · Cited by 27 · see citing works
Self-citationRusso, G. T., Giandalia, A., Romeo, E. L., Alibrandi, A., Horvath, K. V., Asztalos, B. F., & Cucinotta, D. (2014) · International Journal of Endocrinology · doi:10.1155/2014/607924 · Cited by 25 · see citing works
Abdominal fat and metabolic risk in obese children and adolescents
Frauca, J. R., González‐Gil, E. M., Bueno, G., Miguel‐Etayo, P. D., Velasco-Martínez, P., Rey-López, J. P., Lozano, O. B., & Moreno, L. A. (2009) · Journal of Physiology and Biochemistry · doi:10.1007/bf03185937 · Cited by 23 · see citing works
“Accurate and simple methods to assess body composition are required to assess total and abdominal fat ( 6 , 16) Dual energy X-ray absorptiometry (DXA) can be used to assess abdominal and trunkal fat (10).”
MethodPhysical activity, sedentary time, and liver enzymes in adolescents: the HELENA study
; on behalf of the HELENA Study Group, Ruiz, J. R., Labayen, I., Ortega, F. B., Moreno, L. A., Rodrı́guez, G., Breidenassel, C., Μanios, Y., Kafatos, A., Molnár, D., et al. (2014) · Pediatric Research · doi:10.1038/pr.2014.26 · Cited by 23 · see citing works
Louise, S., Warrington, N. M., McCaskie, P. A., Oddy, W. H., Zubrick, S. R., Hands, B. P., Mori, T. A., Briollais, L., Silburn, S., Palmer, L. J., et al. (2012) · Preventive Medicine · doi:10.1016/j.ypmed.2012.03.004 · Cited by 22 · see citing works
“Fasting triglycerides, high-density lipoprotein cholesterol (HDL-C) total cholesterol, insulin and glucose were measured in most children attending (n=1297) at 14 years (Huang et al., 2009).”
BackgroundMethodSelf-citationTian, L., Xu, Y., Fu, M., Peng, T., Liu, Y., & Long, S. (2011) · Lipids in Health and Disease · doi:10.1186/1476-511x-10-17 · Cited by 21 · see citing works
“Some studies indicate that larger HDL2 particles as well as HDL mean particle size are reduced in subjects with low HDL-C [3-7].”
BackgroundPrescott, S. L. (2014) · Allergology International · doi:10.2332/allergolint.13-rai-0659 · Cited by 20 · see citing works
Huang, R., de Klerk, N. H., Mori, T. A., Newnham, J. P., Stanley, F. J., Landau, L. I., Oddy, W. H., Hands, B. P., & Beilin, L. J. (2010) · International Journal of Pediatric Obesity · doi:10.3109/17477166.2010.512388 · Cited by 20 · see citing works
Self-citationApoB48-remnant lipoproteins are associated with increased cardiometabolic risk in adolescents
Krysa, J. A., Vine, D. F., Beilin, L. J., Burrows, S., Huang, R., Mori, T. A., & Proctor, S. D. (2020) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2020.04.021 · Cited by 19 · see citing works
Self-citationUse of the Dietary Guideline Index to assess cardiometabolic risk in adolescents
Ping‐Delfos, W. C. S., Beilin, L. J., Oddy, W. H., Burrows, S., & Mori, T. A. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515001026 · Cited by 18 · see citing works
Self-citationPreeclampsia and cardiovascular disease share genetic risk factors on chromosome 2q22
Løset, M., Johnson, M. P., Melton, P. E., Ang, W., Huang, R., Mori, T. A., Beilin, L. J., Pennell, C. E., Roten, L. T., Iversen, A., et al. (2014) · Pregnancy Hypertension · doi:10.1016/j.preghy.2014.03.005 · Cited by 16 · see citing works
“Serum insulin, glucose, total cholesterol, high density lipoprotein (HDL)-cholesterol, LDL-cholesterol and triglycerides were measured in the PathWest Laboratory at Royal Perth Hospital as described previously [23,24].”
BackgroundMethodSelf-citationKempel, M. K., Winding, T. N., Bøttcher, M., & Andersen, J. H. (2022) · BMC Public Health · doi:10.1186/s12889-022-13158-0 · Cited by 14 · see citing works
“Furthermore, there is an ongoing debate regarding the best way to define measures of cardiometabolic risk in young individuals prior to manifest disease [23, 24].”
BackgroundBerman, Y. E., Doherty, D. A., Mori, T. A., Beilin, L. J., Ayonrinde, O. T., Adams, L. A., Huang, R., Olynyk, J. K., Keelan, J. A., Newnham, J. P., et al. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph192215244 · Cited by 14 · see citing works
Self-citationAssociations of Insulin Resistance and Glycemia With Liver Enzymes in Hispanic/Latino Youths
Parrinello, C. M., Rudolph, B., Lazo, M., Gallo, L. C., Thyagarajan, B., Cotler, S. J., Qi, Q., Seeherunvong, T., Vidot, D. C., Strickler, H. D., et al. (2017) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000946 · Cited by 14 · see citing works
O’Sullivan, T. A., Bremner, A., Mori, T. A., Beilin, L. J., Wilson, C., Hafekost, K., Ambrosini, G. L., Huang, R. C., & Oddy, W. H. (2016) · Nutrients · doi:10.3390/nu8010022 · Cited by 14 · see citing works
“Percentages may not add to 100% if values were missing; p-values for paired t-tests or McNemar tests; NA Test not applicable, or test not valid due to insufficient data; AUD = Australian dollars; BMI = body mass index; CRP = C-reactive protein; LDL = low density lipoprotein; HDL = high density lipoprotein; a The physi…”
BackgroundMethodInfluentialSelf-citationGamma‐glutamyl Transferase Is Strongly Associated With Degree of Overweight and Sex
Wiegand, S., Thamm, M., Kieß, W., Körner, A., Reinehr, T., Krude, H., Hoffmeister, U., Holl, R. W., & APV Study Group and the German Competence Network Adipositas (2011) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181f8417f · Cited by 13 · see citing works
“A cross-sectional analysis of 1377 Australian adolescents revealed an association of liver function markers (ALT, GGT) with C-reactive protein, uric acid, insulin resistance, BMI, and systolic blood pressure, demonstrating a synergy between these metabolic disorders (5).”
BackgroundProtective role of S-Adenosylmethionine against fructose-induced oxidative damage in obesity
Bratoeva, K. Z., Radanova, M. A., Merdzhanova, A., & Donev, I. S. (2017) · Journal of Mind and Medical Sciences · doi:10.22543/7674.42.p163171 · Cited by 13 · see citing works
“of hypertrophic adipose tissue and dysfunction (3).”
Piniewski, B., Codagnone, C., & Osimo, D. (2011) · Joint Research Centre (European Commission) · doi:10.2791/562 · Cited by 12 · see citing works
“0001 [12] • The alarming speed at which the prevalence of paediatric obesity has increased in the last two decades had made it into a recognised public problem[14-18]: – Such trend is linked to clear future Type II diabetes and metabolic syndrome risks [19] – US children born in the year 2000 have a lifetime risk of d…”
BackgroundEnergy drink intake and metabolic syndrome: A prospective investigation in young adults
Trapp, G., Hurworth, M., Jacoby, P. A., Christian, H. E., Ambrosini, G. L., Oddy, W. H., Straker, L. M., Mori, T. A., Beilin, L. J., & Allen, K. L. (2020) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2020.06.012 · Cited by 12 · see citing works
Self-citationAssociations between aggressive behaviour scores and cardiovascular risk factors in childhood
Louise, S., Warrington, N. M., McCaskie, P. A., Oddy, W. H., Zubrick, S. R., Hands, B. P., Mori, T. A., Briollais, L., Silburn, S., Palmer, L. J., et al. (2012) · Pediatric Obesity · doi:10.1111/j.2047-6310.2012.00047.x · Cited by 10 · see citing works
“Briefly, triglycerides and total cholesterol were determined enzymatically on a Cobas MIRA analyzer (Roche Diagnostics, Indianapolis, IN, USA) and HDL-C was determined on a heparin-manganese supernatant (29).”
BackgroundMethodSelf-citationDietary fibre intake and its association with inflammatory markers in adolescents
Swann, O. G., Breslin, M. C., Kilpatrick, M., O’Sullivan, T. A., Mori, T. A., Beilin, L. J., & Oddy, W. H. (2020) · British Journal Of Nutrition · doi:10.1017/s0007114520001609 · Cited by 10 · see citing works
“In our study, we showed that at age 17 years, males had higher intakes of dietary fibre than females, and that females had higher concentrations of hs-CRP, leptin and adiponectin than males, consistent with previous work in this cohort at 14(53) and 17 years(54,55).”
ResultSelf-citationApproach to the Hospitalized Patient with Severe Insulin Resistance
Larsen, J. L., & Goldner, W. S. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0255 · Cited by 8 · see citing works
Serum Uric Acid and Cardiovascular Risk Among Portuguese Adolescents
Gonçalves, J., Ramos, E., Severo, M., Wong, M. C. Y., Ong, K. K., Dunger, D. B., & Lopes, C. M. M. (2015) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2014.11.010 · Cited by 7 · see citing works
Choi, E. J., Lee, H. A., Park, B., Park, B., Kim, H. S., Hong, Y. S., & Park, H. (2021) · Scientific Reports · doi:10.1038/s41598-021-01566-y · Cited by 6 · see citing works
Subjective social status and cardiometabolic risk markers in young adults
Kempel, M. K., Winding, T. N., Bøttcher, M., & Andersen, J. H. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105666 · Cited by 6 · see citing works
“3 suggests a synergistic effect of various biological domains and recommends to incorporate multiple risk markers in the evaluation of early cardiometabolic risk (Huang et al., 2009; Hoogeveen et al., 2020).”
Huang, R., Stanley, F. J., & Beilin, L. J. (2009) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.2009.tb02681.x · Cited by 5 · see citing works
Self-citationZhao, Q., Zhang, R., Liu, S., Luo, C., Qiu, H., Wu, W., Li, H., He, J., Yuan, P., Xu, J., et al. (2025) · Pulmonary Circulation · doi:10.1002/pul2.70210 · Cited by 4 · see citing works
“To minimize order effects, data were randomly reordered before analysis [21 – 23].”
Ralston, R. A., Walker, K. Z., & Truby, H. (2012) · Nutrition & Dietetics · doi:10.1111/j.1747-0080.2012.01603.x · Cited by 4 · see citing works
Gailīte, J., Mikilpa-Mikgelba, A., Siliņa, I., Кириллова, И. А., Lauga-Tuņina, U., Dzīvīte-Krišāne, I., & Gardovska, D. (2018) · Proceedings of the Latvian Academy of Sciences Section B Natural Exact and Applied Sciences · doi:10.2478/prolas-2018-0037 · Cited by 3 · see citing works
“This is important because prevention of childhood obesity reduces the possibility of developing IGT and T2DM ( Maahs et al., 2008; Huang et al., 2009).”
BackgroundChronic hepatitis B infection in a hepatology clinic at a university hospital in Jeddah
Fallatah, H. I., & Akbar, H. O. (2010) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.751 · Cited by 2 · see citing works
“Patients with ultrasound-diagnosed cirrhosis or NAFLD had higher serum ALT and GGT values as compared to those with normal abdominal ultrasounds, which supports the previous data on the value of the use of ALT and GGT as non-invasive biochemical markers in the assessment of the progression of liver disease [40-43].”
ResultYamagiwa, K., Yamamoto, S., Sawada, Y., & Senzaki, A. (1988) · PubMed · Cited by 2 · see citing works
Individual, behavioural and environmental pathways to adolescent obesity
Chivers, P. (2010) · ResearchOnline@ND (The University of Notre Dame) · Cited by 2 · see citing works
Sak, J., Kaboré, J., Kabré, E., Sak, B., & Sawadogo, M. (2012) · African Journal of Biochemistry Research · Cited by 1 · see citing works
The Impact of Infant Feeding on Later Metabolic Health
Oddy, W. H., & McHugh, M. F. (2012) · Humana Press eBooks · doi:10.1007/978-1-62703-224-7_15 · Cited by 1 · see citing works
Self-citationUse of Metabotyping for Targeted Nutrition
Daliri, E. B., Ofosu, F. K., Oh, D., & Lee, B.-H. (2019) · Elsevier eBooks · doi:10.1016/b978-0-08-100596-5.22892-8 · Cited by 1 · see citing works
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Sleep and its association with cardiometabolic risk factors in young adults
Hamidi, A. (2018) · UWA Profiles and Research Repository (University of Western Australia) · doi:10.4225/23/5ad43549ee0cf
“had increased levels of CRP, ALT, GGT and UA irrespective of gender (198) and central obesity appeared to play a central role (199).”
BackgroundMarkers of Non-Fasting Lipids, Remnant Metabolism, and CVD Risk in Youth and Adults
Krysa, J. A. (2019) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3-s941-ec21
Wang, Y. K., & Xu, J. M. (2018) · Biomarkers and Drug Discovery · doi:10.31579/2642-9799/009
“As reported elsewhere blood pressure was measured by trained assessors [30].”
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Kempel, M. K., Winding, T. N., Bøttcher, M., & Jh, A. (2022) · Figshare · doi:10.6084/m9.figshare.19568704
Additional file 1 of Optimisation of a metabotype approach to deliver targeted dietary advice
Hillesheim, E., Ryan, M. F., Gibney, E. R., Roche, H. M., & Brennan, L. (2020) · Figshare · doi:10.6084/m9.figshare.13024197
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- Authors
- Huang, R.-C., Mori, T. A., Burke, V., Newnham, J., Stanley, F. J., Landau, L. I., Kendall, G. E., Oddy, W. H., & Beilin, L. J.
- Affiliations
- The University of Western Australia (AU)
- The Kids Research Institute Australia (AU)
- Corresponding author
- Huang, Rae-Chi
- ORCID
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2009-01-08
- Volume
- 32
- Issue
- 4
- Pages
- 695-701
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- PMC
- PMC2660473
- OpenAlex
- W2116578245
- Cited by
- 93
- References
- 26
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2022: 4 · 2021: 1 · 2020: 7 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 1 · 2015: 7 · 2014: 12 · 2013: 7 · 2012: 13
- FWCI
- 7.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Diabetes Care (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- UWA Profiles and Research Repository (UWA) (publishedVersion, other-oa)
- PubMed (publishedVersion)
- eSpace (Curtin University) (submittedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by-nc-nd)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Obesity, Physical Activity, Diet
- Keywords
- metabolic syndrome, adolescents, adiposity, insulin resistance, inflammation, C-reactive protein, uric acid, alanine aminotransferase, gamma-glutamyl transferase, overweight, cardiovascular risk, metabolic risk factors, clustering, liver function markers, triglycerides, HDL cholesterol, blood pressure, fasting insulin, waist circumference, childhood obesity, dyslipidemia
- MeSH terms
- Adolescent, Alanine Transaminase, Australia, C-Reactive Protein, Cardiovascular Diseases, Cross-Sectional Studies, Female, Humans, Inflammation, Insulin Resistance, Cholesterol, HDL, Male, Metabolic Diseases, Risk Factors, Triglycerides, Uric Acid, Cohort Studies, Cluster Analysis, Risk Assessment, Patient Selection, Overweight
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