Abstract
Background
A body of literature suggests a metabolically healthy phenotype in individuals with obesity. Despite important clinical implications, the early origins of metabolically healthy obesity (MHO) have received little attention.
Objective
To assess the prevalence of MHO among the Northern Finland Birth Cohort 1966 (NFBC1966) at 31 years of age, examine its determinants in early life taking into account the sex specificity.
Methods
We studied 3205 term-born cohort participants with data available for cardio-metabolic health outcomes at 31 years, and longitudinal height and weight data. After stratifying the population by sex, adult BMI and a strict definition of metabolic health (i.e., no risk factors meaning metabolic health), we obtained six groups. Repeated childhood height and weight measures were used to model early growth and early adiposity phenotypes. We employed marginal means adjusted for mother and child covariates including socio-economic status, birth weight and gestational-age, to compare differences between the groups.
Results
The prevalence of adult MHO was 6% in men and 13.5% in women. Differences in adult metabolic status were linked to alterations in BMI and age at adiposity peak in infancy (p < 0.0003 in men and p = 0.027 in women), and BMI and age at adiposity rebound (AR) (p < 0.0001 irrespective of sex). Compared to MHO, metabolically unhealthy obese (MUO) women were five and a half months younger at AR (p = 0.007) with a higher BMI while MUO men were four months older (p = 0.036) with no difference in BMI at AR.
Conclusion
At the time of AR, MHO women appeared to be older than their MUO counterparts while MHO men were younger. These original results support potential risk factors at the time of adiposity rebound linked to metabolic health in adulthood. These variations by sex warrant independent replication.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
WHO. Media Centre. Obesity and Overweight, Fact sheet No. 311. 2017; http://www.who.int/mediacentre/factsheets/fs311/en/.
Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, et al. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA. 2003;289:76–79.
Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health. 2009;9:88.
Hinnouho GM, Czernichow S, Dugravot A, Batty GD, Kivimaki M, Singh-Manoux A. Metabolically healthy obesity and risk of mortality: does the definition of metabolic health matter? Diabetes Care. 2013;36:2294–2300.
van Vliet-Ostaptchouk JV, Nuotio ML, Slagter SN, Doiron D, Fischer K, Foco L, et al. The prevalence of metabolic syndrome and metabolically healthy obesity in Europe: a collaborative analysis of ten large cohort studies. BMC Endocr Disord. 2014;14:9.
Wildman RP, Muntner P, Reynolds K, McGinn AP, Rajpathak S, Wylie-Rosett J, et al. The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999–2004). Arch Intern Med. 2008;168:1617–24.
Pajunen P, Kotronen A, Korpi-Hyovalti E, Keinanen-Kiukaanniemi S, Oksa H, Niskanen L, et al. Metabolically healthy and unhealthy obesity phenotypes in the general population: the FIN-D2D Survey. BMC Public Health. 2011;11:754.
Phillips CM. Metabolically healthy obesity across the life course: epidemiology, determinants, and implications. Ann N Y Acad Sci. 2017;1391:85–100.
Meigs JB, Wilson PW, Fox CS, Vasan RS, Nathan DM, Sullivan LM, et al. Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab. 2006;91:2906–12.
Hamer M, Stamatakis E. Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality. J Clin Endocrinol Metab. 2012;97:2482–8.
Li S, Chen W, Srinivasan SR, Xu J, Berenson GS. Relation of childhood obesity/cardiometabolic phenotypes to adult cardiometabolic profile: the Bogalusa Heart Study. Am J Epidemiol. 2012;176(Suppl 7):142.
Calori G, Lattuada G, Piemonti L, Garancini MP, Ragogna F, Villa M, et al. Prevalence, metabolic features, and prognosis of metabolically healthy obese Italian individuals: the Cremona Study. Diabetes Care. 2011;34:210–5.
Hinnouho GM, Czernichow S, Dugravot A, Nabi H, Brunner EJ, Kivimaki M, et al. Metabolically healthy obesity and the risk of cardiovascular disease and type 2 diabetes: the Whitehall II cohort study. Eur Heart J. 2015;36:551–9.
Soriguer F, Gutierrez-Repiso C, Rubio-Martin E, Garcia-Fuentes E, Almaraz MC, Colomo N, et al. Metabolically healthy but obese, a matter of time? Findings from the prospective Pizarra study. J Clin Endocrinol Metab. 2013;98:2318–25.
Kuk JL, Ardern CI. Are metabolically normal but obese individuals at lower risk for all-cause mortality? Diabetes Care. 2009;32:2297–9.
Chang Y, Jung HS, Cho J, Zhang Y, Yun KE, Lazo M, et al. Metabolically healthy obesity and the development of nonalcoholic fatty liver disease. Am J Gastroenterol 2016;111:1133–40.
Howe LD, Zimmermann E, Weiss R, Sorensen TI. Do rapid BMI growth in childhood and early-onset obesity offer cardiometabolic protection to obese adults in mid-life? Analysis of a longitudinal cohort study of Danish men. BMJ Open. 2014;4:004827.
Araujo de Franca, GV, Lucia Rolfe E, Horta BL, Gigante DP, Yudkin JS, Ong KK, et al. Associations of birth weight, linear growth and relative weight gain throughout life with abdominal fat depots in adulthood: the 1982 Pelotas (Brazil) birth cohort study. Int J Obes. 2015;40:14–21.
Bouhours-Nouet N, Gatelais F, Dufresne S, Rouleau S, Coutant R. High birth weight and early postnatal weight gain protect obese children and adolescents from truncal adiposity and insulin resistance. Arch Pediatr. 2009;16:573–5.
Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJ. Boys live dangerously in the womb. Am J Hum Biol. 2010;22:330–5.
Jarvelin MR, Sovio U, King V, Lauren L, Xu B, McCarthy MI, et al. Early life factors and blood pressure at age 31 years in the 1966 northern Finland birth cohort. Hypertension. 2004;44:838–46.
Laitinen J, Pietilainen K, Wadsworth M, Sovio U, Jarvelin MR. Predictors of abdominal obesity among 31-y-old men and women born in Northern Finland in 1966. Eur J Clin Nutr. 2004;58:180–90.
WHO collaborating centre for drug statistics methodology. http://www.whocc.no/.
Tammelin T, Nayha S, Rintamaki H, Zitting P. Occupational physical activity is related to physical fitness in young workers. Med Sci Sports Exerc. 2002;34:158–65.
Canoy D, Pekkanen J, Elliott P, Pouta A, Laitinen J, Hartikainen AL, et al. Early growth and adult respiratory function in men and women followed from the fetal period to adulthood. Thorax. 2007;62:396–402.
Taponen S, Martikainen H, Jarvelin MR, Sovio U, Laitinen J, Pouta A, et al. Metabolic cardiovascular disease risk factors in women with self-reported symptoms of oligomenorrhea and/or hirsutism: Northern Finland Birth Cohort 1966 Study. J Clin Endocrinol Metab. 2004;89:2114–8.
Tzoulaki I, Sovio U, Pillas D, Hartikainen AL, Pouta A, Laitinen J, et al. Relation of immediate postnatal growth with obesity and related metabolic risk factors in adulthood: the northern Finland birth cohort 1966 study. Am J Epidemiol. 2010;171:989–98.
Sovio U, Kaakinen M, Tzoulaki I, Das S, Ruokonen A, Pouta A, et al. How do changes in body mass index in infancy and childhood associate with cardiometabolic profile in adulthood? Findings from the Northern Finland Birth Cohort 1966 Study. Int J Obes. 2014;38:53–59.
Sovio U, Bennett AJ, Millwood IY, Molitor J, O’Reilly PF, Timpson NJ, et al. Genetic determinants of height growth assessed longitudinally from infancy to adulthood in the northern Finland birth cohort 1966. PLoS Genet. 2009;5:e1000409.
Morin-Papunen L, Martikainen H, McCarthy MI, Franks S, Sovio U, Hartikainen AL, et al. Comparison of metabolic and inflammatory outcomes in women who used oral contraceptives and the levonorgestrel-releasing intrauterine device in a general population. Am J Obstet Gynecol. 2008;199:529.e10.
Lobstein T, Rigby N, Leach R EU platform on diet, physical activity and health: International Obesity Task Force EU Planning Briefing Paper. 2015. http://ec.europa.eu/health/ph_determinants/life_style/nutrition/documents/iotf_en.pdf.
Velho S, Paccaud F, Waeber G, Vollenweider P, Marques-Vidal P. Metabolically healthy obesity: different prevalences using different criteria. Eur J Clin Nutr. 2010;64:1043–51.
Primeau V, Coderre L, Karelis AD, Brochu M, Lavoie ME, Messier V, et al. Characterizing the profile of obese patients who are metabolically healthy. Int J Obes. 2011;35:971–81.
Vartiainen E, Laatikainen T, Peltonen M, Juolevi A, Mannisto S, Sundvall J, et al. Thirty-five-year trends in cardiovascular risk factors in Finland. Int J Epidemiol. 2010;39:504–18.
Käypä hoito. Update on current care guideline: hypertension. Duodecim. 2014;130:2366–8.
Rolland-Cachera MF, Deheeger M, Bellisle F, Sempe M, Guilloud-Bataille M, Patois E. Adiposity rebound in children: a simple indicator for predicting obesity. Am J Clin Nutr. 1984;39:129–35.
Koyama S, Ichikawa G, Kojima M, Shimura N, Sairenchi T, Arisaka O. Adiposity rebound and the development of metabolic syndrome. Pediatrics. 2014;133:114.
Ohlsson C, Lorentzon M, Norjavaara E, Kindblom JM. Age at adiposity rebound is associated with fat mass in young adult males-the GOOD study. PLoS ONE. 2012;7:e49404.
Hughes AR, Sherriff A, Ness AR, Reilly JJ. Timing of adiposity rebound and adiposity in adolescence. Pediatrics. 2014;134:1354.
Rolland-Cachera MF, Deheeger M, Maillot M, Bellisle F. Early adiposity rebound: causes and consequences for obesity in children and adults. Int J Obesity. 2006;30(Suppl 4):11.
Taylor RW, Grant AM, Goulding A, Williams SM. Early adiposity rebound: review of papers linking this to subsequent obesity in children and adults. Curr Opin Clin Nutr Metab Care. 2005;8:607–12.
Johnson W, Soloway LE, Erickson D, Choh AC, Lee M, Chumlea WC, et al. A changing pattern of childhood BMI growth during the 20th century: 70 y of data from the fels longitudinal study. Am J Clin Nutr. 2012;95:1136–43.
Boonpleng W, Park CG, Gallo AM. Timing of adiposity rebound: a step toward preventing obesity. Pediatr Nurs. 2012;38:37–42.
Williams SM. Weight and height growth rate and the timing of adiposity rebound. Obes Res. 2005;13:1123–30.
Rolland-Cachera MF, Peneau S. Growth trajectories associated with adult obesity. World Rev Nutr Diet. 2013;106:127–34.
Taylor RW, Williams SM, Carter PJ, Goulding A, Gerrard DF, Taylor BJ. Changes in fat mass and fat-free mass during the adiposity rebound: FLAME study. Int J Pediatr Obes. 2011;6:243.
Goossens GH. The metabolic phenotype in obesity: fat mass, body fat distribution, and adipose tissue function. Obes Facts. 2017;10:207–15.
Salonen MK, Kajantie E, Osmond C, Forsen T, Yliharsila H, Paile-Hyvarinen M, et al. Role of childhood growth on the risk of metabolic syndrome in obese men and women. Diabetes Metab. 2009;35:94–100.
Eriksson JG, Osmond C, Kajantie E, Forsen TJ, Barker DJ. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia. 2006;49:2853–8.
Acknowledgements
We thank the late professor Paula Rantakallio (launch of NFBC1966), the participants in the 31yrs study and the NFBC project center. NFBC1966 received financial support from University of Oulu Grant No. 65354, Oulu University Hospital Grant No. 2/97, 8/97, Ministry of Health and Social Affairs Grant no. 23/251/97, 160/97, 190/97, National Institute for Health and Welfare, Helsinki Grant No. 54121, Regional Institute of Occupational Health, Oulu, Finland Grant No. 50621, 54231. This work was supported by Biocenter Oulu, Grant 24002964, EurHealthAgeing, Grant No. 277849, Academy of Finland, Grant 243007961 and DynaHEALTH, Grant No. 633595.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Nedelec, R., Jokelainen, J., Miettunen, J. et al. Early determinants of metabolically healthy obesity in young adults: study of the Northern Finland Birth Cohort 1966. Int J Obes 42, 1704–1714 (2018). https://doi.org/10.1038/s41366-018-0115-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41366-018-0115-0