BACKGROUND: The effect of fat tissue on a developing individual is fundamentally different from the effect on an adult. Several changes caused by obesity during sexual maturation have an irreversible and severe negative effect (lower fertility, reduced final height, type 2 diabetes mellitus) even for those who have subsequently lost weight. Our study was focused on monitoring the skeletal structure substantially influenced by sex hormones-the pelvis. The adult pelvis is strongly sexually dimorphic, which is not the case for the juvenile pelvis; skeletal differences between sexes are not so prominent and start to manifest with the onset of puberty. Evidence from animal models and case studies of treatment of gender dysphoria suggests that estrogens have a stimulatory effect on the growth plates present on the pelvis, leading to morphological change. Male obesity, especially in puberty, is connected with hypogonadism, manifesting in low levels of testosterone, and high levels of estrogens. The goal of our study was to evaluate the influence of obesity during adolescence on the morphology of the adult pelvis in the context of androgen and estrogen status. SAMPLE AND METHODS: Our sample consists of 238 individuals (144 females, 94 males) observed after an 8 year follow-up (mean age during enrollment 15.2 years, follow-up 23.3 years). Anthropometry and body composition using bioimpedance analysis (BIA) were obtained. During the follow-up, saliva samples from male participants were also collected to estimate testosterone and estradiol levels using the salivary ELISA kit (Salimetrics LLC, State College, PA, USA). RESULTS: The body fat (percentage of body fat estimated using BIA) was strongly positively associated with relative pelvic breadths in adulthood (males r = 0.64; females r = 0.56, both with p < 0.001). Adulthood pelvic breadth was a highly sensitive (0.81) and specific (0.74) retrospective marker of obesity during adolescence. The complex regression model (with reduction of dimensionality) including testosterone, estradiol to testosterone ratio and body fat (adolescent and adulthood) was able to describe 54.8% variability of pelvic breadth among males. DISCUSSION: We observed that adults with a history of obesity from adolescence tend to have a wider dimension of the bony pelvis in adulthood. Based on the parameters of the adult pelvis, the history of obesity can be determined with satisfactory sensitivity and specificity (<70%). One of the explanations for this observation can be the influence of relatively elevated estrogens levels connected with excessive adiposity leading to a wider pelvis. However, the biomechanical stress connected with elevated body mass also has to be considered, as does the influence of physical activity and gait pattern on the skeletal build.

Department of Anthropology and Human Genetics Faculty of Science Charles University Prague Czech Republic

Institute of Endocrinology Prague Czech Republic

Zobrazit více v PubMed

Agarwal VR, Ashanullah CI, Simpson ER, Bulun SE. Alternatively spliced transcripts of the Aromatase Cytochrome P450 (CYP19) gene in adipose tissue of women. Journal of Clinical Endocrinology & Metabolism. 1997;82(1):70–74. doi: 10.1210/jcem.82.1.3655. PubMed DOI

Agostini GM, Ross AH. The effect of weight on the femur: a cross-sectional analysis. Journal of Forensic Sciences. 2011;56(2):339–343. doi: 10.1111/j.1556-4029.2010.01648.x. PubMed DOI

Al-Hazzaa HM. Prevalence and trends in obesity among school boys in Central Saudi Arabia between 1988 and 2005. Saudi Medical Journal. 2007;28:1569–1574. PubMed

Ayer J, Charakida M, Deanfield JE, Celermajer DS. Lifetime risk: childhood obesity and cardiovascular risk. European Heart Journal. 2015;36(22):1371–1376. doi: 10.1093/eurheartj/ehv089. PubMed DOI

Berthrong M, Goodwin WE, Scott WW. Estrogen production by the testis. Journal of Clinical Endocrinology & Metabolism. 1949;9(7):579–592. doi: 10.1210/jcem-9-7-579. PubMed DOI

Box GEP, Cox DR. An analysis of transformations. Journal of the Royal Statistical Society: Series B (Methodological) 1964;26(2):211–243. doi: 10.1111/j.2517-6161.1964.tb00553.x. DOI

Brambilla DJ, Matsumoto AM, Araujo AB, McKinlay JB. The effect of diurnal variation on clinical measurement of serum testosterone and other sex hormone levels in men. The Journal of Clinical Endocrinology & Metabolism. 2009;94:907–913. doi: 10.1210/jc.2008-1902. PubMed DOI PMC

Brener A, Bello R, Lebenthal Y, Yackobovitch-Gavan M, Phillip M, Shalitin S. The impact of adolescent obesity on adult height. Hormone Research in Paediatrics. 2017;88(3–4):237–243. doi: 10.1159/000478697. PubMed DOI

Cleveland WS. Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association. 1979;74(368):829–836. doi: 10.1080/01621459.1979.10481038. DOI

Cohen P. Obesity in men: the hypogonadal–estrogen receptor relationship and its effect on glucose homeostasis. Medical Hypotheses. 2007;70(2):358–360. doi: 10.1016/j.mehy.2007.05.020. PubMed DOI

Cole TJ. The LMS method for constructing normalized growth standards. European Journal of Clinical Nutrition. 1990;44:45–60. PubMed

Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. British Medical Journal. 2000;320(7244):1240–1240. doi: 10.1136/bmj.320.7244.1240. PubMed DOI PMC

Coleman WH. Sex differences in the growth of the human bony pelvis. American Journal of Physical Anthropology. 1969;31(2):125–151. doi: 10.1002/ajpa.1330310202. PubMed DOI

De Leonibus C, Marcovecchio ML, Chiarelli F. Update on statural growth and pubertal development in obese children. Pediatric Reports. 2012;4(4):35. doi: 10.4081/pr.2012.e35. PubMed DOI PMC

De Ridder CM, Zonderland ML, Thijssen JHH, Bruning PF, Barth A, Steenbruggen A, Erich WBM. The onset of puberty and the availability of sex steroids in female gymnasts. American Journal of Human Biology. 1993;5(3):251–257. doi: 10.1002/ajhb.1310050302. PubMed DOI

Devlin MJ. Estrogen, exercise, and the skeleton. Evolutionary Anthropology: Issues, News, and Reviews. 2011;20(2):54–61. doi: 10.1002/evan.20299. PubMed DOI

Dimitri P. The impact of childhood obesity on skeletal health and development. Journal of Obesity & Metabolic Syndrome. 2019;28(1):4–17. doi: 10.7570/jomes.2019.28.1.4. PubMed DOI PMC

Eston RG, Reilly T. Kinanthropometry and exercise physiology laboratory manual: tests, procedures and data. Abingdon: Routledge; 2009.

Farr JN, Dimitri P. The impact of fat and obesity on bone microarchitecture and strength in children. Calcified Tissue International. 2017;100(5):500–513. doi: 10.1007/s00223-016-0218-3. PubMed DOI PMC

Fawcett T. An introduction to ROC analysis. Pattern Recognition Letters. 2006;27(8):861–874. doi: 10.1016/j.patrec.2005.10.010. DOI

Fejes I, Koloszár S, Závaczki Z, Daru J, Szöllösi J, Pál A. Effect of body weight on testosterone/estradiol ratio in oligozoospermic patients. Archives of Andrology. 2006;52(2):97–102. doi: 10.1080/01485010500315479. PubMed DOI

Frost HM. The Utah paradigm of skeletal physiology: an overview of its insights for bone, cartilage and collagenous tissue organs. Journal of Bone and Mineral Metabolism. 2000;18(6):305–316. doi: 10.1007/s007740070001. PubMed DOI

Gettler LT, McDade TW, Feranil AB, Agustin SS, Kuzawa CW. Salivary estradiol and testosterone in Filipino men: diurnal patterns and relationships with adiposity. American Journal of Human Biology. 2014;26(3):376–383. doi: 10.1002/ajhb.22528. PubMed DOI

Goyal P. Association of age at menarche with anthropometric measures in Punjabi Bania girls. Journal Of Clinical And Diagnostic Research. 2016;10(11):IC01–IC05. doi: 10.7860/JCDR/2016/22205.8796. PubMed DOI PMC

Grantham JP, Henneberg M. The estrogen hypothesis of obesity. PLOS ONE. 2014;9(6):e99776. doi: 10.1371/journal.pone.0099776. PubMed DOI PMC

Harrington KI, Wescott DJ. Size and shape differences in the distal femur and proximal tibia between normal weight and obese American whites. Journal of Forensic Sciences. 2015;60(Suppl. 54):S32–S38. doi: 10.1111/1556-4029.12579. PubMed DOI

He Y, Tian J, Oddy WH, Dwyer T, Venn AJ. Association of childhood obesity with female infertility in adulthood: a 25-year follow-up study. Fertility and Sterility. 2018;110(4):596–604. doi: 10.1016/j.fertnstert.2018.05.011. PubMed DOI

Hills AP, Parker AW. Gait characteristics of obese children. Archives of Physical Medicine and Rehabilitation. 1991;72:403–407. doi: 10.5555/uri:pii:000399939190175I. PubMed DOI

Hughes PC, Tanner JM. The effect of a single neonatal sex hormone injection on the growth of the rat pelvis. Acta Endocrinologica. 1974;77(3):612–624. doi: 10.1530/acta.0.0770612. PubMed DOI

Huseynov A, Zollikofer CPE, Coudyzer W, Gascho D, Kellenberger C, Hinzpeter R, Ponce De León MS. Developmental evidence for obstetric adaptation of the human female pelvis. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(19):5227–5232. doi: 10.1073/pnas.1517085113. PubMed DOI PMC

Ikoma E, Kanda S, Nakata S, Wada Y, Yamazaki K. Quantitative genetic analysis of Bi-lliac breadth. American Journal of Physical Anthropology. 1988;77(3):295–301. doi: 10.1002/ajpa.1330770303. PubMed DOI

Iyengar NM, Brown KA, Zhou XK, Gucalp A, Subbaramaiah K, Giri DD, Zahid H, Bhardwaj P, Wendel NK, Falcone DJ, Wang H, Williams S, Pollak M, Morrow M, Hudis CA, Dannenberg AJ. Metabolic obesity, adipose inflammation and elevated breast aromatase in women with normal body mass index. Cancer Prevention Research. 2017;10(4):235–243. doi: 10.1158/1940-6207.CAPR-16-0314. PubMed DOI PMC

Kelly DM, Jones TH. Testosterone and obesity. Obesity Reviews. 2015;16(7):581–606. doi: 10.1111/obr.12282. PubMed DOI

Kirchengast S, Hartmann B. The impact of the age at menarche on body build and sex hormone levels in healthy adult women from Vienna, Austria. Anthropologie (1962–2002) 1994;32(3):205–214.

Ko S, Stenholm S, Ferrucci L. Characteristic gait patterns in older adults with obesity—results from the Baltimore longitudinal study of aging. Journal of Biomechanics. 2010;43(6):1104–1110. doi: 10.1016/j.jbiomech.2009.12.004. PubMed DOI PMC

Kobzová J, Vignerová J, Bláha P, Krejcovský L, Riedlová J. The 6th nationwide anthropological survey of children and adolescents in the Czech Republic in 2001. Central European Journal of Public Health. 2004;12:126–130. PubMed

Labrie F, Bélanger A, Pelletier G, Martel C, Archer DF, Utian WH. Science of intracrinology in postmenopausal women. Menopause. 2017;24(6):702–712. doi: 10.1097/GME.0000000000000808. PubMed DOI

Lean ME. Pathophysiology of obesity. Proceedings of the Nutrition Society. 2000;59(3):331–336. doi: 10.1017/S0029665100000379. PubMed DOI

Li W, Liu Q, Deng X, Chen Y, Liu S, Story M. Association between obesity and puberty timing: a systematic review and meta-analysis. International Journal of Environmental Research and Public Health. 2017;14(10):1266. doi: 10.3390/ijerph14101266. PubMed DOI PMC

Lorkiewicz-Muszyńska D, Przystańska A, Kociemba W, Sroka A, Rewekant A, Żaba C, Paprzycki W. Body mass estimation in modern population using anthropometric measurements from computed tomography. Forensic Science International. 2013;231(1–3):405.e1–405.e6. doi: 10.1016/j.forsciint.2013.05.017. PubMed DOI

Martin R, Saller K. Lehrbuch der Anthropologie, in systematischer Darstellung. Stuttgart: Fischer; 1957.

Meeuwsen S, Horgan GW, Elia M. The relationship between BMI and percent body fat, measured by bioelectrical impedance, in a large adult sample is curvilinear and influenced by age and sex. Clinical Nutrition. 2010;29(5):560–566. doi: 10.1016/j.clnu.2009.12.011. PubMed DOI

Meloun M, Hill M, Militký J, Kupka K. Transformation in the PC-aided biochemical data analysis. Clinical Chemistry and Laboratory Medicine. 2000;38(6):553–559. doi: 10.1515/CCLM.2000.081. PubMed DOI

Must A, Anderson SE. Body mass index in children and adolescents: considerations for population-based applications. International Journal of Obesity. 2006;30(4):590–594. doi: 10.1038/sj.ijo.0803300. PubMed DOI

Must A, Jacques PF, Dallal GE, Bajema CJ, Dietz WH. Long-term morbidity and mortality of overweight adolescents: a follow-up of the Harvard growth study of 1922 to 1935. New England Journal of Medicine. 1992;327(19):1350–1355. doi: 10.1056/NEJM199211053271904. PubMed DOI

Parizkova J. Activity, obesity, and growth. Monographs of the Society for Research in Child Development. 1970;35(7):28. doi: 10.2307/1165810. PubMed DOI

Polari L, Yatkin E, Martínez Chacón MG, Ahotupa M, Smeds A, Strauss L, Zhang F, Poutanen M, Saarinen N, Mäkelä SI. Weight gain and inflammation regulate aromatase expression in male adipose tissue, as evidenced by reporter gene activity. Molecular and Cellular Endocrinology. 2015;412:123–130. doi: 10.1016/j.mce.2015.06.002. PubMed DOI

Polotsky AJ, Hailpern SM, Skurnick JH, J.C. LO, Sternfeld B, Santoro N. Association of adolescent obesity and lifetime nulliparity—SWAN, the study of women’s health across the nation. Fertility and Sterility. 2010;93(6):2004–2011. doi: 10.1016/j.fertnstert.2008.12.059. PubMed DOI PMC

R Development Core Team . R: a language and environment for statistical computing. Vienna: The R Foundation for Statistical Computing; 2018.

Redinger RN. The pathophysiology of obesity and its clinical manifestations. Gastroenterology & Hepatology. 2007;3:856–863. PubMed PMC

Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez J-C, Müller M. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12(1):77. doi: 10.1186/1471-2105-12-77. PubMed DOI PMC

Ruff CB. Body mass prediction from skeletal frame size in elite athletes. American Journal of Physical Anthropology. 2000;113:507–517. doi: 10.1002/1096-8644(200012)113:4<507::AID-AJPA5>3.0.CO;2-F. PubMed DOI

Ruff CB, Trinkaus E, Holliday TW. Body mass and encephalization in Pleistocene Homo. Nature. 1997;387(6629):173–176. doi: 10.1038/387173a0. PubMed DOI

Savitzky A, Golay MJE. Smoothing and differentiation of data by simplified least squares procedures. Analytical Chemistry. 1964;36(8):1627–1639. doi: 10.1021/ac60214a047. DOI

Schulster M, Bernie AM, Ramasamy R. The role of estradiol in male reproductive function. Asian Journal of Andrology. 2016;18(3):435–440. doi: 10.4103/1008-682X.173932. PubMed DOI PMC

Simpson ER. Sources of estrogen and their importance. Journal of Steroid Biochemistry and Molecular Biology. 2003;86(3–5):225–230. doi: 10.1016/S0960-0760(03)00360-1. PubMed DOI

Stocco C. Tissue physiology and pathology of aromatase. Steroids. 2012;77(1–2):27–35. doi: 10.1016/j.steroids.2011.10.013. PubMed DOI PMC

Taylor VH, MacQueen GM. The role of adipokines in understanding the associations between obesity and depression. Journal of Obesity. 2010;2010(8):1–6. doi: 10.1155/2010/748048. PubMed DOI PMC

Trygg J, Wold S. Orthogonal projections to latent structures (O-PLS) Journal of Chemometrics. 2002;16(3):119–128. doi: 10.1002/cem.695. DOI

Vajargah KF, Sadeghi-Bazargani H, Mehdizadeh-Esfanjani R, Savadi-Oskouei D, Farhoudi M. OPLS statistical model versus linear regression to assess sonographic predictors of stroke prognosis. Neuropsychiatric Disease and Treatment. 2012;8:387–392. doi: 10.2147/NDT.S33991. PubMed DOI PMC

Wagner IV, Sabin MA, Pfäffle RW, Hiemisch A, Sergeyev E, Körner A, Kiess W. Effects of obesity on human sexual development. Nature Reviews Endocrinology. 2012;8(4):246–254. doi: 10.1038/nrendo.2011.241. PubMed DOI

Weise M, De-Levi S, Barnes KM, Gafni RI, Abad V, Baron J. Effects of estrogen on growth plate senescence and epiphyseal fusion. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(12):6871–6876. doi: 10.1073/pnas.121180498. PubMed DOI PMC

WHO Obesity and overweight—factsheet. 2018. https://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight. [24 September 2019]. https://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight

Wickham H. Ggplot2: elegant graphics for data analysis. New York: Springer; 2009.

Wickham H. tidyverse: Easily install and load the “Tidyverse”. 2017. https://CRAN.R-project.org/package=tidyverse https://CRAN.R-project.org/package=tidyverse

Witchel SF. Management of CAH during pregnancy: optimizing outcomes. Current Opinion in Endocrinology, Diabetes, and Obesity. 2012;19(6):489–496. doi: 10.1097/MED.0b013e32835a1a2e. PubMed DOI

Woronkowicz A, Kryst Ł., Kowal M, Brudecki J, Sobiecki J. Long-term changes in body proportions since 1983 to 2010 in children and adolescents from Kraków (Poland) Anthropologischer Anzeiger. 2016;73(2):125–143. doi: 10.1127/anthranz/2016/0578. PubMed DOI

Youden WJ. Index for rating diagnostic tests. Cancer. 1950;3:32–35. doi: 10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3. PubMed DOI

Zhang Y, Wang S. Secular trends in growth and body proportion among children and adolescents from 1985 to 2005 in Shandong. China Anthropological Science. 2009;117(2):69–76. doi: 10.1537/ase.080520. DOI

Ziomkiewicz A, Ellison PT, Lipson SF, Thune I, Jasienska G. Body fat, energy balance and estradiol levels: a study based on hormonal profiles from complete menstrual cycles. Human Reproduction. 2008;23(11):2555–2563. doi: 10.1093/humrep/den213. PubMed DOI

Influence of COVID-19-Related Restrictions on the Prevalence of Overweight and Obese Czech Children