Consequences of COVID-19 on Pediatric Obesity and Endocrinopathies: A Review of the Literature
Main Article Content
Abstract
The COVID-19 pandemic has impacted children from Kindergarten through 12th grade in numerous ways. Strategies aimed at mitigating the spread of the virus early on, predominately social distancing and isolation, negatively impacted children’s physical health by limiting access to physical education and facilitating sedentary lifestyles. These negative effects have longstanding implications on the physical health of pediatric patients, and it is especially pertinent to understand these effects during an already alarming pediatric obesity epidemic. As with obesity in adults, obesity in children is associated with numerous endocrine co-morbidities. Through a literature review, this paper aims to go beyond understanding how the COVID-19 pandemic negatively impacted the physical health of children and describe how the pandemic may have long-term effects on childhood obesity and endocrinopathies in pediatric patients. Additionally, it describes the direct impact COVID-19 may have on the increased incidence of endocrinopathies in pediatric patients.
Keywords:
COVID-19, Consequences of COVID-19, Pediatric Obesity, Pediatric Obesity and Endocrinopathies, Obesity and Endocrinopathies
Article Details
How to Cite
DELGADO, Amanda M.; COLLINS, Patrice Z.; MACARTHUR, Rodger D..
Consequences of COVID-19 on Pediatric Obesity and Endocrinopathies: A Review of the Literature.
Medical Research Archives, [S.l.], v. 11, n. 5, may 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/3859>. Date accessed: 05 nov. 2024.
doi: https://doi.org/10.18103/mra.v11i5.3859.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Childhood Obesity Facts | Overweight & Obesity | CDC. Accessed April 14, 2023. https://www.cdc.gov/obesity/data/childhood.html#:~:text=Prevalence%20of%20Childhood%20Obesity%20in%20the%20United%20States&text=Obesity%20prevalence%20among%20children%20and,14.7%20million%20children%20and%20adolescents.
2. Barrett CE, Koyama AK, Alvarez P, et al. Risk for Newly Diagnosed Diabetes >30 Days After SARS-CoV-2 Infection Among Persons Aged <18 Years - United States, March 1, 2020-June 28, 2021. MMWR Morb Mortal Wkly Rep. 2022;71(2):59-65. doi:10.15585/mmwr.mm7102e2
3. Rodriguez-Gonzalez M, Castellano-Martinez A, Cascales-Poyatos HM, Perez-Reviriego AA. Cardiovascular impact of COVID-19 with a focus on children: A systematic review. World J Clin Cases. 2020;8(21):5250-5283. doi:10.12998/wjcc.v8.i21.5250
4. Walsh K, Furey WJ, Malhi N. Narrative review: COVID-19 and pediatric anxiety. J Psychiatr Res. 2021;144:421-426. doi:10.1016/j.jpsychires.2021.10.013
5. US Preventive Services Task Force, Grossman DC, Bibbins-Domingo K, et al. Screening for obesity in children and adolescents: US preventive services task force recommendation statement. JAMA. 2017;317(23):2417-2426. doi:10.1001/jama.2017.6803
6. Davison KK, Birch LL. Childhood overweight: a contextual model and recommendations for future research. Obes Rev. 2001;2(3):159-171. doi:10.1046/j.1467-789x.2001.00036.x
7. Picchioni F, Goulao LF, Roberfroid D. The impact of COVID-19 on diet quality, food security and nutrition in low and middle income countries: A systematic review of the evidence. Clin Nutr. 2022;41(12):2955-2964. doi:10.1016/j.clnu.2021.08.015
8. Fang D, Thomsen MR, Nayga RM, Yang W. Food insecurity during the COVID-19 pandemic: evidence from a survey of low-income Americans. Food Sec. 2022;14(1):165-183. doi:10.1007/s12571-021-01189-1
9. Hecht AA, Dunn CG, Kinsey EW, et al. Estimates of the Nutritional Impact of Non-Participation in the National School Lunch Program during COVID-19 School Closures. Nutrients. 2022;14(7). doi:10.3390/nu14071387
10. Pietrobelli A, Pecoraro L, Ferruzzi A, et al. Effects of COVID-19 Lockdown on Lifestyle Behaviors in Children with Obesity Living in Verona, Italy: A Longitudinal Study. Obesity (Silver Spring). 2020;28(8):1382-1385. doi:10.1002/oby.22861
11. Pavlovic A, DeFina LF, Natale BL, et al. Keeping children healthy during and after COVID-19 pandemic: meeting youth physical activity needs. BMC Public Health. 2021;21(1):485. doi:10.1186/s12889-021-10545-x
12. Nathan A, George P, Ng M, et al. Impact of COVID-19 Restrictions on Western Australian Children’s Physical Activity and Screen Time. Int J Environ Res Public Health. 2021;18(5). doi:10.3390/ijerph18052583
13. Castañeda-Babarro A, Arbillaga-Etxarri A, Gutiérrez-Santamaría B, Coca A. Physical Activity Change during COVID-19 Confinement. Int J Environ Res Public Health. 2020;17(18). doi:10.3390/ijerph17186878
14. World Health Organization. WHO Guidelines on Physical Activity and Sedentary Behaviour. World Health Organization; 2020.
15. Lange SJ, Kompaniyets L, Freedman DS, et al. Longitudinal Trends in Body Mass Index Before and During the COVID-19 Pandemic Among Persons Aged 2-19 Years - United States, 2018-2020. MMWR Morb Mortal Wkly Rep. 2021;70(37):1278-1283. doi:10.15585/mmwr.mm7037a3
16. Gnocchi M, D’Alvano T, Lattanzi C, et al. Current evidence on the impact of the COVID-19 pandemic on paediatric endocrine conditions. Front Endocrinol (Lausanne). 2022;13:913334. doi:10.3389/fendo.2022.913334
17. Oliveira Neto CP de, Azulay RS de S, Almeida AGFP de, et al. Differences in Puberty of Girls before and during the COVID-19 Pandemic. Int J Environ Res Public Health. 2022;19(8). doi:10.3390/ijerph19084733
18. Rosenbauer J, Stahl-Pehe A, Schlesinger S, Kuß O. Comments on Rahmati et al., The global impact of COVID-19 pandemic on the incidence of pediatric new-onset type 1 diabetes and ketoacidosis: A systematic review and meta-analysis. J Med Virol. 2022; 1-16 (doi: 10.1002/jmv.27996). J Med Virol. 2023;95(1):e28272. doi:10.1002/jmv.28272
19. Somasundaram NP, Gunatilake SSC. Infections in endocrinology: viruses. In: Feingold KR, Anawalt B, Boyce A, et al., eds. Endotext. MDText.com, Inc.; 2000.
20. Kazakou P, Paschou SA, Psaltopoulou T, et al. Early and late endocrine complications of COVID-19. Endocr Connect. 2021;10(9):R229-R239. doi:10.1530/EC-21-0184
21. Nogueira-de-Almeida CA, Del Ciampo LA, Ferraz IS, Del Ciampo IRL, Contini AA, Ued F da V. COVID-19 and obesity in childhood and adolescence: a clinical review. J Pediatr (Rio J). 2020;96(5):546-558. doi:10.1016/j.jped.2020.07.001
22. Capra ME, Stanyevic B, Giudice A, et al. The Effects of COVID-19 Pandemic and Lockdown on Pediatric Nutritional and Metabolic Diseases: A Narrative Review. Nutrients. 2022;15(1). doi:10.3390/nu15010088
23. Yesiltepe Mutlu G, Eviz E, Haliloglu B, et al. The effects of the covid-19 pandemic on puberty: a cross-sectional, multicenter study from Turkey. Ital J Pediatr. 2022;48(1):144. doi:10.1186/s13052-022-01337-z
24. Alfayez OM, Aldmasi KS, Alruwais NH, et al. Incidence of Diabetic Ketoacidosis Among Pediatrics With Type 1 Diabetes Prior to and During COVID-19 Pandemic: A Meta-Analysis of Observational Studies. Front Endocrinol (Lausanne). 2022;13:856958. doi:10.3389/fendo.2022.856958
25. Peinkhofer M, Bossini B, Penco A, et al. Reduction in pediatric growth hormone deficiency and increase in central precocious puberty diagnoses during COVID 19 pandemics. Ital J Pediatr. 2022;48(1):49. doi:10.1186/s13052-022-01238-1
26. Valitutti F, Zenzeri L, Mauro A, et al. Effect of Population Lockdown on Pediatric Emergency Room Demands in the Era of COVID-19. Front Pediatr. 2020;8:521. doi:10.3389/fped.2020.00521
27. Cheng C-W, Huang Y-B, Chao H-Y, Ng C-J, Chen S-Y. Impact of the COVID-19 Pandemic on Pediatric Emergency Medicine: A Systematic Review. Medicina (Kaunas). 2022;58(8). doi:10.3390/medicina58081112
28. Jacob R, Weiser G, Krupik D, et al. Diabetic Ketoacidosis at Emergency Department Presentation During the First Months of the SARS-CoV-2 Pandemic in Israel: A Multicenter Cross-Sectional Study. Diabetes Ther. 2021;12(5):1569-1574. doi:10.1007/s13300-021-01049-3
29. Alaqeel A, Aljuraibah F, Alsuhaibani M, et al. The Impact of COVID-19 Pandemic Lockdown on the Incidence of New-Onset Type 1 Diabetes and Ketoacidosis Among Saudi Children. Front Endocrinol (Lausanne). 2021;12:669302. doi:10.3389/fendo.2021.669302
30. Danne T, Lanzinger S, de Bock M, et al. A Worldwide Perspective on COVID-19 and Diabetes Management in 22,820 Children from the SWEET Project: Diabetic Ketoacidosis Rates Increase and Glycemic Control Is Maintained. Diabetes Technol Ther. 2021;23(9):632-641. doi:10.1089/dia.2021.0110
31. Health Disparities | DASH | CDC. Accessed March 20, 2023. https://www.cdc.gov/healthyyouth/disparities/index.htm
32. Chung A, Backholer K, Wong E, Palermo C, Keating C, Peeters A. Trends in child and adolescent obesity prevalence in economically advanced countries according to socioeconomic position: a systematic review. Obes Rev. 2016;17(3):276-295. doi:10.1111/obr.12360
33. Haushofer J, Fehr E. On the psychology of poverty. Science. 2014;344(6186):862-867. doi:10.1126/science.1232491
34. Goodman E, Whitaker RC. A prospective study of the role of depression in the development and persistence of adolescent obesity. Pediatrics. 2002;110(3):497-504. doi:10.1542/peds.110.3.497
35. Vliegenthart J, Noppe G, van Rossum EFC, Koper JW, Raat H, van den Akker ELT. Socioeconomic status in children is associated with hair cortisol levels as a biological measure of chronic stress. Psychoneuroendocrinology. 2016;65:9-14. doi:10.1016/j.psyneuen.2015.11.022
36. Drewnowski A. The economics of food choice behavior: why poverty and obesity are linked. Nestle Nutr Inst Workshop Ser. 2012;73:95-112. doi:10.1159/000341303
37. Drewnowski A, Specter SE. Poverty and obesity: the role of energy density and energy costs. Am J Clin Nutr. 2004;79(1):6-16. doi:10.1093/ajcn/79.1.6
38. Gucciardi E, Vahabi M, Norris N, Del Monte JP, Farnum C. The Intersection between Food Insecurity and Diabetes: A Review. Curr Nutr Rep. 2014;3(4):324-332. doi:10.1007/s13668-014-0104-4
39. Jenssen BP, Kelly MK, Powell M, Bouchelle Z, Mayne SL, Fiks AG. COVID-19 and Changes in Child Obesity. Pediatrics. 2021;147(5). doi:10.1542/peds.2021-050123
40. Niessen LW, Mohan D, Akuoku JK, et al. Tackling socioeconomic inequalities and non-communicable diseases in low-income and middle-income countries under the Sustainable Development agenda. Lancet. 2018;391(10134):2036-2046. doi:10.1016/S0140-6736(18)30482-3
41. Hauerslev M, Narang T, Gray N, Samuels TA, Bhutta ZA. Childhood obesity on the rise during COVID-19: A request for global leaders to change the trajectory. Obesity (Silver Spring). 2022;30(2):288-291. doi:10.1002/oby.23307
42. Centers for Disease Control and Prevention (CDC). CDC grand rounds: childhood obesity in the United States. MMWR Morb Mortal Wkly Rep. 2011;60(2):42-46.
43. Rao PV. Type 2 diabetes in children: Clinical aspects and risk factors. Indian J Endocrinol Metab. 2015;19(Suppl 1):S47-50. doi:10.4103/2230-8210.155401
44. Tsikouras P, Spyros L, Manav B, et al. Features of Polycystic Ovary Syndrome in adolescence. J Med Life. 2015;8(3):291-296.
45. Engmann L, Jin S, Sun F, et al. Racial and ethnic differences in the polycystic ovary syndrome metabolic phenotype. Am J Obstet Gynecol. 2017;216(5):493.e1-493.e13. doi:10.1016/j.ajog.2017.01.003
46. Wagner IV, Sabin MA, Pfäffle RW, et al. Effects of obesity on human sexual development. Nat Rev Endocrinol. 2012;8(4):246-254. doi:10.1038/nrendo.2011.241
47. Rutters F, Nieuwenhuizen AG, Verhoef SPM, Lemmens SGT, Vogels N, Westerterp-Plantenga MS. The relationship between leptin, gonadotropic hormones, and body composition during puberty in a Dutch children cohort. Eur J Endocrinol. 2009;160(6):973-978. doi:10.1530/EJE-08-0762
2. Barrett CE, Koyama AK, Alvarez P, et al. Risk for Newly Diagnosed Diabetes >30 Days After SARS-CoV-2 Infection Among Persons Aged <18 Years - United States, March 1, 2020-June 28, 2021. MMWR Morb Mortal Wkly Rep. 2022;71(2):59-65. doi:10.15585/mmwr.mm7102e2
3. Rodriguez-Gonzalez M, Castellano-Martinez A, Cascales-Poyatos HM, Perez-Reviriego AA. Cardiovascular impact of COVID-19 with a focus on children: A systematic review. World J Clin Cases. 2020;8(21):5250-5283. doi:10.12998/wjcc.v8.i21.5250
4. Walsh K, Furey WJ, Malhi N. Narrative review: COVID-19 and pediatric anxiety. J Psychiatr Res. 2021;144:421-426. doi:10.1016/j.jpsychires.2021.10.013
5. US Preventive Services Task Force, Grossman DC, Bibbins-Domingo K, et al. Screening for obesity in children and adolescents: US preventive services task force recommendation statement. JAMA. 2017;317(23):2417-2426. doi:10.1001/jama.2017.6803
6. Davison KK, Birch LL. Childhood overweight: a contextual model and recommendations for future research. Obes Rev. 2001;2(3):159-171. doi:10.1046/j.1467-789x.2001.00036.x
7. Picchioni F, Goulao LF, Roberfroid D. The impact of COVID-19 on diet quality, food security and nutrition in low and middle income countries: A systematic review of the evidence. Clin Nutr. 2022;41(12):2955-2964. doi:10.1016/j.clnu.2021.08.015
8. Fang D, Thomsen MR, Nayga RM, Yang W. Food insecurity during the COVID-19 pandemic: evidence from a survey of low-income Americans. Food Sec. 2022;14(1):165-183. doi:10.1007/s12571-021-01189-1
9. Hecht AA, Dunn CG, Kinsey EW, et al. Estimates of the Nutritional Impact of Non-Participation in the National School Lunch Program during COVID-19 School Closures. Nutrients. 2022;14(7). doi:10.3390/nu14071387
10. Pietrobelli A, Pecoraro L, Ferruzzi A, et al. Effects of COVID-19 Lockdown on Lifestyle Behaviors in Children with Obesity Living in Verona, Italy: A Longitudinal Study. Obesity (Silver Spring). 2020;28(8):1382-1385. doi:10.1002/oby.22861
11. Pavlovic A, DeFina LF, Natale BL, et al. Keeping children healthy during and after COVID-19 pandemic: meeting youth physical activity needs. BMC Public Health. 2021;21(1):485. doi:10.1186/s12889-021-10545-x
12. Nathan A, George P, Ng M, et al. Impact of COVID-19 Restrictions on Western Australian Children’s Physical Activity and Screen Time. Int J Environ Res Public Health. 2021;18(5). doi:10.3390/ijerph18052583
13. Castañeda-Babarro A, Arbillaga-Etxarri A, Gutiérrez-Santamaría B, Coca A. Physical Activity Change during COVID-19 Confinement. Int J Environ Res Public Health. 2020;17(18). doi:10.3390/ijerph17186878
14. World Health Organization. WHO Guidelines on Physical Activity and Sedentary Behaviour. World Health Organization; 2020.
15. Lange SJ, Kompaniyets L, Freedman DS, et al. Longitudinal Trends in Body Mass Index Before and During the COVID-19 Pandemic Among Persons Aged 2-19 Years - United States, 2018-2020. MMWR Morb Mortal Wkly Rep. 2021;70(37):1278-1283. doi:10.15585/mmwr.mm7037a3
16. Gnocchi M, D’Alvano T, Lattanzi C, et al. Current evidence on the impact of the COVID-19 pandemic on paediatric endocrine conditions. Front Endocrinol (Lausanne). 2022;13:913334. doi:10.3389/fendo.2022.913334
17. Oliveira Neto CP de, Azulay RS de S, Almeida AGFP de, et al. Differences in Puberty of Girls before and during the COVID-19 Pandemic. Int J Environ Res Public Health. 2022;19(8). doi:10.3390/ijerph19084733
18. Rosenbauer J, Stahl-Pehe A, Schlesinger S, Kuß O. Comments on Rahmati et al., The global impact of COVID-19 pandemic on the incidence of pediatric new-onset type 1 diabetes and ketoacidosis: A systematic review and meta-analysis. J Med Virol. 2022; 1-16 (doi: 10.1002/jmv.27996). J Med Virol. 2023;95(1):e28272. doi:10.1002/jmv.28272
19. Somasundaram NP, Gunatilake SSC. Infections in endocrinology: viruses. In: Feingold KR, Anawalt B, Boyce A, et al., eds. Endotext. MDText.com, Inc.; 2000.
20. Kazakou P, Paschou SA, Psaltopoulou T, et al. Early and late endocrine complications of COVID-19. Endocr Connect. 2021;10(9):R229-R239. doi:10.1530/EC-21-0184
21. Nogueira-de-Almeida CA, Del Ciampo LA, Ferraz IS, Del Ciampo IRL, Contini AA, Ued F da V. COVID-19 and obesity in childhood and adolescence: a clinical review. J Pediatr (Rio J). 2020;96(5):546-558. doi:10.1016/j.jped.2020.07.001
22. Capra ME, Stanyevic B, Giudice A, et al. The Effects of COVID-19 Pandemic and Lockdown on Pediatric Nutritional and Metabolic Diseases: A Narrative Review. Nutrients. 2022;15(1). doi:10.3390/nu15010088
23. Yesiltepe Mutlu G, Eviz E, Haliloglu B, et al. The effects of the covid-19 pandemic on puberty: a cross-sectional, multicenter study from Turkey. Ital J Pediatr. 2022;48(1):144. doi:10.1186/s13052-022-01337-z
24. Alfayez OM, Aldmasi KS, Alruwais NH, et al. Incidence of Diabetic Ketoacidosis Among Pediatrics With Type 1 Diabetes Prior to and During COVID-19 Pandemic: A Meta-Analysis of Observational Studies. Front Endocrinol (Lausanne). 2022;13:856958. doi:10.3389/fendo.2022.856958
25. Peinkhofer M, Bossini B, Penco A, et al. Reduction in pediatric growth hormone deficiency and increase in central precocious puberty diagnoses during COVID 19 pandemics. Ital J Pediatr. 2022;48(1):49. doi:10.1186/s13052-022-01238-1
26. Valitutti F, Zenzeri L, Mauro A, et al. Effect of Population Lockdown on Pediatric Emergency Room Demands in the Era of COVID-19. Front Pediatr. 2020;8:521. doi:10.3389/fped.2020.00521
27. Cheng C-W, Huang Y-B, Chao H-Y, Ng C-J, Chen S-Y. Impact of the COVID-19 Pandemic on Pediatric Emergency Medicine: A Systematic Review. Medicina (Kaunas). 2022;58(8). doi:10.3390/medicina58081112
28. Jacob R, Weiser G, Krupik D, et al. Diabetic Ketoacidosis at Emergency Department Presentation During the First Months of the SARS-CoV-2 Pandemic in Israel: A Multicenter Cross-Sectional Study. Diabetes Ther. 2021;12(5):1569-1574. doi:10.1007/s13300-021-01049-3
29. Alaqeel A, Aljuraibah F, Alsuhaibani M, et al. The Impact of COVID-19 Pandemic Lockdown on the Incidence of New-Onset Type 1 Diabetes and Ketoacidosis Among Saudi Children. Front Endocrinol (Lausanne). 2021;12:669302. doi:10.3389/fendo.2021.669302
30. Danne T, Lanzinger S, de Bock M, et al. A Worldwide Perspective on COVID-19 and Diabetes Management in 22,820 Children from the SWEET Project: Diabetic Ketoacidosis Rates Increase and Glycemic Control Is Maintained. Diabetes Technol Ther. 2021;23(9):632-641. doi:10.1089/dia.2021.0110
31. Health Disparities | DASH | CDC. Accessed March 20, 2023. https://www.cdc.gov/healthyyouth/disparities/index.htm
32. Chung A, Backholer K, Wong E, Palermo C, Keating C, Peeters A. Trends in child and adolescent obesity prevalence in economically advanced countries according to socioeconomic position: a systematic review. Obes Rev. 2016;17(3):276-295. doi:10.1111/obr.12360
33. Haushofer J, Fehr E. On the psychology of poverty. Science. 2014;344(6186):862-867. doi:10.1126/science.1232491
34. Goodman E, Whitaker RC. A prospective study of the role of depression in the development and persistence of adolescent obesity. Pediatrics. 2002;110(3):497-504. doi:10.1542/peds.110.3.497
35. Vliegenthart J, Noppe G, van Rossum EFC, Koper JW, Raat H, van den Akker ELT. Socioeconomic status in children is associated with hair cortisol levels as a biological measure of chronic stress. Psychoneuroendocrinology. 2016;65:9-14. doi:10.1016/j.psyneuen.2015.11.022
36. Drewnowski A. The economics of food choice behavior: why poverty and obesity are linked. Nestle Nutr Inst Workshop Ser. 2012;73:95-112. doi:10.1159/000341303
37. Drewnowski A, Specter SE. Poverty and obesity: the role of energy density and energy costs. Am J Clin Nutr. 2004;79(1):6-16. doi:10.1093/ajcn/79.1.6
38. Gucciardi E, Vahabi M, Norris N, Del Monte JP, Farnum C. The Intersection between Food Insecurity and Diabetes: A Review. Curr Nutr Rep. 2014;3(4):324-332. doi:10.1007/s13668-014-0104-4
39. Jenssen BP, Kelly MK, Powell M, Bouchelle Z, Mayne SL, Fiks AG. COVID-19 and Changes in Child Obesity. Pediatrics. 2021;147(5). doi:10.1542/peds.2021-050123
40. Niessen LW, Mohan D, Akuoku JK, et al. Tackling socioeconomic inequalities and non-communicable diseases in low-income and middle-income countries under the Sustainable Development agenda. Lancet. 2018;391(10134):2036-2046. doi:10.1016/S0140-6736(18)30482-3
41. Hauerslev M, Narang T, Gray N, Samuels TA, Bhutta ZA. Childhood obesity on the rise during COVID-19: A request for global leaders to change the trajectory. Obesity (Silver Spring). 2022;30(2):288-291. doi:10.1002/oby.23307
42. Centers for Disease Control and Prevention (CDC). CDC grand rounds: childhood obesity in the United States. MMWR Morb Mortal Wkly Rep. 2011;60(2):42-46.
43. Rao PV. Type 2 diabetes in children: Clinical aspects and risk factors. Indian J Endocrinol Metab. 2015;19(Suppl 1):S47-50. doi:10.4103/2230-8210.155401
44. Tsikouras P, Spyros L, Manav B, et al. Features of Polycystic Ovary Syndrome in adolescence. J Med Life. 2015;8(3):291-296.
45. Engmann L, Jin S, Sun F, et al. Racial and ethnic differences in the polycystic ovary syndrome metabolic phenotype. Am J Obstet Gynecol. 2017;216(5):493.e1-493.e13. doi:10.1016/j.ajog.2017.01.003
46. Wagner IV, Sabin MA, Pfäffle RW, et al. Effects of obesity on human sexual development. Nat Rev Endocrinol. 2012;8(4):246-254. doi:10.1038/nrendo.2011.241
47. Rutters F, Nieuwenhuizen AG, Verhoef SPM, Lemmens SGT, Vogels N, Westerterp-Plantenga MS. The relationship between leptin, gonadotropic hormones, and body composition during puberty in a Dutch children cohort. Eur J Endocrinol. 2009;160(6):973-978. doi:10.1530/EJE-08-0762