Percent Body Fat-Related Disparities of Serum Ferritin on the Risk of Lipid Metabolism Abnormalities in Children and Adolescents
Abstract
:1. Introduction
2. Method
2.1. Study Population
2.2. Anthropometric and Biochemical Measurements
2.3. Definition of Dyslipidemia
2.4. Potential Confounders
2.5. Statistical Analysis
3. Results
3.1. Characteristics of Participants
3.2. Associations of Ferritin Quartiles with Dyslipidemia among Different PBF Categories
3.3. Relationship between Ferritin and Lipid Abnormalities Profiles among Different PBF Categories
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Pirillo, A.; Casula, M.; Olmastroni, E.; Norata, G.D.; Catapano, A.L. Global epidemiology of dyslipidaemias. Nat. Rev. Cardiol. 2021, 18, 689–700. [Google Scholar] [CrossRef]
- Yandrapalli, S.; Nabors, C.; Goyal, A.; Aronow, W.S.; Frishman, W.H. Modifiable Risk Factors in Young Adults With First Myocardial Infarction. J. Am. Coll. Cardiol. 2019, 73, 573–584. [Google Scholar] [CrossRef]
- Kavey, R.-E.W.; Daniels, S.R.; Lauer, R.M.; Atkins, D.L.; Hayman, L.L.; Taubert, K. American Heart Association Guidelines for Primary Prevention of Atherosclerotic Cardiovascular Disease Beginning in Childhood. Circulation 2003, 107, 1562–1566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, H.; Yu, Y.-Q.; Li, Y.; Kou, C.-G.; Li, B.; Tao, Y.-C.; Zhen, Q.; Wang, C.; Kanu, J.S.; Huang, X.-F.; et al. Dyslipidemia awareness, treatment, control and influence factors among adults in the Jilin province in China: A cross-sectional study. Lipids Health Dis. 2014, 13, 122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, J.-R.; Gao, R.-L.; Zhao, S.-P.; Lu, G.-P.; Zhao, D.; Li, J.-J. 2016 Chinese guidelines for the management of dyslipidemia in adults. J. Geriatr. Cardiol. 2018, 15, 1. [Google Scholar] [CrossRef]
- Xiao, P.; Huang, T.; Yan, Y.; Zhao, X.; Li, H.; Mi, J. Performance of gender- and age-specific cut-points versus NCEP pediatric cutpoints in dyslipidemia screening among Chinese children. Atherosclerosis 2019, 280, 37–44. [Google Scholar] [CrossRef] [PubMed]
- Gazzola, K.; Reeskamp, L.; van den Born, B.-J. Ethnicity, lipids and cardiovascular disease. Curr. Opin. Lipidol. 2017, 28, 225–230. [Google Scholar] [CrossRef]
- Eslami, A.; Mozaffary, A.; Derakhshan, A.; Azizi, F.; Khalili, D.; Hadaegh, F. Sex-specific incidence rates and risk factors of premature cardiovascular disease. A long term follow up of the Tehran Lipid and Glucose Study. Int. J. Cardiol. 2017, 227, 826–832. [Google Scholar] [CrossRef]
- Besarab, A.; Drueke, T.B. The problem with transferrin saturation as an indicator of iron ‘sufficiency’ in chronic kidney disease. Nephrol. Dial. Transplant. 2020, 36, 1377–1383. [Google Scholar] [CrossRef]
- Lipschitz, D.A.; Cook, J.D.; Finch, C.A. A Clinical Evaluation of Serum Ferritin as an Index of Iron Stores. N. Engl. J. Med. 1974, 290, 1213–1216. [Google Scholar] [CrossRef]
- Shim, Y.S.; Kang, M.J.; Oh, Y.J.; Baek, J.W.; Yang, S.; Hwang, I.T. Association of serum ferritin with insulin resistance, abdominal obesity, and metabolic syndrome in Korean adolescent and adults: The Korean National Health and Nutrition Examination Survey, 2008 to 2011. Medicine 2017, 96, e6179. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Bao, W.; Zhang, T.; Zhou, Y.; Yang, H.; Jia, H.; Wang, R.; Cao, Y.; Xiao, C. Independent relationship between serum ferritin levels and dyslipidemia in Chinese adults: A population study. PLoS ONE 2017, 12, e0190310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, B.; Ren, H.; Zhou, X.; Yuan, G. Associations of iron status with apolipoproteins and lipid ratios: A cross-sectional study from the China Health and Nutrition Survey. Lipids Health Dis. 2020, 19, 140. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.K.; Baek, K.H.; Song, K.-H.; Kang, M.I.; Choi, J.H.; Bae, J.C.; Park, C.Y.; Lee, W.Y.; Oh, K.W. Increased serum ferritin predicts the development of hypertension among middle-aged men. Am. J. Hypertens. 2012, 25, 492–497. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, L.; Wang, K.; Lo, K.; Zhong, Y.; Yang, A.; Fang, X.; Akezhuoli, H.; Song, Z.; Chen, L.; An, P.; et al. Sex-Specific Association of Circulating Ferritin Level and Risk of Type 2 Diabetes: A Dose-Response Meta-Analysis of Prospective Studies. J. Clin. Endocrinol. & Metab. 2019, 104, 4539–4551. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Li, Y.; Yang, X.; Hemler, E.C.; Fang, Y.; Zhao, L.; Zhang, J.; Yang, Z.; Wang, Z.; He, L.; et al. The dietary transition and its association with cardiometabolic mortality among Chinese adults, 1982–2012: A cross-sectional population-based study. Lancet Diabetes Endocrinol. 2019, 7, 540–548. [Google Scholar] [CrossRef]
- Vuppalanchi, R.; Troutt, J.S.; Konrad, R.J.; Ghabril, M.; Saxena, R.; Bell, L.N.; Kowdley, K.V.; Chalasani, N. Serum hepcidin levels are associated with obesity but not liver disease. Obes. (Silver Spring) 2014, 22, 836–841. [Google Scholar] [CrossRef] [Green Version]
- Zhu, Z.; He, Y.; Wang, Z.; He, X.; Zang, J.; Guo, C.; Jia, X.; Ren, Y.; Shan, C.; Sun, J.; et al. The associations between sugar-sweetened beverage intake and cardiometabolic risks in Chinese children and adolescents. Pediatr. Obes. 2020, 15, e12634. [Google Scholar] [CrossRef]
- Daniels, S.R.; Greer, F.R. Lipid Screening and Cardiovascular Health in Childhood. Pediatrics 2008, 122, 198–208. [Google Scholar] [CrossRef] [Green Version]
- Expert Panel on Integrated Guidelines for Cardiovascular Health and Risk Reduction in Children and Adolescents. Expert panel on integrated guidelines for cardiovascular health and risk reduction in children and adolescents: Summary report. Pediatrics 2011, 128 (Suppl. S5), S213–S256. [Google Scholar] [CrossRef]
- Dong, H.; Yan, Y.; Liu, J.; Cheng, H.; Zhao, X.; Shan, X.; Huang, G.; Mi, J.; Mi, J.; Liu, J.; et al. Reference centiles for evaluating total body fat development and fat distribution by dual-energy x-ray absorptiometry among children and adolescents aged 3–18 years. Clin. Nutr. 2021, 40, 1289–1295. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.-E.; Kim, D.-H.; Roh, Y.-K.; Ju, S.-Y.; Yoon, Y.-J.; Nam, G.-E.; Nam, H.-Y.; Choi, J.-S.; Lee, J.-E.; Sang, J.-E.; et al. Relationship between Serum Ferritin Levels and Dyslipidemia in Korean Adolescents. PLoS ONE 2016, 11, e0153167. [Google Scholar] [CrossRef] [Green Version]
- Al Akl, N.S.; Khalifa, O.; Errafii, K.; Arredouani, A. Association of dyslipidemia, diabetes and metabolic syndrome with serum ferritin levels: A middle eastern population-based cross-sectional study. Sci. Rep. 2021, 11, 24080. [Google Scholar] [CrossRef] [PubMed]
- Arosio, P.; Levi, S. Ferritin, iron homeostasis, and oxidative damage1,2 1Guest Editor: Mario Comporti 2This article is part of a series of reviews on “Iron and Cellular Redox Status.” The full list of papers may be found on the homepage of the journal. Free Radic. Biol. Med. 2002, 33, 457–463. [Google Scholar] [CrossRef]
- Nelson, J.E.; Klintworth, H.; Kowdley, K.V. Iron Metabolism in Nonalcoholic Fatty Liver Disease. Curr. Gastroenterol. Rep. 2011, 14, 8–16. [Google Scholar] [CrossRef] [PubMed]
- Guo, H.; Ling, W. The update of anthocyanins on obesity and type 2 diabetes: Experimental evidence and clinical perspectives. Rev. Endocr. Metab. Disord. 2015, 16, 1–13. [Google Scholar] [CrossRef]
- Abril-Ulloa, V.; Flores-Mateo, G.; Solà-Alberich, R.; Manuel-y-Keenoy, B.; Arija, V. Ferritin levels and risk of metabolic syndrome: Meta-analysis of observational studies. BMC Public Health 2014, 14, 483. [Google Scholar] [CrossRef] [Green Version]
- Moen, I.W.; Bergholdt, H.K.M.; Mandrup-Poulsen, T.; Nordestgaard, B.G.; Ellervik, C. Increased Plasma Ferritin Concentration and Low-Grade Inflammation—A Mendelian Randomization Study. Clin. Chem. 2018, 64, 374–385. [Google Scholar] [CrossRef]
- Andrews, M.; Soto, N.; Arredondo-Olguín, M. Association between ferritin and hepcidin levels and inflammatory status in patients with type 2 diabetes mellitus and obesity. Nutrition 2015, 31, 51–57. [Google Scholar] [CrossRef]
- Aranda, N.; Fernandez-Cao, J.C.; Tous, M.; Arija, V. Increased iron levels and lipid peroxidation in a Mediterranean population of Spain. Eur. J. Clin. Investig. 2016, 46, 520–526. [Google Scholar] [CrossRef]
- Andrews, S.C.; Robinson, A.K.; Rodríguez-Quiñones, F. Bacterial iron homeostasis. FEMS Microbiol. Rev. 2003, 27, 215–237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kau, A.L.; Ahern, P.P.; Griffin, N.W.; Goodman, A.L.; Gordon, J.I. Human nutrition, the gut microbiome and the immune system. Nature 2011, 474, 327–336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moore Heslin, A.; O’Donnell, A.; Buffini, M.; Nugent, A.P.; Walton, J.; Flynn, A.; McNulty, B.A. Risk of Iron Overload in Obesity and Implications in Metabolic Health. Nutrients 2021, 13, 1539. [Google Scholar] [CrossRef]
- Zhu, Y.; He, B.; Xiao, Y.; Chen, Y. Iron metabolism and its association with dyslipidemia risk in children and adolescents: A cross-sectional study. Lipids Health Dis. 2019, 18, 50. [Google Scholar] [CrossRef] [Green Version]
- Mörwald, K.; Aigner, E.; Bergsten, P.; Brunner, S.M.; Forslund, A.; Kullberg, J.; Ahlström, H.; Manell, H.; Roomp, K.; Schütz, S.; et al. Serum Ferritin Correlates With Liver Fat in Male Adolescents With Obesity. Front. Endocrinol. (Lausanne) 2020, 11, 340. [Google Scholar] [CrossRef]
- Zhang, J.; Cao, J.; Xu, H.; Dong, G.; Huang, K.; Wu, W.; Ye, J.; Fu, J. Ferritin as a key risk factor for nonalcoholic fatty liver disease in children with obesity. J. Clin. Lab. Anal. 2021, 35, e23602. [Google Scholar] [CrossRef]
- Stoffel, N.U.; El-Mallah, C.; Herter-Aeberli, I.; Bissani, N.; Wehbe, N.; Obeid, O.; Zimmermann, M.B. The effect of central obesity on inflammation, hepcidin, and iron metabolism in young women. Int. J. Obes. 2020, 44, 1291–1300. [Google Scholar] [CrossRef]
- Rodríguez-Mortera, R.; Caccavello, R.; Hermo, R.; Garay-Sevilla, M.E.; Gugliucci, A. Higher Hepcidin Levels in Adolescents with Obesity Are Associated with Metabolic Syndrome Dyslipidemia and Visceral Fat. Antioxidants 2021, 10, 751. [Google Scholar] [CrossRef]
- Kumar, S.; Bhatia, P.; Jain, R.; Bharti, B. Plasma Hepcidin Levels in Healthy Children: Review of Current Literature Highlights Limited Studies. J. Pediatr. Hematol./Oncol. 2019, 41, 238–242. [Google Scholar] [CrossRef]
Characteristics | Boys (n = 1897) | Girls (n = 1922) |
---|---|---|
Age, years | 11.55 ± 3.40 | 11.54 ± 3.42 |
6–10 years, n (%) | 767 (50.8) | 742 (49.2) |
11–17 years, n (%) | 1130 (48.9) | 1180 (51.1) |
PBF (%) | 18.41 ± 9.66 | 23.11 ± 8.20 |
BMI (kg/m2) | 19.54 ± 4.19 | 19.45 ± 4.78 |
WHtR | 0.44 ± 0.06 | 0.44 ± 0.06 |
Sedentary time, h/d | 3.3 ± 1.5 | 3.7 ± 1.4 |
Energy intake, kcal/d | 2043.73 ± 638.88 | 2127.73 ± 646.60 |
Pubertal stage, n (%) | 467(24.6) | 968 (50.4) |
Hs-CRP, mg/L | 0.30 (0.10, 0.80) | 0.20 (0.10, 0.50) |
Serum ferritin (µg/L) | 48.80 (33.20, 73.90) | 35.90 (23.08, 53.63) |
TC (mg/dL) | 150.18 ± 27.55 | 155.67 ± 26.26 |
TG (mg/dL) | 52.26 (38.09, 74.40) | 56.69 (45.52, 78.83) |
HDL-C (mg/dL) | 59.39 ± 12.36 | 61.89 ± 12.08 |
LDL-C (mg/dL) | 83.21 ± 23.05 | 85.85 ± 21.74 |
High TC (≥200 mg/dL), n (%) | 95 (5.0) | 103 (5.4) |
High TG (≥100 mg/dL, 0–9 years; ≥130 mg/dL, 10–19 years), n (%) | 129 (6.8) | 111 (5.8) |
Low HDLC (≤40 mg/dL), n (%) | 48 (2.5) | 24 (1.2) |
High LDLC (≥130 mg/dL), n (%) | 73 (3.9) | 63 (3.3) |
Dyslipidemia, n (%) | 240 (12.7) | 222 (11.6) |
Obesity categories based on PBF | ||
Low body fat, n(%) | 272 (14.4) | 258 (13.5) |
Healthy body fat, n(%) | 1307 (69.2) | 1379 (71.9) |
Overweight/obesity, n(%) | 311 (16.5) | 280 (14.6) |
Serum Ferritin † | ||||||
---|---|---|---|---|---|---|
Low Fat (PBF Z-Score < −1) | Healthy Fat (−1 ≤ PBF Z-Score ≤ 1) | Overweight/Obesity (PBF Z-Score > 1) | ||||
Gender | AUC (95% CI) | p | AUC (95% CI) | p | AUC (95% CI) | p |
All | 0.50 (0.41 to 0.58) | 0.92 | 0.53 (0.50 to 0.57) | 0.07 | 0.64 (0.59 to 0.69) | <0.001 |
Boys | 0.46 (0.32 to 0.60) | 0.53 | 0.53 (0.47 to 0.58) | 0.30 | 0.61 (0.54 to 0.68) | 0.004 |
Girls | 0.56 0.45 to 0.67) | 0.37 | 0.55 (0.50 to 0.59) | 0.07 | 0.68 (0.61 to 0.75) | <0.001 |
Serum Ferritin † | |||||||||
---|---|---|---|---|---|---|---|---|---|
Characteristics | Low Fat (PBF Z-Score < −1) | Healthy Fat (−1 ≤ PBF Z-Score ≤ 1) | Overweight/Obesity (PBF Z-Score > 1) | ||||||
Rate | OR (95% CI) | p | Rate | OR (95% CI) | p | Rate | OR (95% CI) | p | |
High TC | 4.5% | 2.00 (0.42 to 9.57) | 0.39 | 5.1% | 1.68 (0.89 to 3.19) | 0.11 | 6.1% | 23.96 (5.71 to 100.47) | <0.001 |
High TG | 2.8% | 0.71 (0.10 to 5.03) | 0.73 | 4.5% | 2.55 (1.35 to 4.83) | 0.004 | 17.8% | 9.67 (4.20 to 22.26) | <0.001 |
Low HDLC | 0.8% | - | - | 1.7% | 1.95 (0.67 to 5.63) | 0.22 | 3.7% | 0.41 (0.09 to 1.81) | 0.24 |
High LDLC | 2.1% | 0.71 (0.10 to 5.03) | 0.67 | 3.4% | 3.65 (1.64 to 8.13) | 0.001 | 5.9% | 11.82 (3.45 to 40.51) | <0.001 |
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He, X.; Wang, W.; Zhu, Z.; Zang, J.; Liu, T.; Shi, Y.; Fu, C. Percent Body Fat-Related Disparities of Serum Ferritin on the Risk of Lipid Metabolism Abnormalities in Children and Adolescents. Int. J. Environ. Res. Public Health 2022, 19, 16235. https://doi.org/10.3390/ijerph192316235
He X, Wang W, Zhu Z, Zang J, Liu T, Shi Y, Fu C. Percent Body Fat-Related Disparities of Serum Ferritin on the Risk of Lipid Metabolism Abnormalities in Children and Adolescents. International Journal of Environmental Research and Public Health. 2022; 19(23):16235. https://doi.org/10.3390/ijerph192316235
Chicago/Turabian StyleHe, Xin, Wenjing Wang, Zhenni Zhu, Jiajie Zang, Tong Liu, Yan Shi, and Chen Fu. 2022. "Percent Body Fat-Related Disparities of Serum Ferritin on the Risk of Lipid Metabolism Abnormalities in Children and Adolescents" International Journal of Environmental Research and Public Health 19, no. 23: 16235. https://doi.org/10.3390/ijerph192316235
APA StyleHe, X., Wang, W., Zhu, Z., Zang, J., Liu, T., Shi, Y., & Fu, C. (2022). Percent Body Fat-Related Disparities of Serum Ferritin on the Risk of Lipid Metabolism Abnormalities in Children and Adolescents. International Journal of Environmental Research and Public Health, 19(23), 16235. https://doi.org/10.3390/ijerph192316235