Circulating Fatty Acids Associate with Metabolic Changes in Adolescents Living with Obesity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Measurement of Blood Lipids and Associated Parameters
2.2. Assessment of Redox Status Parameters
2.3. Analysis of Total Plasma Fatty Acid Composition
2.4. Measurement of Relative Leukocyte Telomere Length (rLTL)
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- World Obesity. Available online: https://www.worldobesity.org/ (accessed on 20 December 2023).
- Devlin, T. Textbook of Biochemistry: With Clinical Correlations, 7th ed.; John Wiley & Sons: Hoboken, NJ, USA, 2011; p. 691. [Google Scholar]
- Longo, M.; Zatterale, F.; Naderi, J.; Parrillo, L.; Formisano, P.; Raciti, G.A.; Beguinot, F.; Miele, C. Adipose Tissue Dysfunction as Determinant of Obesity-Associated Metabolic Complications. Int. J. Mol. Sci. 2019, 20, 2358. [Google Scholar] [CrossRef] [PubMed]
- Roberts, R.; Hodson, L.; Dennis, A.L.; Neville, M.J.; Humphreys, S.M.; Harnden, K.E.; Micklem, K.J.; Frayn, K.N. Markers of de novo lipogenesis in adipose tissue: Associations with small adipocytes and insulin sensitivity in humans. Diabetologia 2009, 52, 882–890. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.I.; Huh, J.Y.; Sohn, J.H.; Choe, S.S.; Lee, Y.S.; Lim, C.Y.; Jo, A.; Park, S.B.; Han, W.; Kim, J.B. Lipid-overloaded enlarged adipocytes provoke insulin resistance independent of inflammation. Mol. Cell. Biol. 2015, 10, 1686–1699. [Google Scholar] [CrossRef] [PubMed]
- McLaughlin, T.; Craig, C.; Liu, L.F.; Perelman, D.; Allister, C.; Spielman, D.; Cushman, S.W. Adipose cell size and regional fat deposition as predictors of metabolic response to overfeeding in insulin resistant and insulin-sensitive humans. Diabetes 2016, 65, 1245–1254. [Google Scholar] [CrossRef] [PubMed]
- Lawik, M.; Vidal-Puig, A.J. Lipotoxicity, overnutrition and energy metabolism in aging. Ageing Res. Rev. 2006, 5, 144–164. [Google Scholar]
- Gustafson, B.; Smith, U. Cytokines promote Wnt signaling and inflammation and impair the normal differentiation and lipid accumulation in 3T3-L1 preadipocytes. J. Biol. Chem. 2006, 281, 9507–9516. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Jiang, Q.; Wang, L. Appetite Regulation of TLR4-Induced Inflammatory Signaling. Front. Endocrinol. 2021, 12, 777997. [Google Scholar] [CrossRef] [PubMed]
- Bournat, J.C.; Brown, C.W. Mitochondrial dysfunction in obesity. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 5, 446–452. [Google Scholar] [CrossRef] [PubMed]
- Hirabara, S.M.; Curi, R.; Maechler, P. Saturated fatty acid-induced insulin resistance is associated with mitochondrial dysfunction in skeletal muscle cells. J. Cell. Physiol. 2010, 1, 187–194. [Google Scholar] [CrossRef] [PubMed]
- Klopstock, T.; Naumann, M.; Seibel, P.; Shalke, B.; Reiners, K.; Reichmann, H. Mitochondrial DNA mutations in multiple symmetric lipomatosis. Mol. Cell. Biochem. 1997, 1–2, 271–275. [Google Scholar] [CrossRef]
- Hliwa, A.; Ramos-Molina, B.; Laski, D.; Mika, A.; Sledzinski, T. The Role of Fatty Acids in Non-Alcoholic Fatty Liver Disease Progression: An Update. Int. J. Mol. Sci. 2021, 13, 6900. [Google Scholar] [CrossRef] [PubMed]
- Schwingshackl, L.; Hoffmann, G. Monounsaturated fatty acids and risk of cardiovascular disease: Synopsis of the evidence available from systematic reviews and meta-analyses. Nutrients 2012, 4, 1989–2007. [Google Scholar] [CrossRef] [PubMed]
- Tarrago-Trani, M.T.; Phillips, K.M.; Lemar, L.E.; Holden, J.M. New and existing oils and fats used in products with reduced trans-fatty acids content. J. Am. Diet. Assoc. 2006, 106, 867–880. [Google Scholar] [CrossRef] [PubMed]
- Djuricic, I.; Calder, P.C. Beneficial outcomes of omega-6 and omega-3 polyunsaturated fatty acids on human health: An update for 2021. Nutrients 2021, 15, 2421. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, S.; O’Conneli, J.F.; Carlson, O.D.; Gonzalez-Mariscal, I.; Kim, Y.; Moaddel, R.; Ghosh, P.; Egan, J.M. Linoleic acid in diets of mice increases total endocannabinoid levels in bowel and liver: Modification by dietary glucose. Obes. Sci. Pract. 2019, 5, 383–394. [Google Scholar] [CrossRef] [PubMed]
- Ma, X.; Jiang, Z.; Lai, C. Significance of Increasing n-3 PUFA Content in Pork on Human Health. Crit. Rev. Food Sci. Nutr. 2016, 56, 858–870. [Google Scholar] [CrossRef] [PubMed]
- Kordinas, V.; Ioannidis, A.; Chatzipanagiotou, S. The Telomere/Telomerase System in Chronic Inflammatory Diseases. Cause or Effect? Genes 2016, 7, 60. [Google Scholar] [CrossRef] [PubMed]
- Srinivas, N.; Rachakonda, S.; Kumar, R. Telomeres and Telomere Length: A General Overview. Cancers 2020, 12, 558. [Google Scholar] [CrossRef] [PubMed]
- Raftopoulou, C.; Paltoglou, G.; Charmandari, E. Association between Telomere Length and Pediatric Obesity: A Systematic Review. Nutrients 2022, 14, 1244. [Google Scholar] [CrossRef] [PubMed]
- Statistical Office of the Republic of Serbia. Available online: https://publikacije.stat.gov.rs/G2021/pdfE/G20216003.pdf (accessed on 19 March 2024).
- Kang, H. Sample size determination and power analysis using the G*Power software. J. Educ. Eval. Health Prof. 2021, 18, 17. [Google Scholar] [CrossRef] [PubMed]
- Erel, O. A Novel Automated Direct Measurement Method for Total Antioxidant Capacity Using a New Generation, More Stable ABTS Radical Cation. Clin. Biochem. 2004, 37, 277. [Google Scholar] [CrossRef] [PubMed]
- Paripović, D.; Kotur-Stevuljević, J.; Vukašinović, A.; Ilisić, T.; Miloševski-Lomić, G.; Peco-Antić, A. The influence of oxidative stress on cardiac remodeling in obese adolescents. Scand. J. Clin. Lab. Investig. 2018, 78, 595–600. [Google Scholar] [CrossRef] [PubMed]
- Kostić, K.; Brborić, J.; Delogum, G.; Simić, M.R.; Samardžić, S.; Maksimović, Z.; Dettori, M.A.; Fabbri, D.; Kotur-Stevuljević, J.; Saso, L. Antioxidant Activity of Natural Phenols and Derived Hydroxylated Biphenyls. Molecules 2023, 28, 2646. [Google Scholar] [CrossRef] [PubMed]
- Erel, O. A New Automated Colorimetric Method for Measuring Total Oxidant Status. Clin. Biochem. 2005, 38, 1103. [Google Scholar] [CrossRef] [PubMed]
- Obradovic, D.; Anđelić, T.; Ninković, M.; Dejanović, B.; Kotur-Stevuljević, J. Superoxide dismutase (SOD), advanced oxidation protein products (AOPP), and disease-modifying treatment are related to better relapse recovery after corticosteroid treatment in multiple sclerosis. Neurol. Sci. 2020, 42, 3241–3247. [Google Scholar] [CrossRef] [PubMed]
- Bar-Or, D.; Lau, E.; Winkler, J. A novel Assay for Cobalt-albumin Binding and its Potential as a Marker for Myocardial Ischemia—A preliminary report. J. Emerg. Med. 2000, 19, 311–315. [Google Scholar] [CrossRef]
- Alamdari, D.H.; Paletas, K.; Pegiou, T.; Sarigianni, M.; Befani, C.; Koliakos, G. A Novel Assay for the Evaluation of the Prooxidant-antioxidant Balance, Before and After Antioxidant Vitamin administration in type II Diabetes Patients. Clin. Biochem. 2007, 40, 248–254. [Google Scholar] [CrossRef] [PubMed]
- Glaser, C.; Demmelmair, H.; Koletzko, B. High-Throughput Analysis of Total Plasma Fatty Acid Composition with Direct In Situ Transesterification. PLoS ONE 2010, 8, e12045. [Google Scholar] [CrossRef] [PubMed]
- Wege, H.; Chui, M.S.; Le, H.T.; Tran, J.M.; Zern, M.A. SYBR Green Real-time Telomeric Repeat Amplification Protocol for the Rapid Quantification of Telomerase Activity. Nucleic Acids Res. 2003, 31, e3. [Google Scholar] [CrossRef] [PubMed]
- Skinner, A.C.; Perrin, E.M.; Moss, L.A.; Skelton, J.A. Cardiometabolic Risks and Severity of Obesity in Children and Young Adults. N. Engl. J. Med. 2015, 373, 1307–1317. [Google Scholar] [CrossRef]
- Friedland, O.; Nemet, D.; Gorodnitsky, N.; Wolach, B.; Eliakim, A. Obesity and lipid profiles in children and adolescents. J. Pediatr. Endocrinol. Metab. 2002, 7, 1011–1016. [Google Scholar] [CrossRef] [PubMed]
- Plourde, G. Impact of obesity on glucose and lipid profiles in adolescents at different age groups in relation to adulthood. BMC Fam. Pract. 2002, 3, 18. [Google Scholar] [CrossRef] [PubMed]
- Garcés, C.; Oya, I.; Lasunción, M.A.; López-Simón, L.; Cano, B.; de Oya, M. Sex hormone-binding globulin and lipid profile in pubertal children. Metabolism 2010, 2, 166–171. [Google Scholar] [CrossRef] [PubMed]
- Kummrow, E.; Hussain, M.M.; Pan, M.; Marsh, J.B.; Fisher, E.A. Myristic acid increases dense lipo-protein secretion by inhibiting apoB degradation and triglyceride recruitment. J. Lipid Res. 2002, 12, 2155–2163. [Google Scholar] [CrossRef]
- French, M.A.; Sundram, K.; Clandinin, M.T. Cholesterolaemic effect of palmitic acid in relation to other dietary fatty acids. Asia Pac. J. Clin. Nutr. 2002, 11, 401–407. [Google Scholar] [CrossRef] [PubMed]
- Chien, K.R.; Bellary, A.; Nicar, M.; Mukherjee, A.; Buja, L.M. Induction of a reversible cardiac lipidosis by a dietary long-chain fatty acid (erucic acid). Relationship to lipid accumulation in border zones of myocardial infarcts. Am. J. Pathol. 1983, 1, 68. [Google Scholar]
- Kramer, J.K.G.; Sauer, F.D.; Wolynetz, M.S.; Farnworth, E.R.; Johnston, K.M. Effects of dietary saturated fat on erucic acid induced myocardial lipidosis in rats. Lipids 1992, 8, 619–623. [Google Scholar] [CrossRef] [PubMed]
- Van Linthout, S.; Frias, M.; Singh, N.; De Geest, B. Therapeutic potential of HDL in cardioprotection and tissue repair. In Handbook of Experimental Pharmacology; Springer: Berlin/Heidelberg, Germany, 2015; pp. 527–565. [Google Scholar]
- Yvan-Charvet, L.; Wang, N.; Tall, A.R. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 139–143. [Google Scholar] [CrossRef]
- Jomard, A.; Osto, E. High Density Lipoproteins: Metabolism, Function, and Therapeutic Potential. Front. Cardiovasc. Med. 2020, 31, 39. [Google Scholar] [CrossRef] [PubMed]
- Djuricic, I.; Calder, P.C. Polyunsaturated fatty acids and metabolic health: Novel insights. Curr. Opin. Clin. Nutr. Metab. Care 2022, 25, 420–436. [Google Scholar] [CrossRef] [PubMed]
- Azain, M.J. Role of fatty acids in adipocyte growth and development. J. Anim. Sci. 2004, 82, 916–924. [Google Scholar] [CrossRef] [PubMed]
- Simopoulos, A.P. An Increase in the Omega-6/Omega-3 Fatty Acid Ratio Increases the Risk for Obesity. Nutrients 2016, 8, 128. [Google Scholar] [CrossRef] [PubMed]
- DiNicolantonio, J.J.; O’Keefe, J. The Importance of Maintaining a Low Omega-6/Omega-3 Ratio for Reducing the Risk of Autoimmune Diseases, Asthma, and Allergies. Mo. Med. 2021, 5, 453–459. [Google Scholar]
- González-Becerra, K.; Ramos-Lopez, O.; Barrón-Cabrera, E.; Riezu-Boj, J.I.; Milagro, F.I.; Martinez-Lopez, E.; Martínez, J.A. Fatty acids, epigenetic mechanisms and chronic diseases: A systematic review. Lipids Health Dis. 2019, 18, 178. [Google Scholar] [CrossRef]
- Liu, X.; Liu, X.; Shi, Q.; Fan, X.; Qi, K. Association of telomere length and telomerase methylation with n-3 fatty acids in preschool children with obesity. BMC Pediatr. 2021, 21, 24. [Google Scholar] [CrossRef]
- Seo, B.; Yang, K.; Kahe, K.; Qureshi, A.A.; Chan, A.T.; De Vivo, I.; Cho, E.; Giovannucci, E.L.; Nan, H. Association of omega-3 and omega-6 fatty acid intake with leukocyte telomere length in US males. Am. J. Clin. Nutr. 2022, 116, 1759–1766. [Google Scholar] [CrossRef] [PubMed]
- Hopps, E.; Noto, D.; Caimi, G.; Averna, M.R. A novel component of the metabolic syndrome: The oxidative stress. Nutr. Metab. Cardiovasc. Dis. 2010, 1, 72. [Google Scholar] [CrossRef] [PubMed]
- Dimitrijević-Srećković, V.; Čolak, E.; Đorđević, P.; Gostiljac, D.; Srećković, B.; Popović, S.; Canović, F.; Ilić, M.; Obrenović, R.; Vukčević, V.; et al. Prothrombogenic factors and reduced antioxidative defense in children and adolescents with pre-metabolic and metabolic syndrome. Clin. Chem. Lab. Med. 2007, 9, 1140. [Google Scholar] [CrossRef] [PubMed]
- Basu, S.; Smedman, A.; Vessby, B. Conjugated linoleic acid induces lipid peroxidation in humans. FEBS Lett. 2000, 18, 468. [Google Scholar] [CrossRef] [PubMed]
Parameter | Obese (n = 91) | Control (n = 44) | p |
---|---|---|---|
Sex (male/female) | 45/46 | 22/22 | ns |
Age (year) | 15 (11.5–16.0) | 15 (12.5–16.5) | ns |
BMI (kg/m2) aaa,bbb | 33.3 (27.3–37.0) | 17.2 (16.1–21.1) | <0.001 |
Total cholesterol (mmol/L) | 4.51 (3.78–5.08) | 4.12 (3.38–4.72) | ns |
LDL-cholesterol (mmol/L) aa | 2.62 (2.33–3.12) | 2.14 (1.85–2.68) | 0.045 |
HDL-cholesterol (mmol/L) aa | 1.30 (1.05–1.56) | 1.58 (1.34–1.75) | 0.028 |
Triglycerides (mmol/L) aa | 0.91 (0.51–1.20) | 0.75 (0.63–1.00) | 0.028 |
RFCVD aa | 3.4 (2.6–4.2) | 2.4 (2.2–3.1) | <0.001 |
IA aa | 2.1 (1.5–2.7) | 1.4 (1.0–1.9) | <0.001 |
TAS (mmol/L) aaa,bbb | 729(651–783) | 439 (289–401) | <0.001 |
SOD (U/L) aaa,bbb | 95 (82–118) | 139 (135–144) | <0.001 |
SHG (mmol/L) aaa,bbb | 0.352 (0.240–0.402) | 0.455 (0.381–0.565) | <0.001 |
TOS (mmol/L) aaa,bbb | 100 (83–104) | 61 (58–76) | <0.001 |
AOPPs (μmol/L) aaa,bbb | 78.1 (64.8–95.6) | 44.9 (40.7–50.3) | <0.001 |
PAB (HK) aaa,bbb | 100.5 (94.7–110.5) | 59.2 (51.0–67.7) | <0.001 |
PON (U/L) aaa,bbb | 171 (123–313) | 261 (186–575) | <0.001 |
rLTLaaa,bbb | 0.643 (0.440–0.871) | 1.597 (1.520–1.819) | <0.001 |
14:0 (%) aaa,bbb | 2.8 (1.40–4.05) | 0.70 (0.59–0.84) | <0.001 |
16:0 (%) | 27.4 (26.06–28.28) | 26.4 (23.69–27.45) | ns |
18:0 (%) a,b | 11.49 (10.03–12.42) | 12.35 (11.49–13.20) | 0.01 |
18:1n-9 (%) | 11.38 (10.13–12.23 | 11.61 (11.00–13.95) | 0.045 |
18:2n-6 (%) | 24.41 (22.61–26.07) | 24.15 (21.85–27.24) | ns |
20:3n-3 (%) a | 2.00 (1.90–2.23) | 1.75 (1.65–2.05) | 0.01 |
20:4n-6 (%) a,b | 10.21 (8.98–10.84) | 10.98 (10.28–11.65) | 0.045 |
22:1n-9 (%) aaa,bbb | 1.85 (1.46–3.47) | 0.70 (0.45–0.95) | <0.001 |
22:4n-6 (%) a,b | 0.37 (0.28–0.70) | 0.69 (0.41–0.90) | 0.05 |
20:5n-3 (%) a,b | 0.88 (0.78–0.99) | 1.15 (0.89–1.30) | 0.002 |
22:5n-3 (%) a,b | 0.40 (0.31–0.51) | 0.84 (0.60–0.92) | <0.001 |
22:6n-3 (%) | 2.17 (1.77–3.03) | 2.48 (2.05–2.58) | ns |
Total n-3 PUFAs aa,bb | 5.45 (4.95–6.39) | 6.22 (5.26–7.15) | 0.003 |
Total n-6 PUFAs | 34.99 (34.04–37.95) | 35.82 (33.0–38.60) | ns |
n-6-to-n-3 PUFA ratio aa,bb | 6.41 (5.60–7.15) | 5.60 (4.91–6.40) | 0.01 |
Parameter | 14:0 | 16:0 | 18:0 | 18:1n-9 | 18:2n-6 | 20:4n-6 | 22:1n-9 | 22:4n-6 | Total n-3 | Total n-6 | n-6/n-3 |
---|---|---|---|---|---|---|---|---|---|---|---|
Obese group | |||||||||||
Total cholesterol | - | 0.250 * | - | - | - | 0.218 * | −0.212 * | −0.231 * | - | - | - |
LDL-cholesterol | - | 0.264 ** | - | - | - | - | - | - | - | - | - |
HDL-cholesterol | - | - | - | - | - | - | −0.357 *** | -0.242 * | - | - | - |
Triglycerides | 0.266 ** | - | - | - | - | - | - | - | - | - | 0.243 * |
RFCVD | 0.250 * | - | - | - | - | - | - | - | - | - | - |
IA | 0.225 * | - | - | - | - | - | - | 0.205 * | - | - | - |
TOS | 0.391 *** | - | - | - | 0.225 * | - | - | - | - | 0.290 ** | - |
AOPPs | 0.470 *** | - | - | - | 0.200 * | - | - | - | - | 0.240 * | - |
TAS | −0.331 * | - | - | - | - | - | - | - | - | - | - |
SOD | - | - | - | - | - | - | - | - | - | - | |
SHG | 0.385 *** | - | - | - | - | - | - | - | - | - | - |
Control group | |||||||||||
HDL- cholesterol | - | - | −0.410 ** | - | - | - | - | - | - | - | |
TOS | - | - | 0.349 ** | - | - | 0.526 * | - | - | −0.477 ** | - | 0.505 ** |
AOPPs | - | - | - | 0.474 * | - | - | - | - | - | −0.608 ** | - |
TAS | - | - | - | −0.504 * | 0.596 ** | - | - | - | - | 0.544 * | - |
SOD | - | - | −0.264 * | - | - | - | - | - | 0.527 ** | - | −0.444 * |
SHG | - | −0.295 * | - | - | −0.601 ** | - | - | 0.493 * | - | −0.517 * | |
PAB | - | - | - | - | - | - | - | - | −0.561 ** | - | 0.517 * |
IMA | - | −0.341 ** | - | - | - | - | - | - | −0.485 * | - | 0.441 * |
Parameter | Low n-6/n-3 PUFA Ratio | High n-6/n-3 PUFA Ratio | p |
---|---|---|---|
rLTL | 1.09 (0.79–1.28) | 0.61 (0.41–0.89) | 0.005 |
18:0 | 13.04 (10.91–13.63) | 11.59 (10.17–12.34) | 0.009 |
18:2n-6 | 20.54 (19.35–22.44) | 24.51 (23.20–26.23) | <0.001 |
20:5n-3 | 0.78 (0.64–1.03) | 0.50 (0.46–0.57) | 0.028 |
n-3 PUFAs | 7.44 (7.10–7.86) | 6.33 (6.09–6.48) | <0.001 |
n-6 PUFAs | 33.39 (32.25–34.88) | 34.00 (32.59–35.90) | 0.047 |
n-6-to-n-3 PUFA ratio | 4.48 (4.17–4.75) | 5.37 (5.13–5.62) | <0.001 |
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Subošić, B.; Kotur-Stevuljević, J.; Bogavac-Stanojević, N.; Zdravković, V.; Ješić, M.; Kovačević, S.; Đuričić, I. Circulating Fatty Acids Associate with Metabolic Changes in Adolescents Living with Obesity. Biomedicines 2024, 12, 883. https://doi.org/10.3390/biomedicines12040883
Subošić B, Kotur-Stevuljević J, Bogavac-Stanojević N, Zdravković V, Ješić M, Kovačević S, Đuričić I. Circulating Fatty Acids Associate with Metabolic Changes in Adolescents Living with Obesity. Biomedicines. 2024; 12(4):883. https://doi.org/10.3390/biomedicines12040883
Chicago/Turabian StyleSubošić, Branko, Jelena Kotur-Stevuljević, Nataša Bogavac-Stanojević, Vera Zdravković, Maja Ješić, Smiljka Kovačević, and Ivana Đuričić. 2024. "Circulating Fatty Acids Associate with Metabolic Changes in Adolescents Living with Obesity" Biomedicines 12, no. 4: 883. https://doi.org/10.3390/biomedicines12040883
APA StyleSubošić, B., Kotur-Stevuljević, J., Bogavac-Stanojević, N., Zdravković, V., Ješić, M., Kovačević, S., & Đuričić, I. (2024). Circulating Fatty Acids Associate with Metabolic Changes in Adolescents Living with Obesity. Biomedicines, 12(4), 883. https://doi.org/10.3390/biomedicines12040883