Sex-Related Differences in the Associations between Adiponectin and Serum Lipoproteins in Healthy Subjects and Patients with Metabolic Syndrome
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design, Participants, and Routine Laboratory Procedures
2.2. Adiponectin Measurements
2.3. Lipoprotein Profiling Using Nuclear Magnetic Resonance (NMR) Spectroscopy
2.4. Statistics
3. Results
3.1. Differences in Demographic and Clinical Characteristics between Females and Males within the Groups
3.2. Sex Differences in Serum Levels of Adiponectin, Routine Laboratory Data, and Lipoprotein Subclasses within Each Group
3.3. Correlation Analyses between Adiponectin and the Serum Levels of the VLDL Subclasses
3.4. Correlation Analyses between Adiponectin and the Serum Levels of IDL
3.5. Correlation Analyses between Adiponectin and the Serum Levels of the LDL Subclasses
3.6. Correlation Analyses between Adiponectin and the Serum Levels of the HDL Subclasses
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ALT | alanine aminotransferase |
Apo | apolipoprotein |
AST | aspartate aminotransferase |
BMI | body mass index |
C | cholesterol |
CK | creatine kinase |
CRP | C-reactive protein |
DBP | diastolic blood pressure |
eGFR | estimated glomerular filtration rate |
FC | free cholesterol |
GGT | gamma-glutamyl transpeptidase |
HDL | high-density lipoprotein |
HL | hepatic lipase |
HR | heart rate |
IDL | Intermediate-density lipoprotein |
IL-6 | Interleukin-6 |
LDH | lactate dehydrogenase |
LDL | low-density lipoprotein |
LPL | lipoprotein lipase |
MAP | mean arterial pressure |
MS | metabolic syndrome |
NMR | nuclear magnetic resonance |
PL | phospholipid |
SBP | systolic blood pressure |
TC | total cholesterol |
TG | triglyceride |
VLDL | very low-density lipoprotein |
References
- Christou, G.A.; Kiortsis, D.N. Adiponectin and lipoprotein metabolism. Obes. Rev. 2013, 14, 939–949. [Google Scholar] [CrossRef]
- Yanai, H.; Hirowatari, Y.; Yoshida, H. Diabetic dyslipidemia: Evaluation and mechanism. Glob. Health Med. 2019, 1, 30–35. [Google Scholar] [CrossRef] [PubMed]
- Yamauchi, T.; Kamon, J.; Minokoshi, Y.; Ito, Y.; Waki, H.; Uchida, S.; Yamashita, S.; Noda, M.; Kita, S.; Ueki, K.; et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 2002, 8, 1288–1295. [Google Scholar] [CrossRef]
- Yamauchi, T.; Kamon, J.; Waki, H.; Terauchi, Y.; Kubota, N.; Hara, K.; Mori, Y.; Ide, T.; Murakami, K.; Tsuboyama-Kasaoka, N.; et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 2001, 7, 941–946. [Google Scholar] [CrossRef]
- Ouchi, N.; Kihara, S.; Arita, Y.; Nishida, M.; Matsuyama, A.; Okamoto, Y.; Ishigami, M.; Kuriyama, H.; Kishida, K.; Nishizawa, H.; et al. Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation 2001, 103, 1057–1063. [Google Scholar] [CrossRef]
- Zocchi, M.; Della Porta, M.; Lombardoni, F.; Scrimieri, R.; Zuccotti, G.V.; Maier, J.A.; Cazzola, R. A Potential Interplay between HDLs and Adiponectin in Promoting Endothelial Dysfunction in Obesity. Biomedicines 2022, 10, 1344. [Google Scholar] [CrossRef] [PubMed]
- Lara-Castro, C.; Fu, Y.; Chung, B.H.; Garvey, W.T. Adiponectin and the metabolic syndrome: Mechanisms mediating risk for metabolic and cardiovascular disease. Curr. Opin. Lipidol. 2007, 18, 263–270. [Google Scholar] [CrossRef] [PubMed]
- Combs, T.P.; Berg, A.H.; Obici, S.; Scherer, P.E.; Rossetti, L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J. Clin. Investig. 2001, 108, 1875–1881. [Google Scholar] [CrossRef]
- Kahn, B.B.; Flier, J.S. Obesity and insulin resistance. J. Clin. Investig. 2000, 106, 473–481. [Google Scholar] [CrossRef]
- Alberti, K.G.; Eckel, R.H.; Grundy, S.M.; Zimmet, P.Z.; Cleeman, J.I.; Donato, K.A.; Fruchart, J.C.; James, W.P.; Loria, C.M.; Smith, S.C., Jr.; et al. Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009, 120, 1640–1645. [Google Scholar] [CrossRef]
- Adiels, M.; Olofsson, S.O.; Taskinen, M.R.; Boren, J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 1225–1236. [Google Scholar] [CrossRef] [PubMed]
- Hirano, T. Pathophysiology of Diabetic Dyslipidemia. J. Atheroscler. Thromb. 2018, 25, 771–782. [Google Scholar] [CrossRef]
- Christou, G.A.; Tellis, K.C.; Elisaf, M.C.; Tselepis, A.D.; Kiortsis, D.N. High density lipoprotein is positively correlated with the changes in circulating total adiponectin and high molecular weight adiponectin during dietary and fenofibrate treatment. Hormones 2012, 11, 178–188. [Google Scholar] [CrossRef]
- Riestra, P.; Garcia-Anguita, A.; Lasuncion, M.A.; Cano, B.; de Oya, M.; Garces, C. Relationship of adiponectin with metabolic syndrome components in pubertal children. Atherosclerosis 2011, 216, 467–470. [Google Scholar] [CrossRef]
- Shin, M.J.; Kim, O.Y. Plasma adiponectin is associated with less atherogenic lipoprotein phenotype. Nutr. Metab. Cardiovasc. Dis. 2011, 21, 770–775. [Google Scholar] [CrossRef] [PubMed]
- Tsubakio-Yamamoto, K.; Sugimoto, T.; Nishida, M.; Okano, R.; Monden, Y.; Kitazume-Taneike, R.; Yamashita, T.; Nakaoka, H.; Kawase, R.; Yuasa-Kawase, M.; et al. Serum adiponectin level is correlated with the size of HDL and LDL particles determined by high performance liquid chromatography. Metab. Clin. Exp. 2012, 61, 1763–1770. [Google Scholar] [CrossRef]
- Qiao, L.; Zou, C.; van der Westhuyzen, D.R.; Shao, J. Adiponectin reduces plasma triglyceride by increasing VLDL triglyceride catabolism. Diabetes 2008, 57, 1824–1833. [Google Scholar] [CrossRef] [PubMed]
- Weiss, R.; Otvos, J.D.; Flyvbjerg, A.; Miserez, A.R.; Frystyk, J.; Sinnreich, R.; Kark, J.D. Adiponectin and lipoprotein particle size. Diabetes Care 2009, 32, 1317–1319. [Google Scholar] [CrossRef] [PubMed]
- Oku, H.; Matsuura, F.; Koseki, M.; Sandoval, J.C.; Yuasa-Kawase, M.; Tsubakio-Yamamoto, K.; Masuda, D.; Maeda, N.; Ohama, T.; Ishigami, M.; et al. Adiponectin deficiency suppresses ABCA1 expression and ApoA-I synthesis in the liver. FEBS Lett. 2007, 581, 5029–5033. [Google Scholar] [CrossRef]
- Matsuura, F.; Oku, H.; Koseki, M.; Sandoval, J.C.; Yuasa-Kawase, M.; Tsubakio-Yamamoto, K.; Masuda, D.; Maeda, N.; Tsujii, K.; Ishigami, M.; et al. Adiponectin accelerates reverse cholesterol transport by increasing high density lipoprotein assembly in the liver. Biochem. Biophys. Res. Commun. 2007, 358, 1091–1095. [Google Scholar] [CrossRef]
- Chan, D.C.; Barrett, P.H.; Ooi, E.M.; Ji, J.; Chan, D.T.; Watts, G.F. Very low density lipoprotein metabolism and plasma adiponectin as predictors of high-density lipoprotein apolipoprotein A-I kinetics in obese and nonobese men. J. Clin. Endocrinol. Metab. 2009, 94, 989–997. [Google Scholar] [CrossRef] [PubMed]
- Verges, B.; Petit, J.M.; Duvillard, L.; Dautin, G.; Florentin, E.; Galland, F.; Gambert, P. Adiponectin is an important determinant of apoA-I catabolism. Arterioscler. Thromb. Vasc. Biol. 2006, 26, 1364–1369. [Google Scholar] [CrossRef] [PubMed]
- von Eynatten, M.; Schneider, J.G.; Humpert, P.M.; Rudofsky, G.; Schmidt, N.; Barosch, P.; Hamann, A.; Morcos, M.; Kreuzer, J.; Bierhaus, A.; et al. Decreased plasma lipoprotein lipase in hypoadiponectinemia: An association independent of systemic inflammation and insulin resistance. Diabetes Care 2004, 27, 2925–2929. [Google Scholar] [CrossRef] [PubMed]
- Schneider, J.G.; von Eynatten, M.; Schiekofer, S.; Nawroth, P.P.; Dugi, K.A. Low plasma adiponectin levels are associated with increased hepatic lipase activity in vivo. Diabetes Care 2005, 28, 2181–2186. [Google Scholar] [CrossRef]
- Drew, B.G.; Duffy, S.J.; Formosa, M.F.; Natoli, A.K.; Henstridge, D.C.; Penfold, S.A.; Thomas, W.G.; Mukhamedova, N.; de Courten, B.; Forbes, J.M.; et al. High-density lipoprotein modulates glucose metabolism in patients with type 2 diabetes mellitus. Circulation 2009, 119, 2103–2111. [Google Scholar] [CrossRef]
- Kriketos, A.D.; Gan, S.K.; Poynten, A.M.; Furler, S.M.; Chisholm, D.J.; Campbell, L.V. Exercise increases adiponectin levels and insulin sensitivity in humans. Diabetes Care 2004, 27, 629–630. [Google Scholar] [CrossRef]
- Klobucar, I.; Habisch, H.; Klobucar, L.; Trbusic, M.; Pregartner, G.; Berghold, A.; Kostner, G.M.; Scharnagl, H.; Madl, T.; Frank, S.; et al. Serum Levels of Adiponectin Are Strongly Associated with Lipoprotein Subclasses in Healthy Volunteers but Not in Patients with Metabolic Syndrome. Int. J. Mol. Sci. 2024, 25, 5050. [Google Scholar] [CrossRef]
- Nishizawa, H.; Shimomura, I.; Kishida, K.; Maeda, N.; Kuriyama, H.; Nagaretani, H.; Matsuda, M.; Kondo, H.; Furuyama, N.; Kihara, S.; et al. Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes 2002, 51, 2734–2741. [Google Scholar] [CrossRef]
- Tomono, Y.; Hiraishi, C.; Yoshida, H. Age and sex differences in serum adiponectin and its association with lipoprotein fractions. Ann. Clin. Biochem. 2018, 55, 165–171. [Google Scholar] [CrossRef]
- Ryo, M.; Nakamura, T.; Kihara, S.; Kumada, M.; Shibazaki, S.; Takahashi, M.; Nagai, M.; Matsuzawa, Y.; Funahashi, T. Adiponectin as a biomarker of the metabolic syndrome. Circ. J. 2004, 68, 975–981. [Google Scholar] [CrossRef]
- Mester, P.; Rath, U.; Schmid, S.; Muller, M.; Buechler, C.; Pavel, V. Exploring the Relationship between Plasma Adiponectin, Gender, and Underlying Diseases in Severe Illness. Biomedicines 2023, 11, 3287. [Google Scholar] [CrossRef]
- Klobucar, I.; Klobucar, L.; Lechleitner, M.; Trbusic, M.; Pregartner, G.; Berghold, A.; Habisch, H.; Madl, T.; Frank, S.; Degoricija, V. Associations between Endothelial Lipase and Apolipoprotein B-Containing Lipoproteins Differ in Healthy Volunteers and Metabolic Syndrome Patients. Int. J. Mol. Sci. 2023, 24, 10681. [Google Scholar] [CrossRef]
- Klobucar, I.; Stadler, J.T.; Klobucar, L.; Lechleitner, M.; Trbusic, M.; Pregartner, G.; Berghold, A.; Habisch, H.; Madl, T.; Marsche, G.; et al. Associations between Endothelial Lipase, High-Density Lipoprotein, and Endothelial Function Differ in Healthy Volunteers and Metabolic Syndrome Patients. Int. J. Mol. Sci. 2023, 24, 2073. [Google Scholar] [CrossRef] [PubMed]
- Klobucar, I.; Hofmann, L.; Habisch, H.; Lechleitner, M.; Klobucar, L.; Trbusic, M.; Pregartner, G.; Berghold, A.; Madl, T.; Frank, S.; et al. Advanced Oxidation Protein Products Are Strongly Associated with the Serum Levels and Lipid Contents of Lipoprotein Subclasses in Healthy Volunteers and Patients with Metabolic Syndrome. Antioxidants 2024, 13, 339. [Google Scholar] [CrossRef]
- World Medical, A. World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 2013, 310, 2191–2194. [Google Scholar] [CrossRef]
- Carrero, J.J.; Hecking, M.; Chesnaye, N.C.; Jager, K.J. Sex and gender disparities in the epidemiology and outcomes of chronic kidney disease. Nat. Rev. Nephrol. 2018, 14, 151–164. [Google Scholar] [CrossRef] [PubMed]
- Mauvais-Jarvis, F.; Bairey Merz, N.; Barnes, P.J.; Brinton, R.D.; Carrero, J.J.; DeMeo, D.L.; De Vries, G.J.; Epperson, C.N.; Govindan, R.; Klein, S.L.; et al. Sex and gender: Modifiers of health, disease, and medicine. Lancet 2020, 396, 565–582. [Google Scholar] [CrossRef] [PubMed]
- Ahonen, T.; Saltevo, J.; Laakso, M.; Kautiainen, H.; Kumpusalo, E.; Vanhala, M. Gender differences relating to metabolic syndrome and proinflammation in Finnish subjects with elevated blood pressure. Mediat. Inflamm. 2009, 2009, 959281. [Google Scholar] [CrossRef]
- Kautzky-Willer, A.; Harreiter, J.; Pacini, G. Sex and Gender Differences in Risk, Pathophysiology and Complications of Type 2 Diabetes Mellitus. Endocr. Rev. 2016, 37, 278–316. [Google Scholar] [CrossRef]
- Juszczak, F.; Pierre, L.; Decarnoncle, M.; Jadot, I.; Martin, B.; Botton, O.; Caron, N.; Dehairs, J.; Swinnen, J.V.; Decleves, A.E. Sex differences in obesity-induced renal lipid accumulation revealed by lipidomics: A role of adiponectin/AMPK axis. Biol. Sex Differ. 2023, 14, 63. [Google Scholar] [CrossRef]
- Palmer, B.F.; Clegg, D.J. The sexual dimorphism of obesity. Mol. Cell Endocrinol. 2015, 402, 113–119. [Google Scholar] [CrossRef] [PubMed]
- Saltevo, J.; Kautiainen, H.; Vanhala, M. Gender differences in adiponectin and low-grade inflammation among individuals with normal glucose tolerance, prediabetes, and type 2 diabetes. Gend. Med. 2009, 6, 463–470. [Google Scholar] [CrossRef] [PubMed]
- Cnop, M.; Havel, P.J.; Utzschneider, K.M.; Carr, D.B.; Sinha, M.K.; Boyko, E.J.; Retzlaff, B.M.; Knopp, R.H.; Brunzell, J.D.; Kahn, S.E. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: Evidence for independent roles of age and sex. Diabetologia 2003, 46, 459–469. [Google Scholar] [CrossRef] [PubMed]
- Gavin, K.M.; Bessesen, D.H. Sex Differences in Adipose Tissue Function. Endocrinol. Metab. Clin. N. Am. 2020, 49, 215–228. [Google Scholar] [CrossRef] [PubMed]
- Palmisano, B.T.; Zhu, L.; Eckel, R.H.; Stafford, J.M. Sex differences in lipid and lipoprotein metabolism. Mol. Metab. 2018, 15, 45–55. [Google Scholar] [CrossRef]
- Tramunt, B.; Smati, S.; Grandgeorge, N.; Lenfant, F.; Arnal, J.F.; Montagner, A.; Gourdy, P. Sex differences in metabolic regulation and diabetes susceptibility. Diabetologia 2020, 63, 453–461. [Google Scholar] [CrossRef]
- Wang, F.H.; Meng, L.Y.; Yu, T.Y.; Tan, Y.; Quan, H.; Hu, J.Y.; Bai, Q.K.; Xie, J.C.; Zhao, Y.X. Associations of Abdominal Visceral Fat Content and Plasma Adiponectin Level with Intracranial Atherosclerotic Stenosis: A Cross-Sectional Study. Front. Neurol. 2022, 13, 893401. [Google Scholar] [CrossRef]
- Loucif, Y.; Methot, J.; Tremblay, K.; Brisson, D.; Gaudet, D. Contribution of adiponectin to the cardiometabolic risk of postmenopausal women with loss-of-function lipoprotein lipase gene mutations. Menopause 2011, 18, 558–562. [Google Scholar] [CrossRef]
- Strauss, J.G.; Frank, S.; Kratky, D.; Hammerle, G.; Hrzenjak, A.; Knipping, G.; von Eckardstein, A.; Kostner, G.M.; Zechner, R. Adenovirus-mediated rescue of lipoprotein lipase-deficient mice. Lipolysis of triglyceride-rich lipoproteins is essential for high density lipoprotein maturation in mice. J. Biol. Chem. 2001, 276, 36083–36090. [Google Scholar] [CrossRef]
- Brudasca, I.; Cucuianu, M. Pathogenic role of abnormal fatty acids and adipokines in the portal flow. Relevance for metabolic syndrome, hepatic steatosis and steatohepatitis. Rom. J. Intern. Med. 2007, 45, 149–157. [Google Scholar]
- Ng, T.W.; Watts, G.F.; Farvid, M.S.; Chan, D.C.; Barrett, P.H. Adipocytokines and VLDL metabolism: Independent regulatory effects of adiponectin, insulin resistance, and fat compartments on VLDL apolipoprotein B-100 kinetics? Diabetes 2005, 54, 795–802. [Google Scholar] [CrossRef] [PubMed]
- Shirakawa, T.; Nakajima, K.; Yatsuzuka, S.; Shimomura, Y.; Kobayashi, J.; Machida, T.; Sumino, H.; Murakami, M. The role of circulating lipoprotein lipase and adiponectin on the particle size of remnant lipoproteins in patients with diabetes mellitus and metabolic syndrome. Clin. Chim. Acta Int. J. Clin. Chem. 2015, 440, 123–132. [Google Scholar] [CrossRef]
- Lucero, D.; Zago, V.; Lopez, G.H.; Cacciagiu, L.; Lopez, G.I.; Wikinski, R.; Nakajima, K.; Schreier, L. Predominance of large VLDL particles in metabolic syndrome, detected by size exclusion liquid chromatography. Clin. Biochem. 2012, 45, 293–297. [Google Scholar] [CrossRef] [PubMed]
- Tan, C.E.; Foster, L.; Caslake, M.J.; Bedford, D.; Watson, T.D.; McConnell, M.; Packard, C.J.; Shepherd, J. Relations between plasma lipids and postheparin plasma lipases and VLDL and LDL subfraction patterns in normolipemic men and women. Arterioscler. Thromb. Vasc. Biol. 1995, 15, 1839–1848. [Google Scholar] [CrossRef]
- Carr, M.C.; Hokanson, J.E.; Zambon, A.; Deeb, S.S.; Barrett, P.H.; Purnell, J.Q.; Brunzell, J.D. The contribution of intraabdominal fat to gender differences in hepatic lipase activity and low/high density lipoprotein heterogeneity. J. Clin. Endocrinol. Metab. 2001, 86, 2831–2837. [Google Scholar] [CrossRef] [PubMed]
- Conlon, D.M.; Welty, F.K.; Reyes-Soffer, G.; Amengual, J. Sex-Specific Differences in Lipoprotein Production and Clearance. Arterioscler. Thromb. Vasc. Biol. 2023, 43, 1617–1625. [Google Scholar] [CrossRef] [PubMed]
- Palmisano, B.T.; Zhu, L.; Stafford, J.M. Role of Estrogens in the Regulation of Liver Lipid Metabolism. Adv. Exp. Med. Biol. 2017, 1043, 227–256. [Google Scholar] [CrossRef]
- Holven, K.B.; Roeters van Lennep, J. Sex differences in lipids: A life course approach. Atherosclerosis 2023, 384, 117270. [Google Scholar] [CrossRef]
- Rashid, S.; Watanabe, T.; Sakaue, T.; Lewis, G.F. Mechanisms of HDL lowering in insulin resistant, hypertriglyceridemic states: The combined effect of HDL triglyceride enrichment and elevated hepatic lipase activity. Clin. Biochem. 2003, 36, 421–429. [Google Scholar] [CrossRef]
- Stadler, J.T.; Lackner, S.; Morkl, S.; Trakaki, A.; Scharnagl, H.; Borenich, A.; Wonisch, W.; Mangge, H.; Zelzer, S.; Meier-Allard, N.; et al. Obesity Affects HDL Metabolism, Composition and Subclass Distribution. Biomedicines 2021, 9, 242. [Google Scholar] [CrossRef]
- Shannon, G.; Jansen, M.; Williams, K.; Caceres, C.; Motta, A.; Odhiambo, A.; Eleveld, A.; Mannell, J. Gender equality in science, medicine, and global health: Where are we at and why does it matter? Lancet 2019, 393, 560–569. [Google Scholar] [CrossRef] [PubMed]
- Roeters van Lennep, J.E.; Tokgozoglu, L.S.; Badimon, L.; Dumanski, S.M.; Gulati, M.; Hess, C.N.; Holven, K.B.; Kavousi, M.; Kayikcioglu, M.; Lutgens, E.; et al. Women, lipids, and atherosclerotic cardiovascular disease: A call to action from the European Atherosclerosis Society. Eur. Heart J. 2023, 44, 4157–4173. [Google Scholar] [CrossRef] [PubMed]
Healthy | MS | |||||
---|---|---|---|---|---|---|
Variable | Female (N = 31) | Male (N = 34) | p-Value | Female (N = 31) | Male (N = 34) | p-Value |
Age (years) | 52.0 (47.0, 57.0) | 57.0 (53.8, 61.0) | 0.002 | 56.0 (49.0, 60.0) | 57.50 (52.0, 60.0) | 0.808 |
BMI (kg/m2) | 24.6 (23.7, 26.0) | 27.12 (23.5, 29.2) | 0.037 | 32.8 (30.1, 39.8) | 32.4 (29.5, 34.8) | 0.222 |
Waist circumference (cm) | 85.0 (81.5, 87.0) | 98.0 (94.0, 104.8) | <0.001 | 110.0 (103.5, 119.0) | 114.0 (107.0, 125.0) | 0.193 |
HR (beats/min) | 65.0 (58.5, 70.0) | 62.50 (58.0, 69.8) | 0.693 | 72.0 (68.5, 76.0) | 73.00 (65.3, 76.0) | 0.519 |
SBP (mm Hg) | 120.0 (112.5, 125.0) | 125.0 (115.0, 130.0) | 0.218 | 140.0 (130.0, 145.0) | 140.0 (130.0, 145.0) | 0.685 |
DBP (mm Hg) | 70.0 (70.0, 80.0) | 80.0 (70.0, 80.0) | 0.136 | 80.0 (80.0, 80.0) | 80.0 (80.0, 80.0) | 0.411 |
MAP (mmHg) | 86.7 (84.2, 95.0) | 93.3 (85.4, 96.7) | 0.125 | 98.33 (96.7, 101.7) | 99.2 (96.7, 103.3) | 0.947 |
Chronic diseases | ||||||
High blood pressure | 0 (0.0%) | 0 (0.0%) | 29 (93.5%) | 31 (91.2%) | 0.720 | |
Diabetes mellitus type 2 | 0 (0.0%) | 0 (0.0%) | 20 (64.5%) | 7 (20.6%) | <0.001 | |
Functions and habits | ||||||
Physical activity (≥3 times/week) | 27 (87.1%) | 31 (91.2%) | 0.596 | 19 (61.3%) | 28 (82.4%) | 0.058 |
Menstrual cycle | 12/31 (38.7%) | 6/31 (19.4%) |
Healthy | MS | |||||
---|---|---|---|---|---|---|
Variable | Female (N = 31) | Male (N = 34) | p-Value | Female (N = 31) | Male (N = 34) | p-Value |
Adiponectin (µg/mL) | 20.20 (14.75, 25.90) | 13.10 (10.00, 16.65) | <0.001 | 14.90 (11.85, 18.50) | 10.60 (8.80, 13.82) | 0.002 |
TG (mmol/L) | 0.99 (0.81, 1.25) | 1.11 (0.79, 1.39) | 0.442 | 1.52 (1.05, 2.13) | 1.71 (1.16, 2.58) | 0.325 |
TC (mmol/L) | 5.41 (5.12, 5.95) | 5.62 (5.13, 5.97) | 0.660 | 4.84 (4.26, 5.94) | 5.25 (4.32, 6.54) | 0.386 |
LDL-C (mmol/L) | 3.04 (2.76, 3.71) | 3.35 (2.95, 4.01) | 0.279 | 2.83 (2.33, 3.56) | 3.12 (2.39, 3.93) | 0.379 |
HDL-C (mmol/L) | 1.66 (1.47, 2.01) | 1.50 (1.33, 1.81) | 0.084 | 1.22 (1.12, 1.44) | 1.14 (0.91, 1.40) | 0.070 |
Glucose (mmol/L) | 4.88 (4.69, 5.13) | 5.08 (4.84, 5.49) | 0.027 | 5.66 (5.30, 6.60) | 5.66 (5.36, 6.33) | 0.963 |
Protein (g/L) | 71.00 (69.00, 74.00) | 73.00 (69.00, 75.00) | 0.418 | 75.00 (72.00, 77.00) | 74.00 (71.00, 77.00) | 0.589 |
Albumin (g/L) | 47.00 (46.00, 48.00) | 47.50 (46.00, 50.00) | 0.235 | 48.00 (45.50, 49.00) | 48.00 (45.00, 49.75) | 0.995 |
CRP (µg/mL) | 0.90 (0.70, 1.85) | 1.45 (0.54, 2.90) | 0.176 | 2.40 (1.75, 6.75) | 2.60 (1.12, 4.25) | 0.354 |
IL-6 (pg/mL) | 2.10 (1.36, 2.85) | 2.50 (1.90, 3.98) | 0.129 | 6.00 (3.50, 8.10) | 3.95 (2.50, 5.60) | 0.008 |
Bilirubin (µmol/L) | 7.87 (5.47, 11.54) | 10.43 (7.87, 15.18) | 0.010 | 5.99 (4.62, 8.12) | 9.66 (7.35, 11.12) | 0.001 |
AST (U/L) | 21.00 (18.00, 25.00) | 23.00 (21.25, 24.75) | 0.116 | 23.00 (19.00, 32.50) | 23.00 (20.00, 30.50) | 0.703 |
ALT (U/L) | 19.00 (14.00, 23.00) | 24.00 (20.00, 36.00) | 0.001 | 28.00 (20.00, 41.00) | 32.50 (23.50, 43.75) | 0.210 |
AP (U/L) | 60.00 (51.00, 70.50) | 59.00 (48.75, 67.75) | 0.870 | 71.00 (62.00, 84.00) | 60.00 (51.00, 67.50) | 0.006 |
GGT (U/L) | 13.00 (11.00, 16.00) | 27.00 (16.25, 41.25) | <0.001 | 23.00 (17.00, 29.00) | 37.50 (31.00, 55.25) | <0.001 |
CK (U/L) | 93.00 (67.00, 136.00) | 126.00 (97.00, 163.50) | 0.056 | 119.00 (70.00, 195.50) | 169.50 (98.75, 254.00) | 0.033 |
LDH (U/L) | 173.00 (157.00, 188.00) | 163.50 (145.50, 191.75) | 0.325 | 178.00 (147.50, 194.50) | 174.50 (160.50, 191.25) | 0.713 |
Urea (mmol/L) | 4.32 (3.90, 5.06) | 5.73 (4.57, 6.31) | <0.001 | 5.48 (4.90, 6.97) | 5.73 (4.81, 6.31) | 0.608 |
Urate (µmol/L) | 232.05 (199.32, 249.90) | 318.32 (285.60, 361.46) | <0.001 | 297.50 (249.90, 321.30) | 345.10 (315.35, 377.83) | 0.001 |
Creatinine (µmol/L) | 69.03 (64.16, 73.90) | 88.06 (78.99, 93.81) | <0.001 | 66.38 (61.06, 73.01) | 84.08 (78.77, 90.27) | <0.001 |
eGFR (mL/min/1.73 m2) | 88.30 (78.53, 95.28) | 85.86 (75.94, 93.33) | 0.537 | 87.97 (77.23, 99.04) | 89.01 (82.74, 97.52) | 0.941 |
Sodium (mmol/L) | 140.00 (138.00, 141.50) | 140.00 (139.00, 141.00) | 0.695 | 139.00 (137.50, 140.00) | 140.00 (138.00, 140.75) | 0.378 |
Potassium (mmol/L) | 4.10 (3.95, 4.30) | 4.40 (4.20, 4.60) | 0.005 | 4.20 (4.10, 4.60) | 4.20 (4.03, 4.60) | 0.833 |
Chloride (mmol/L) | 101.00 (99.00, 103.00) | 101.00 (100.00, 103.00) | 0.601 | 100.00 (97.50, 101.50) | 100.00 (98.00, 101.00) | 0.953 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Klobučar, I.; Habisch, H.; Klobučar, L.; Trbušić, M.; Pregartner, G.; Berghold, A.; Kostner, G.M.; Scharnagl, H.; Madl, T.; Frank, S.; et al. Sex-Related Differences in the Associations between Adiponectin and Serum Lipoproteins in Healthy Subjects and Patients with Metabolic Syndrome. Biomedicines 2024, 12, 1972. https://doi.org/10.3390/biomedicines12091972
Klobučar I, Habisch H, Klobučar L, Trbušić M, Pregartner G, Berghold A, Kostner GM, Scharnagl H, Madl T, Frank S, et al. Sex-Related Differences in the Associations between Adiponectin and Serum Lipoproteins in Healthy Subjects and Patients with Metabolic Syndrome. Biomedicines. 2024; 12(9):1972. https://doi.org/10.3390/biomedicines12091972
Chicago/Turabian StyleKlobučar, Iva, Hansjörg Habisch, Lucija Klobučar, Matias Trbušić, Gudrun Pregartner, Andrea Berghold, Gerhard M. Kostner, Hubert Scharnagl, Tobias Madl, Saša Frank, and et al. 2024. "Sex-Related Differences in the Associations between Adiponectin and Serum Lipoproteins in Healthy Subjects and Patients with Metabolic Syndrome" Biomedicines 12, no. 9: 1972. https://doi.org/10.3390/biomedicines12091972