Analysis of the Association between Metabolic Syndrome and Renal Function in Middle-Aged Patients with Diabetes
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Participants
2.2. Measures
2.2.1. Demographic and Disease Characteristics and Metabolic Syndrome
2.2.2. Biochemical Measurements
2.2.3. Renal Function
2.3. Analytic Strategy
3. Results
3.1. Demographic and Clinical Characteristics
3.2. eGFR According to the General Characteristics
3.3. Association for Metabolic Syndrome among the Subitems and the eGFR
3.4. Correlation of Metabolic Syndrome among the Sub-Items with the eGFR
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bae, J.H.; Han, K.D.; Ko, S.H.; Yang, Y.S.; Choi, J.H.; Choi, K.M.; Kwon, H.S.; Won, K.C. Diabetes fact sheet in Korea. Diabetes Metab. J. 2022, 46, 417–426. [Google Scholar] [CrossRef]
- Organisation for Economic Co-operation and Development. Available online: https://stats.oecd.org/Index.aspx?QueryId=28240# (accessed on 4 July 2022).
- Sun, H.; Saeedi, P.; Karuranga, S.; Pinkepank, M.; Ogurtsova, K.; Duncan, B.; Stein, C.; Basit, A.; Chan, J.; Mbanya, J.C.; et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res. Clin. Pract. 2022, 183, 109119. [Google Scholar] [CrossRef]
- Tietjen, A.K.; Ghandour, R.; Mikki, N.; Jerdén, L.; Eriksson, J.W.; Norberg, M.; Husseini, A. Complications of type 2 diabetes mellitus in Ramallah and al-Bireh: The Palestinian diabetes complications and control study (PDCCS). Qual Life Res. 2021, 30, 547–557. [Google Scholar] [CrossRef]
- Wang, Q.; Xu, G. Chronic kidney disease in patients with diabetes: Diabetic vs. Non-diabetic kidney etiologies. J. Diabet. Res. Rev. Rep. 2022, 4, 1–3. [Google Scholar]
- Porrini, E.; Ruggenenti, P.; Mogensen, C.E.; Barlovic, D.P.; Praga, M.; Cruzado, J.M.; Hojs, R.; Abbate, M.; de Vries, A.P.; ERA-EDTA Diabesity Working Group. Non-proteinuric pathways in loss of renal function in patients with type 2 diabetes. Lancet Diabetes Endocrinol. 2015, 3, 382–391. [Google Scholar] [CrossRef]
- Harjutsalo, V.; Groop, P.H. Epidemiology and risk factors for diabetic kidney disease. Adv. Chronic Kidney Dis. 2014, 21, 260–266. [Google Scholar] [CrossRef]
- Hudish, L.I.; Reusch, J.E.; Sussel, L. Β cell dysfunction during progression of metabolic syndrome to type 2 diabetes. J. Clin. Investig. 2019, 129, 4001–4008. [Google Scholar] [CrossRef]
- Jung, C.H.; Son, J.W.; Kang, S.; Kim, W.J.; Kim, H.; Kim, H.S.; Seo, M.; Shin, H.; Lee, S.; Jeong, S.J. Diabetes fact sheets in korea, 2020: An appraisal of current status. Diabetes Metab. J. 2021, 45, 1–10. [Google Scholar] [CrossRef]
- Li, J.; Shangguan, H.; Chen, X.; Ye, X.; Zhong, B.; Chen, P.; Wang, Y.; Xin, B.; Bi, Y.; Zhu, D. Advanced glycation end product levels were correlated with inflammation and carotid atherosclerosis in type 2 diabetes patients. Open Life Sci. 2020, 15, 364–372. [Google Scholar] [CrossRef]
- Choi, H.; Koo, D.; Yim, J. Correlation of advanced glycation end products and heme oxygenase-1 in Korean diabetic patients. J. Nutr. Health 2022, 55, 348–358. [Google Scholar] [CrossRef]
- Expert Panel on Detection, Evaluation, and Treatment of High Cholesterol in Adult. Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 2001, 285, 2486–2497. [Google Scholar] [CrossRef]
- Park, S.; Lee, W.; Kim, S. The relative risks of the metabolic syndrome defined by adult treatment panel iii according to insulin resistance in Korean population. J. Korean Med. Sci. 2003, 64, 552–560. [Google Scholar]
- Haffner, S.M.; Valdez, R.A.; Hazuda, H.P.; Mitchell, B.D.; Morales, P.A.; Stern, M.P. Prospective analysis of the insulin-resistance syndrome (syndrome x). Diabetes 1992, 41, 715–722. [Google Scholar] [CrossRef]
- Hong, E. The mediating effect of self-efficacy in the relationship between diabetes knowledge and health promoting behaviors: Focus on gender differentiation. J. Korean Acad. Soc. Nurs. Educ. 2015, 21, 509–517. [Google Scholar] [CrossRef]
- Statistics Korea. Statistics Korea Government Official Work Conference. Available online: http://www.index.go.kr/unify/idx-info.do?idxCd=8021 (accessed on 4 June 2022).
- Ha, K.; Song, Y. Associations of meal timing and frequency with obesity and metabolic syndrome among Korean adults. Nutrients 2019, 11, 2437. [Google Scholar] [CrossRef] [PubMed]
- Stevens, L.A.; Coresh, J.; Greene, T.; Levey, A.S. Assessing kidney function—Measured and estimated glomerular filtration rate. N. Engl. J. Med. 2006, 354, 2473–2483. [Google Scholar] [CrossRef]
- National Kidney Foundation. Estimated Glomerular Filtration Rate(eGFR). Available online: https://www.kidney.org/atoz/content/gfr (accessed on 3 May 2022).
- Brar, A.; Markell, M. Impact of gender and gender disparities in patients with kidney disease. Curr. Opin. Nephrol. Hypertens. 2019, 28, 178–182. [Google Scholar] [CrossRef]
- Neugarten, J.; Golestaneh, L. Gender and the prevalence and progression of renal disease. Adv. Chronic Kidney Dis. 2013, 20, 390–395. [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]
- Ricardo, A.C.; Yang, W.; Sha, D.; Appel, L.J.; Chen, J.; Krousel-Wood, M.; Manoharan, A.; Steigerwalt, S.; Wright, J.; Rahman, M.; et al. Sex-Related Disparities in CKD Progression. J. Am. Soc. Nephrol. 2019, 30, 137–146. [Google Scholar] [CrossRef]
- Maric, C. Sex, diabetes and the kidney. Am. J. Physiol. Renal Physiol. 2009, 296, F680–F688. [Google Scholar] [CrossRef] [PubMed]
- Cherney, D.Z.; Sochett, E.B.; Miller, J.A. Gender differences in renal responses to hyperglycemia and angiotensin-converting enzyme inhibition in diabetes. Kidney Int. 2005, 68, 1722–1728. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, M.K.; Katon, W.; Young, B.A. Associations between sex and incident chronic kidney disease in a prospective diabetic cohort. Nephrology 2015, 20, 451–458. [Google Scholar] [CrossRef] [PubMed]
- Earle, K.A.; Ng, L.; White, S.; Zitouni, K. Sex differences in vascular stiffness and relationship to the risk of renal functional decline in patients with type 2 diabetes. Diab. Vasc. Dis. Res. 2017, 14, 304–309. [Google Scholar] [CrossRef] [PubMed]
- Alicic, R.Z.; Rooney, M.T.; Tuttle, K.R. Diabetic kidney disease: Challenges, progress, and possibilities. Clin. J. Am. Soc. Nephrol. 2017, 12, 2032–2045. [Google Scholar] [CrossRef]
- Thomas, B. The global burden of diabetic kidney disease: Time trends and gender gaps. Curr. Diab. Rep. 2019, 19, 18. [Google Scholar] [CrossRef]
- Cosmo, S.D.; Lamacchia, O.; Rauseo, A.; Viti, R.; Gesualdo, L.; Pilotti, A.; Trischitta, V.; Cignarelli, M. Cigarette smoking is associated with low glomerular filtration rate in male patients with type 2 diabetes. Diabetes Care 2006, 29, 2467–2470. [Google Scholar] [CrossRef]
- Barnett, A. Diabetics exposed to telmisartan and enalapril study group. Angiotensin-receptor blockade versus converting-enzyme inhibition in type 2 diabetes and nephropathy. N. Engl. J. Med. 2004, 351, 1952–1961. [Google Scholar] [CrossRef]
- Statistics Korea. Risk Factors of Metabolic Syndrome by Age and Gender. Available online: https://kosis.kr/statHtml/statHtml.do?orgId=350&tblId=DT_35007_N139 (accessed on 12 June 2022).
- Lim, D.M.; Park, K.Y.; Kim, B.J.; Lee, K.W.; Lee, M.J.; Yom, Y.S.; Koh, G.P. Cardiovascular risk according to the components of metabolic syndrome in type 2 diabetes. J. Korean Diabetes 2009, 10, 196–203. [Google Scholar] [CrossRef]
- Katsiki, N.; Anagnostis, P.; Kotsa, K.; Goulis, D.G.; Mikhailidis, D.P. Obesity, metabolic syndrome and the risk of microvascular complications in patients with diabetes mellitus. Curr. Pharm. Des. 2019, 25, 2051–2059. [Google Scholar] [CrossRef]
- Costa, L.A.; Canani, L.H.; Lisboa, H.R.; Tres, G.S.; Gross, J.L. Aggregation of features of the metabolic syndrome is associated with increased prevalence of chronic complications in type 2 diabetes. Diabetes Med. 2004, 21, 252–255. [Google Scholar] [CrossRef] [PubMed]
- Essafi, M.A.; Aynaou, H.; Salhi, H.; Ouahabi, H.E. Metabolic syndrome in patients with diabetes mellitus. Cureus 2022, 14, e24469. [Google Scholar] [CrossRef] [PubMed]
- Cho, I.; Kim, Y.; Chae, Y.; Kim, T.; Yun, S.J.; Lee, S.; Kim, W.; Kim, Y. Effects of metabolic syndrome on chronic kidney disease. Korean J. Urol. 2009, 50, 261–266. [Google Scholar] [CrossRef]
- Boo, S.Y.; Yoon, J.; Oh, H. Evaluating the prevalence, awareness, and control of hypertension, diabetes, and dyslipidemia in Korea using the NHIS-NSC database: A cross-sectional analysis. Medicine 2018, 97, e13713. [Google Scholar] [CrossRef] [PubMed]
- Anagnostis, P.; Bitzer, J.; Cano, A.; Ceausu, I.; Chedraui, P.; Durmusoglu, F.; Erkkola, R.; Goulis, D.G.; Hirschberg, A.L.; Kiesel, L. Menopause symptom management in women with dyslipidemias: An EMAS clinical guide. Maturitas 2020, 135, 82–88. [Google Scholar] [CrossRef] [PubMed]
- Lym, Y.L.; Hwang, S.W.; Shim, H.J.; Oh, E.H.; Chang, Y.S.; Cho, B.L. Prevalence and risk factors of the metabolic syndrome as defined by NCEP-ATP III. J. Korean Acad. Fam. Med. 2003, 24, 135–143. [Google Scholar]
- Paley, C.A.; Johnson, M.I. Abdominal obesity and metabolic syndrome: Exercise as medicine? BMC Sports Sci. Med. Rehabil. 2018, 10, 7. [Google Scholar] [CrossRef]
- Lee, H.; Lee, M.; Park, G.; Khang, A.R. Prevalence of chronic diabetic complications in patients with type 2 diabetes mellitus: A retrospective study based on the National Health Insurance Service-National Health Screening Cohort in Korea, 2002~2015. Korean J. Adult Nurs. 2022, 34, 39–50. [Google Scholar] [CrossRef]
- Haghighatpanah, M.; Nejad, A.S.; Haghighatpanah, M.; Thunga, G.; Mallayasamy, S. Factors that Correlate with Poor Glycemic Control in Type 2 Diabetes Mellitus Patients with Complications. Osong Public Health Res. Perspect. 2018, 9, 167–174. [Google Scholar] [CrossRef]
- Moehlecke, M.; Leitão, C.B.; Kramer, C.K.; Rodrigues, T.C.; Nickel, C.; Silveiro, S.P.; Gross, J.L.; Canani, L. Effect of metabolic syndrome and of its individual components on renal function of patients with type 2 diabetes mellitus. Braz. J. Med. Biol. Res. 2010, 43, 687–693. [Google Scholar] [CrossRef] [Green Version]
Category | Male (n = 153) | Female (n = 126) | p |
---|---|---|---|
N (%), M ± SD | N (%), M ± SD | ||
Age, years | 56.05 ± 6.31 | 57.51 ± 5.65 | 0.051 |
House Income | |||
Lowest | 24 (15.7) | 23 (18.3) | 0.682 |
Lower middle | 35 (22.9) | 33 (26.2) | |
Upper middle | 43 (28.1) | 36 (28.6) | |
Highest | 51 (33.3) | 34 (27.0) | |
Education, years | |||
0–6 | 14 (9.2) | 30 (23.8) | 0.001 |
7–9 | 20 (13.1) | 21 (16.7) | |
10–12 | 48 (31.4) | 41 (32.5) | |
≥13 | 54 (35.3) | 25 (19.8) | |
Smoking | |||
No | 22 (14.4) | 111 (88.1) | 0.000 |
Yes | 131 (85.6) | 15 (11.9) | |
Hypertension | |||
No | 70 (45.8) | 71 (56.3) | 0.078 |
Yes | 83 (54.2) | 55 (43.7) | |
Dyslipidemia | |||
No | 67 (43.8) | 41 (32.5) | 0.055 |
yes | 86 (56.2) | 85 (67.5) | |
Duration of diabetes, years | 8.77 ± 7.88 | 6.60 ± 5.67 | 0.011 |
Waist circumference, cm | 92.71 ± 9.00 | 86.43 ± 8.93 | 0.000 |
Body mass index, kg/m2 | 25.86 ± 3.63 | 25.33 ± 3.41 | 0.221 |
Systolic blood pressure, mmHg | 123.17 ± 14.18 | 121.89 ± 14.87 | 0.467 |
Diastolic blood pressure, mmHg | 78.87 ± 9.54 | 74.87 ± 8.19 | 0.000 |
Fasting blood glucose, mg/dL | 146.98 ± 47.12 | 133.63 ± 37.21 | 0.012 |
HbA1C, % | 7.46 ± 1.30 | 7.33 ± 1.52 | 0.465 |
Triglyceride, mg/d | 180.75 ± 141.39 | 133.75 ± 71.84 | 0.001 |
HDL-cholesterol, mg/dL | 44.15 ± 10.62 | 48.84 ± 11.17 | 0.001 |
LDL-cholesterol, mg/dL | 96.35 ± 32.95 | 98.15 ± 31.30 | 0.861 |
Total cholesterol, mg/dL | 146.98 ± 39.49 | 168.61 ± 40.20 | 0.191 |
Blood urea nitrogen, mg/dL | 16.38 ± 5.69 | 15.09 ± 4.61 | 0.045 |
Creatinine, mg/dL | 0.97 ± 0.60 | 0.67 ± 0.13 | 0.000 |
Albuminuria, mg/dL | 70.60 ± 243.85 | 31.61 ± 118.93 | 0.114 |
Metabolic syndrome | |||
No | 30 (19.6) | 23 (18.2) | 0.717 |
Yes | 119 (77.8) | 102 (81.0) | |
Unmeasurable | 4 (2.6) | 1 (0.8) | |
eGFR, mL/min/1.73 m2 | 90.29 ± 15.33 | 95.16 ± 11.07 | 0.003 |
Category | eGFR, mL/min/1.73 m 2 | p | |
---|---|---|---|
≥90 (n = 189) | <90 (n = 90) | ||
Gender | |||
Male | 91 (48.1) | 62 (68.9) | 0.001 |
Female | 98 (51.9) | 28 (31.1) | |
Age, years | 56.14 ± 6.29 | 57.83 ± 5.37 | 0.029 |
House Income | |||
Lowest | 30 (15.9) | 17 (18.9) | 0.411 |
Lower middle | 48 (25.4) | 20 (22.2) | |
Upper middle | 58 (30.7) | 21 (23.3) | |
Highest | 53 (28.0) | 32 (35.6) | |
Education, years | 0.534 | ||
0–6 | 28 (14.8) | 16 (17.8) | |
7–9 | 27 (14.3) | 14 (15.6) | |
10–12 | 66 (34.9) | 23 (25.6) | |
≥13 | 52 (27.5) | 27 (30.0) | |
Smoking | 0.077 | ||
No | 97 (51.3) | 36(40.0) | |
Yes | 92 (48.7) | 54(60.0) | |
Hypertension | 0.901 | ||
No | 96 (50.8) | 45 (50.0) | |
Yes | 93 (49.2) | 45 (50.0) | |
Dyslipidemia | 0.125 | ||
No | 79 (41.8) | 29 (32.2) | |
Yes | 110 (58.2) | 61 (67.8) | |
Duration of diabetes, years | 7.13 ± 6.41 | 9.12 ± 8.36 | 0.024 |
Waist circumference, cm | 89.38 ± 8.74 | 90.93 ± 10.88 | 0.206 |
Body mass index, kg/m2 | 25.68 ± 3.41 | 25.47 ± 3.82 | 0.649 |
Systolic blood pressure, mmHg | 121.68 ± 13.64 | 124.52 ± 16.07 | 0.132 |
Diastolic blood pressure, mmHg | 76.59 ± 9.12 | 78.10 ± 9.06 | 0.203 |
Fasting blood glucose, mg/dL | 140.29 ± 41.53 | 141.97 ± 46.81 | 0.766 |
HbA1C, mg/dL | 7.39 ± 1.42 | 7.42 ± 1.38 | 0.890 |
Triglyceride, mg/dL | 161.48 ± 112.69 | 154.62 ± 125.64 | 0.651 |
HDL-cholesterol, mg/dL | 46.81 ± 11.11 | 45.29 ± 11.08 | 0.289 |
LDL-cholesterol, mg/dL | 99.63 ± 31.39 | 90.68 ± 34.30 | 0.325 |
Total cholesterol, mg/dL | 156.33 ± 34.47 | 169.61 ± 41.73 | 0.010 |
Metabolic syndrome | 0.646 | ||
No | 37 (19.6) | 16 (17.8) | |
Yes | 147 (77.8) | 74 (82.2) | |
Unmeasurable | 2 (2.6) |
Category | Male | Female | ||
---|---|---|---|---|
OR (CI) | p | OR (CI) | p | |
eGFR, mL/min/1.73 m2 | 0.99 (0.96–1.02) | 0.617 | 1.03 (0.98–1.09) | 0.260 |
Systolic blood pressure, mmHg | 1.07 (1.02–1.13) | 0.008 | 10.36 (0.99–1.09) | 0.163 |
Diastolic blood pressure, mmHg | 1.00 (0.93–1.08) | 0.998 | 0.96 (0.88–1.04) | 0.314 |
Waist circumference, cm | 1.11 (1.03–1.19) | 0.004 | 1.14 (1.04–1.24) | 0.005 |
Fasting blood glucose, mg/dL | 1.00 (0.99–1.01) | 0.839 | 0.99 (0.98–1.01) | 0.435 |
Triglyceride, mg/dL | 1.00 (1.00–1.01) | 0.383 | 1.01 (0.99–1.02) | 0.390 |
HDL-cholesterol, mg/dL | 0.96 (0.91–1.00) | 0.060 | 0.89 (0.83–0.95) | 0.001 |
BPsys, mmHg | BPdia, mmHg | WC | FBS | HDL-C | TG | |
---|---|---|---|---|---|---|
BPsys, mmHg | 1 | |||||
BPdia, mmHg | 0.55 (0.000) | 1 | ||||
WC, cm | 0.26 (0.000) | 0.37 (0.000) | 1 | |||
FBS, mg/dL | 0.21 (0.001) | 0.20 (0.001) | 0.12 (0.059) | 1 | ||
HDL-C, mg/dL | 0.03 (0.687) | −0.09 (0.144) | −0.19 (0.002) | −0.04 (0.482) | 1 | |
TG, mg/dL | 0.16 (0.008) | 0.25 (0.000) | 0.12 (0.049) | 0.29 (0.000) | −0.30 (0.000) | 1 |
eGFR, mL/min/1.73 m2 | 0.12 (0.049) | 0.02 (0.729) | 0.02 (0.719) | 0.02 (0.809) | 0.09 (0.165) | 0.07 (0.225) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Park, Y.; Lee, S.J. Analysis of the Association between Metabolic Syndrome and Renal Function in Middle-Aged Patients with Diabetes. Int. J. Environ. Res. Public Health 2022, 19, 11832. https://doi.org/10.3390/ijerph191811832
Park Y, Lee SJ. Analysis of the Association between Metabolic Syndrome and Renal Function in Middle-Aged Patients with Diabetes. International Journal of Environmental Research and Public Health. 2022; 19(18):11832. https://doi.org/10.3390/ijerph191811832
Chicago/Turabian StylePark, Yoonjin, and Su Jung Lee. 2022. "Analysis of the Association between Metabolic Syndrome and Renal Function in Middle-Aged Patients with Diabetes" International Journal of Environmental Research and Public Health 19, no. 18: 11832. https://doi.org/10.3390/ijerph191811832
APA StylePark, Y., & Lee, S. J. (2022). Analysis of the Association between Metabolic Syndrome and Renal Function in Middle-Aged Patients with Diabetes. International Journal of Environmental Research and Public Health, 19(18), 11832. https://doi.org/10.3390/ijerph191811832