Skip to main content
Log in

Relationship between dyslipidemia and albuminuria in prediabetic adults: The Korea National Health and Nutrition Examination Survey 2011–2012

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

This study aimed to estimate the relationship between various lipid abnormalities and albuminuria in Korean prediabetic adults. Data obtained from the Korea National Health and Nutrition Examination Survey (KNHANES) 2011–2012 were analyzed. The study consisted of 4,811 subjects in the normal glucose group and 3,872 in the prediabetic group. Prediabetes was defined by the fasting plasma glucose or hemoglobin A1c level. Albuminuria was defined as a urine albumin to creatinine ratio (UACR) ≥30 mg/g. Various parameters of dyslipidemia were assessed. No differences were observed in the prevalence of lipid abnormalities in prediabetic men with different values of UACR. Prediabetic women with increased urinary albumin excretion showed a significantly higher prevalence of lipid abnormalities. The proportion of mixed dyslipidemia was significantly higher in prediabetic women with albuminuria. Higher levels of total cholesterol, triglyceride (TG), low-density lipoprotein cholesterol (LDL-C), non-high-density lipoprotein cholesterol (non-HDL-C), and TC to HDL-C ratio, TG to HDL-C ratio, and LDL-C to HDL-C ratio were significantly associated with increased risk of albuminuria in prediabetic women. Conclusions: Several lipid abnormalities were significantly associated with the increased risk of albuminuria in prediabetic women. Hence, screening for lipid abnormalities may be helpful for identification of risk for albuminuria in prediabetic subjects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. M.H. Lee, H.C. Kim, S.V. Ahn, N.W. Hur, D.P. Choi, C.G. Park, I. Suh, Prevalence of dyslipidemia among Korean adults: Korea National Health and Nutrition Survey 1998–2005. Diabetes Metab J 36, 43–55 (2012)

    Article  PubMed Central  PubMed  Google Scholar 

  2. A.N. Habib, B.C. Baird, J.K. Leypoldt, A.K. Cheung, A.S. Goldfarb-Rumyantzev, The association of lipid levels with mortality in patients on chronic peritoneal dialysis. Nephrol. Dial. Transplant. 21, 2881–2892 (2006)

    Article  PubMed  Google Scholar 

  3. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. 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 285, 2486–2497 (2001)

    Article  Google Scholar 

  4. S.M. Boekholdt, B.J. Arsenault, S. Mora, T.R. Pedersen, J.C. LaRosa, P.J. Nestel, R.J. Simes, P. Durrington, G.A. Hitman, K.M. Welch, D.A. DeMicco, A.H. Zwinderman, M.B. Clearfield, J.R. Downs, A.M. Tonkin, H.M. Colhoun, A.M. Gotto Jr, P.M. Ridker, J.J. Kastelein, Association of LDL cholesterol, non-HDL cholesterol, and apolipoprotein B levels with risk of cardiovascular events among patients treated with statins: a meta-analysis. JAMA 307, 1302–1309 (2012)

    Article  CAS  PubMed  Google Scholar 

  5. F. Barzi, A. Patel, M. Woodward, C.M. Lawes, T. Ohkubo, D. Gu, T.H. Lam, H. Ueshima, Asia Pacific Cohort Studies Collaboration, A comparison of lipid variables as predictors of cardiovascular disease in the Asia Pacific region. Ann. Epidemiol. 15, 405–413 (2005)

    Article  CAS  PubMed  Google Scholar 

  6. American Diabetes Association, Diagnosis and classification of diabetes mellitus. Diabetes Care 37, S81–S90 (2014)

    Article  Google Scholar 

  7. D.J. Kim, The epidemiology of diabetes in Korea. Diabetes Metab J 35, 303–308 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

  8. S. Wild, G. Roglic, A. Green, R. Sicree, H. King, Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27, 1047–1053 (2004)

    Article  PubMed  Google Scholar 

  9. M.S. Player, V.A. Diaz, A.G. Mainous 3rd, S.H. Gregorie, M.E. Knoll, C.J. Everett, Ethnic differences in the relationship of prediabetes with the presence of target-organ disease. Diabetes Metab 37, 403–409 (2011)

    Article  CAS  PubMed  Google Scholar 

  10. H. Wang, N.M. Shara, D. Calhoun, J.G. Umans, E.T. Lee, B.V. Howard, Incidence rates and predictors of diabetes in those with prediabetes: the strong heart study. Diabetes Metab Res Rev 26, 378–385 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. H.C. Gerstein, J.F. Mann, Q. Yi, B. Zinman, S.F. Dinneen, B. Hoogwerf, J.P. Hallé, J. Young, A. Rashkow, C. Joyce, S. Nawaz, S. Yusuf, HOPE Study Investigators, Albuminuria and risk ofcardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 286, 421–426 (2001)

    Article  CAS  PubMed  Google Scholar 

  12. P. Hovind, L. Tarnow, P. Rossing, B.R. Jensen, M. Graae, I. Torp, C. Binder, H.H. Parving, Predictors for the development ofmicroalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ (2004). doi:10.1136/bmj.38070.450891.FE

    PubMed Central  PubMed  Google Scholar 

  13. Toyama T, Shimizu M, Furuichi K, Kaneko S, Wada T, (2013) Treatment and impact of dyslipidemia in diabetic nephropathy. ClinExpNephrol18, 201–205

  14. D.P. Agarwal, Cardioprotective effects of light-moderate consumption of alcohol: a review of putative mechanisms. Alcohol Alcohol. 37, 409–415 (2002)

    Article  CAS  PubMed  Google Scholar 

  15. J.Y. Oh, Y.J. Yang, B.S. Kim, J.H. Kang, Validity and reliability of Korean version of International Physical Activity Questionnaire (IPAQ) short form. Korean J Fam Med 28, 532–541 (2007)

    Google Scholar 

  16. W.T. Friedewald, R.I. Levy, D.S. Fredrickson, Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. ClinChem 18, 499–502 (1972)

    CAS  Google Scholar 

  17. S. Natarajan, H. Glick, M. Criqui, D. Horowitz, S.R. Lipsitz, B. Kinosian, Cholesterol measures to identify and treat individuals at risk for coronary heart disease. Am. J. Prev. Med. 25, 50–57 (2003)

    Article  PubMed  Google Scholar 

  18. V. Hanak, J. Munoz, J. Teague, AJr Stanley, AJr Bittner, Accuracy of the triglyceride to high-density lipoprotein cholesterol ratio for prediction of the low-density lipoprotein phenotype B. Am J Cardiol 94, 219–222 (2004)

    Article  CAS  PubMed  Google Scholar 

  19. M.L. Fernandez, D. Webb, The LDL to HDL cholesterol ratio as a valuable tool to evaluate coronary heart disease risk. J Am CollNutr 27, 1–5 (2008)

    CAS  Google Scholar 

  20. P.E. Stevens, A. Levin, Evaluation and management of chronic kidney disease: synopsis of the kidney disease: improving global outcomes 2012 clinical practice guideline. Ann. Intern. Med. 158, 825–830 (2013)

    Article  PubMed  Google Scholar 

  21. A.S. Levey, J. Coresh, T. Greene, L.A. Stevens, Y.L. Zhang, S. Hendriksen, J.W. Kusek, F. Van Lente, Chronic, Kidney Disease Epidemiology Collaboration, Using standardized serumcreatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann. Intern. Med. 145, 247–254 (2006)

    Article  CAS  PubMed  Google Scholar 

  22. I.H. de Boer, B.C. Astor, H. Kramer, W. Palmas, K. Rudser, S.L. Seliger, M.G. Shlipak, D.S. Siscovick, M.Y. Tsai, B. Kestenbaum, Mild elevations of urine albuminexcretion are associated with atherogenic lipoprotein abnormalities in the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis 197(407–414), 13 (2008)

    Google Scholar 

  23. C.M. O’Seaghdha, S.J. Hwang, A. Upadhyay, J.B. Meigs, C.S. Fox, Predictors of incident albuminuria in the Framingham Offspring cohort. Am. J. Kidney Dis. 56, 852–860 (2010)

    Article  PubMed Central  PubMed  Google Scholar 

  24. G.E. Nam, K. Han, Y.G. Park, Y.H. Kim, B. Han, S.M. Kim, Y.S. Choi, K.H. Cho, K.S. Lee, H. do Kim, Prevalence and related risk factors of albuminuria in korean adults: the 2011 Korea national health and nutrition examination survey. NephronClinPract 124, 232–238 (2013)

    Google Scholar 

  25. N. Tolonen, C. Forsblom, L. Thorn, J. Waden, M. Rosengard-Barlund, M. Saraheimo, M. Feodoroff, V.P. Mäkinen, D. Gordin D, M.R. Taskinen MR, P.H. Groop PH, FinnDiane Study Group, Lipid abnormalities predict progression of renal disease in patients with type 1 diabetes. Diabetologia 52, 2522–2530 (2009)

    Article  CAS  PubMed  Google Scholar 

  26. K.J. Tien, S.T. Tu, H.C. Chen, J.Y. Hsiao, M.C. Hsieh, Triglycerides are independently associated with albuminuria in Taiwanese type 2 diabetic patients. J. Endocrinol. Invest. 35, 800–803 (2012)

    CAS  PubMed  Google Scholar 

  27. I.T. Lee, C.Y. Wang, C.N. Huang, C.C. Fu, W.H. Sheu, High triglyceride-to-HDL cholesterol ratio associated with albuminuria in type 2 diabetic subjects. Journal Diabetes Complications 27, 243–247 (2013)

    Article  Google Scholar 

  28. R. Marin, P. Rodriguez, S. Tranche, J. Redon, F. Morales-Olivas, A. Galgo, M.A. Brito, J. Mediavilla, J.V. Lozano, C. Filozof, MAGAL group, Prevalence of abnormalurinary albumin excretion rate in hypertensive patients with impaired fasting glucose and its association with cardiovascular disease. J Am SocNephrol 17, S178–S188 (2006)

    CAS  Google Scholar 

  29. K.C. Sung, E.J. Rhee, H. Kim, J.B. Park, Y.K. Kim, S. Woo, A.M. Wilson, An elevated apolipoprotein B/AI ratio is independently associated with microalbuminuria in male subjects with impaired fasting glucose. NutrMetab Cardiovasc Dis 21, 610–616 (2011)

    CAS  Google Scholar 

  30. J. Kaur, A comprehensive review on metabolic syndrome. Cardiol Res Pract (2014). doi:10.1155/2014/943162

    Google Scholar 

  31. J.B. Meigs, R.B. D’Agostino Sr, D.M. Nathan, N. Rifai, P.W. Wilson, Longitudinal association of glycemia and microalbuminuria: the Framingham Offspring Study. Diabetes Care 25, 977–983 (2002)

    Article  PubMed  Google Scholar 

  32. L. Mykkanen, D.J. Zaccaro, L.E. Wagenknecht, D.C. Robbins, M. Gabriel, S.M. Haffner, Microalbuminuria is associated with insulin resistance in nondiabetic subjects: the insulin resistance atherosclerosis study. Diabetes 47, 793–800 (1998)

    Article  CAS  PubMed  Google Scholar 

  33. A.H. Brantsma, S.J. Bakker, H.L. Hillege, D. de Zeeuw, P.E. de Jong, R.T. Gansevoort, Urinary albumin excretion and its relation with C-reactive protein and the metabolic syndrome in the prediction of type 2 diabetes. Diabetes Care 28(2525–2530), 14 (2005)

    Google Scholar 

  34. J.M. Weinberg, Lipotoxicity. Kidney Int. 70, 1560–1566 (2006)

    Article  CAS  PubMed  Google Scholar 

  35. C.J. Packard, J. Shepherd, Lipoprotein heterogeneity and apolipoprotein B metabolism. ArteriosclerThromb VascBiol 17, 3542–3556 (1997)

    Article  CAS  Google Scholar 

  36. D.M. Kim, C.W. Ahn, J.S. Park, B.S. Cha, S.K. Lim, K.R. Kim, H.C. Lee, K.B. Huh, An implication of hypertriglyceridemia in the progression of diabetic nephropathy in metabolically obese, normal weight patients with type 2 diabetes mellitus in Korea. Diabetes Res ClinPract 66, S169–S172 (2004)

    Article  CAS  Google Scholar 

  37. G. Zoppini, G. Targher, M. Chonchol, F. Perrone, G. Lippi, M. Muggeo, Higher HDL cholesterol levels are associated with a lower incidence of chronic kidney disease in patients with type 2 diabetes. NutrMetab Cardiovasc Dis 19, 580–586 (2009)

    Article  CAS  Google Scholar 

  38. P.V. Subbaiah, R.A. Rodby, Abnormal acyltransferase activities and accelerated cholesteryl ester transfer in patients with nephrotic syndrome. Metabolism 43, 1126–1133 (1994)

    Article  CAS  PubMed  Google Scholar 

  39. M.M. Lai, C.I. Li, S.L. Kardia, C.S. Liu, W.Y. Lin, Y.D. Lee, P.C. Chang, C.C. Lin, T.C. Li et al., Sex difference in the association of metabolic syndrome with high sensitivity C-reactive protein in a Taiwanese population. BMC Public Health (2010). doi:10.1186/1471-2458-10-429

    Google Scholar 

  40. G.P. Shantha, A.A. Kumar, M.K. Bharadhi, P. Arthur, Role of gender in the associations of microalbuminuria with inflammatory markers in hypertensive subjects: a cross-sectional study. Kidney Blood Press Res 32, 434–439 (2009)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We greatly appreciate the participants in the Korea National Health and Nutrition Examination Survey 2011-2012.

Conflict of interest

The authors declare that they have no conflict of interest or funding source.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Kyun Roh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nam, G.E., Han, K., Kim, D.H. et al. Relationship between dyslipidemia and albuminuria in prediabetic adults: The Korea National Health and Nutrition Examination Survey 2011–2012. Endocrine 48, 557–565 (2015). https://doi.org/10.1007/s12020-014-0411-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-014-0411-y

Keywords

Navigation