Lipidaemia and Diabetic Renal Disease

  • Per-Henrik Groop

Abstract

Coronary heart disease (CHD) is not only a major cause of death in the general population but also in IDDM and NIDDM [1]. Whereas in IDDM the increased early cardiovascular morbidity and mortality is largely confined to those with persistent proteinuria [2,3], such complications are frequently seen without signs of renal involvement in NIDDM. The prevalence of CHD and risk of premature death though increases with increasing albuminuria also in NIDDM [4–8]. The same major risk factors (lipid abnormalities) seem to be operative in the diabetic population as in the non-diabetic population [9,10]. However, there are differences in the lipid patterns between IDDM and NIDDM patients, and renal disease further modulates the lipid pattern. A thorough characterization of the lipid metabolism of these high risk patients is necessary to propose treatment strategies to prevent cardiovascular complications. This chapter will briefly review the present knowledge of the lipid and lipoprotein abnormalities observed in IDDM and NIDDM.

Keywords

Albumin Excretion Rate NIDDM Patient IDDM Patient Intermediate Density Lipoprotein Diabetic Renal Disease 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Pyörälä K, Laakso M, Uusitupa M. Diabetes and atherosclerosis: an epidemiologic view. Diab Metab Rev 1987; 3: 462–524.Google Scholar
  2. 2.
    Borch-Johnsen K, Andersen PK, Deckert T: The effect of proteinuria on relative mortality in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 1985; 28: 590–596.PubMedCrossRefGoogle Scholar
  3. 3.
    Borch-Johnsen K, Kreiner S: Proteinuria: value as predictor of cardiovascular mortality in insulin-dependent diabetes mellitus. BMJ 1987; 294: 1651–1654.PubMedCrossRefGoogle Scholar
  4. 4.
    Nelson RG, Pettitt DJ, Carraher M-J, Baird HR, Knowler WC. Effect of proteinuria on mortality in NIDDM. Diabetes 1988; 37: 1499–1504.PubMedCrossRefGoogle Scholar
  5. 5.
    Mogensen CE. Microalbuminuria predicts clinical proteinuria and early mortality in maturity-onset diabetes. N Engl J Med 1984; 310: 356–360.PubMedCrossRefGoogle Scholar
  6. 6.
    Schmitz A, Vaeth M. Microalbuminuria: A major risk factor in non-insulin dependenrt diabetes. A 10-year follow-up study of 503 diabetic patients. Diabetic Med 5: 126–134, 1988.Google Scholar
  7. 7.
    Mattock MB, Morrish NJ, Viberti GC, Keen H, Fitzgerald A, Jackson G. Prospective study of microalbuminuria as predictor of mortality in NIDDM. Diabetes 1992; 41: 736–741.PubMedCrossRefGoogle Scholar
  8. 8.
    Nielsen FS, Voldsgaard AI, Gall M-A, Rossing P, Hommel E, Andersen P, Dyerberg J, Parving H-H. Apolipoprotein (a) and cardiovascular disease in Type 2 (non-insulin-dependent) diabetic patiernts with and without diabetic nephropathy. Diabetologia 1993; 36: 438–444.PubMedCrossRefGoogle Scholar
  9. 9.
    Laakso M, Pyörälä K, Sarlund H, Voutilainen E. Lipid and lipoprotein abnormalities associated with coronary heart disease in patients with insulin-dependent diabetes mellitus. Arteriosclerosis 1986; 6: 679–684.PubMedCrossRefGoogle Scholar
  10. 10.
    Laakso M, Lehto S, Penttilä I, Pyörälä K. Lipid and lipoproteins predicting coronary heart disease mortality and morbidity in patients with non-insulin-dependent diabetes mellitus. Circulation 1993; 88: 1421–1430.PubMedCrossRefGoogle Scholar
  11. 11.
    Howard BJ. Lipoproten metabolism in diabetes mellitus. J Lipid Res 1994; 28: 613–628.Google Scholar
  12. 12.
    Groop PH, Elliott T, Ekstrand A, Franssila-Lallunki A, Friedman R, Viberti GC, Taskinen M-R. Multiple lipoprotein abnormalities in Type-1 diabetic-patients with renal-disease. Diabetes 1996; 45: 974–979.PubMedCrossRefGoogle Scholar
  13. 13.
    Östlund RE Jr, Semenkovich CF, Schechtman KB. Quantitative relationship between plasma lipids and glycohemoglobin in Type 1 patients. Longitudinal study of 212 patients. Diabetes Care 1989; 12: 332–336.Google Scholar
  14. 14.
    Nikkilä EA, Hormila P. Serum lipids and lipoproteins in insulin-treated diabetes. Diabetes 1978; 27: 1078–1086.PubMedCrossRefGoogle Scholar
  15. 15.
    Mattock MB, Salter AM, Fuller JH, Omer T, Gohari REI, Redmond SD, Keen H. High density lipoprotein subfractions in insulin-dependent diabetic and normal subjects. Atherosclerosis 1982; 45: 67–79.PubMedCrossRefGoogle Scholar
  16. 16.
    Eckel RH, Albers JJ, Cheung MC, Wahl PW, Lindgren FT, Bierman EL. High density lipoprotein composition in insulin-dependent diabetes mellitus. Diabetes 1981; 30: 132–138.PubMedCrossRefGoogle Scholar
  17. 17.
    Kahri J, Groop PH, Viberti GC, Elliott T, Taskinen M-R. Regulation of apolipoprotein A-I-containing lipoproteins in IDDM. Diabetes 1993; 42: 1281–1288.PubMedCrossRefGoogle Scholar
  18. 18.
    Taskinen M-R. Hyperlipidaemia in diabetes. Clin Endocrinol Metab 1990; 4: 743–775.Google Scholar
  19. 19.
    Taskinen M-R. Quantitative and qualitative lipoprotein abnormalities in diabetes mellitus. Diabetes 1992; 41: Suppl. 2: 12–17.PubMedCrossRefGoogle Scholar
  20. 20.
    Howard BJ, Abbott WGH, Beltz WF, Harper IT, Fields RM, Grundy SM, Taskinen M-R. Integrated study of low density lipoprotein metabolism and very low density lipoprotein metabolism in non-insulin dependent diabetes. Metabolism 1987; 36: 870–877.PubMedCrossRefGoogle Scholar
  21. 21.
    Rönnemaa T, Laakso M, Kallio V, Pyörälä K, Marniemi J, Puukka P. Serum lipids, lipoproteins, and apolipoproteins and the excessive occurrence of coronary heart disease in non-insulin-dependent diabetic patients. Am J Epidemiol 1989; 130: 632–645.PubMedGoogle Scholar
  22. 22.
    Taskinen M-R, Packard CJ, Shepherd J: Effect of insulin therapy on metabolic fate of apolipoprotein B-containing lipoproteins in NIDDM. Diabetes 1990; 39:1017–1027.PubMedCrossRefGoogle Scholar
  23. 23.
    Fisher RM, Coppack SW, Gibbons GF, Frayn KN. Very low density lipoprotein sub-fraction metabolism in normal and obese subjects. Int J Obesity 1993; 17: 263–269.Google Scholar
  24. 24.
    Shepherd J, Packard CJ. Metabolic heterogeneity in very low-density lipoproteins. Am Heart J 1987; 113:503–508.PubMedCrossRefGoogle Scholar
  25. 25.
    Parhofer KG, Barrett PHR, Bier DM, Schonfield G. Determination of kinetic parameters of apolipoprotein B metabolism using aminoacids labeled with stable isotopes. Clin Chem 1991; 36: 1431–1435.Google Scholar
  26. 26.
    Caslake MJ, Packard CJ, Series JJ, Yip B, Dagen MM, Shepherd J. Plasma triglyceride and low density lipoprotein metabolism. Eur J Clin Invest 1992; 22: 96–104.PubMedCrossRefGoogle Scholar
  27. 27.
    Taskinen M-R. Hyperlipidaemia in diabetes. In Bailliere’s Clinical Endocrinology and Metabolism 1990; 4: 743–775.CrossRefGoogle Scholar
  28. 28.
    Taskinen M-R, Välimäki M, Nikkilä EA, Kuusi T, Ehnholm C, Ylikahri R. High density lipoprotein subfractions and postheparin plasma lipases in alcoholic men before and after ethanol withdrawal. Metabolism 1982; 31: 1168–1174.PubMedCrossRefGoogle Scholar
  29. 29.
    Laakso M, Voutilainen E, Sarlund H, Aro A, Pyörälä K, Penttilä I. Serum lipids and lipoproteins in middle aged non-insulin-dependent diabetics. Atherosclerosis 1985; 56: 271–281.PubMedCrossRefGoogle Scholar
  30. 30.
    Nikkilä EA, Huttunen JK, Ehnholm C. Postheparin plasma lipoprotein lipase and hepatic lipase in diabetes mellitus. Diabetes 1977; 26: 11–21.PubMedCrossRefGoogle Scholar
  31. 31.
    Taskinen M-R, Nikkilä EA, Kuusi T, Harno K. Lipoprotein lipase activity and serum lipoproteins in untreated Type 2 (insulin-independent) diabetes associated with obesity. Diabetologia 1982; 22: 46–50.PubMedCrossRefGoogle Scholar
  32. 32.
    Laakso M, Pyörälä K, Voutilainen E, Marniemi J. Plasma insulin and serum lipids and lipoproteins in middle-aged non-insulin dependent diabetic and non-diabetic subjects. Am J Epidemiol 1987; 125: 611–621.PubMedGoogle Scholar
  33. 33.
    Taskinen M-R, Nestel PJ. »Hypolipidemic agents: their roles in diabetes mellitus.« In International Textbook of Diabetes Mellitus. Alberti KGMM, DeFronzo RA, Keen H, Zimmet, eds. John Wiley & Sons, 1992; pp 817-830.Google Scholar
  34. 34.
    Vannini P, Ciavarella A, Flammini M, Bargossi AM, Forlani G, Borgnino LC, Orsoni G: Lipid abnormalities in insulin-dependent diabetic patients with albuminuria. Diabetes Care 1984; 7: 151–154.PubMedCrossRefGoogle Scholar
  35. 35.
    Jensen T, Stender S, Deckert T. Abnormalities in plasma concentrations of lipoproteins and fibrinogen in Type 1 (insulin-dependent) diabetic patients with increased urinary albumin excretion. Diabetologia 1988; 31: 142–145.PubMedCrossRefGoogle Scholar
  36. 36.
    Holm J, Hemmingsen L, Nielsen NV. Serum concentrations of lipids and lipoproteins related to degree of albuminuria and low-molecular weight (tubular) proteinuria in insulin-dependent diabetics. Med Sci Res 1989; 17: 945–947.Google Scholar
  37. 37.
    Haaber AB, Kofoed-Enevoldsen A, Jensen T. The prevalence of hypercholesterolaemia and its relationship with albuminuria in insulin-dependent diabetic patients: an epidemiological study. Diabetic Med 1992; 9: 557–561.PubMedCrossRefGoogle Scholar
  38. 38.
    Dullaart RPF, Groener JEM, Dikkeschei LD, Erkelens DW, Doorenbos H: Increased cholesterylester transfer activity in complicated Type 1 (insulin-dependent) diabetes mellitus — its relationship with serum lipids. Diabetologia 1989; 32: 14–19.PubMedGoogle Scholar
  39. 39.
    Jones SL. coagulation factor concentrations in insulin-dependent diabetics with microalbuminuria. BMJ 1989; 289: 487–489.CrossRefGoogle Scholar
  40. 40.
    Watts GF, Naumova R, Slavin BM, Morris RW, Houlston R, Kubal C, Shaw KM: Serum lipids and lipoproteins in insulin-dependent diabetic patients with persistent microalbuminuria. Diabetic Med 1989; 6: 25–30.PubMedCrossRefGoogle Scholar
  41. 41.
    Tatami R, Mabuchi H, Ueda K, Ueda R, Haba T, Kametani T, Ito S, Koizumi J, Ohta M, Miyamoto S, Nakayama A, Kanaya H, Oiwake H, Genda A, Takeda R: Intermediate-density lipoprotein and cholesterol-rich very low density lipoprotein in angiographically determined coronary artery disease. Circulation 1981; 64: 1174–1184.PubMedCrossRefGoogle Scholar
  42. 42.
    Krauss RM: Relationship of intermediate and low-density lipoprotein subspecies to risk of coronary artery disease. Am Heart J 1987; 113: 578–582.PubMedCrossRefGoogle Scholar
  43. 43.
    Krauss RM, Lindgren FT, Williams PT, Kelsey SF, Brensike J, Vranizan K, Detre KM, Levy RI: Intermediate-density lipoproteins and progression of coronary artery disease in hypercholesterolaemic men. Lancet 1987; ii: 62–65.CrossRefGoogle Scholar
  44. 44.
    Steiner G, Schwartz L, Shumak S, Poapst M: The association of increased levels of intermediate-density lipoproteins with smoking and with coronary artery disease. Atherosclerosis 1987; 75: 124–130.Google Scholar
  45. 45.
    Winocour PH, Durrington PN, Bhatnagar D, Ishola M, Mackness M, Arrol S: Influence of early nephropathy on very low density lipoprotein (VLDL), intermediate density lipoprotein (IDL), and low density lipoprotein (LDL) composition. Atherosclerosis 1991; 89: 49–57.PubMedCrossRefGoogle Scholar
  46. 46.
    Nielsen FS, Voldsgaard AI, Gall M-A, Rossing P, Hommel E, Andersen P, Dyerberg J, Parving H-H. Apolipoprotein (a) and cardiovascular disease in Type 2 (non-insulin-dependent) diabetic patients with and without diabetic nephropathy. Diabetologia 1993; 36: 438–444.PubMedCrossRefGoogle Scholar
  47. 47.
    Mattock MB, Morrish NJ, Viberti GC, Keen H, Fitzgerald A, Jackson G. Prospective study of microalbuminuria as predictor of mortality in NIDDM. Diabetes 1992; 41: 736–741.PubMedCrossRefGoogle Scholar
  48. 48.
    Bruno G, Cavallo-Perin P, Bargero G, Borra M, Calvi V, D’Errico N, Deambrogio P, Pagano G. Prevalence and risk factors for micro-and macroalbuminuria in an Italian population-based cohort of NIDDM subjects. Diabetes Care 1996; 19: 43–47.PubMedCrossRefGoogle Scholar
  49. 49.
    Austin MA, Breslow JL, Hennekens CH, Buring JE, Willet WC, Krauss RM. Low-density lipoprotein subclass patterns and risk of myocardial infarction. JAMA 1988; 260: 1917–1921.PubMedCrossRefGoogle Scholar
  50. 50.
    Austin MA, Krauss RM. Genetic control of low-density lipoprotein subclasses. Lancet 1986; ii: 592–595.CrossRefGoogle Scholar
  51. 51.
    Austin MA, King MC, Vranizan KM, Krauss RM. Atherogenic lipoprotein phenotype. A proposed genetic marker for coronary heart disease. Circulation 1990; 82: 495–506.Google Scholar
  52. 52.
    Deckelbaum RJ, Granot E, Oschry Y, Rose L, Eisenberg S. Plasma triglyceride determines structure-composition in low and high density lipoproteins. Arteriosclerosis 1984; 4: 225–231.PubMedCrossRefGoogle Scholar
  53. 53.
    Lahdenperä S, Groop PH, Tilly-Kiesi M, Kuusi T, Elliott TG, Viberti GC, Taskinen M-R: LDL subclasses in IDDM patients: relation to diabetic nephropathy. Diabetologia 1994; 37: 681–88.PubMedCrossRefGoogle Scholar
  54. 54.
    Bagdade JD, Buchanan WE, Kuusi T, Taskinen M-R. Persistent abnormalities in lipoprotein composition in non-insulion-dependent diabetes after intensive insulin therapy. Arteriosclerosis 1990; 10: 232–239.PubMedCrossRefGoogle Scholar
  55. 55.
    James RW, Pometta D. The distribution profiles of very low density and low density lipoproteins in poorly-controlled male, type 2 (non-insulin-dependent) diabetic patients. Diabetologia 1991; 34: 246–252.PubMedCrossRefGoogle Scholar
  56. 56.
    Uusitupa MIJ, Niskanen LK, Siitonen O, Voutilainen E, Pyörälä K. Ten-year cardiovascular mortality in relation to risk factors and abnormalities in lipoprotein composition in type 2 (non-insulin-dependent) diabetic and nondiabetic subjects. Diabetologia 1993; 36: 1175–1184.PubMedCrossRefGoogle Scholar
  57. 57.
    Haffner SM, Mykkänen L, Stern MP, Paidi M, Howard BV. Greater effect of diabetes on LDL size in women than in men. Diabetes Care 1994; 17: 1164–1171.PubMedCrossRefGoogle Scholar
  58. 58.
    Lahdenperä S, Syvänne M, Kahri J, Taskinen M-R. Regulation of low-density lipoprotein particle size distribution in NIDDM and coronary disease: importance of serum triglycerides. Diabetologia 1996; 39: 453–461.PubMedCrossRefGoogle Scholar
  59. 59.
    Jay RH, Jones SL, Hill CE, Richmond W, Viberti GC, Rampling MW, Betteridge DJ. Blood rheology and cardiovascular risk factors in type 1 diabetes: relationship with microalbuminuria. Diabetic Med 1991; 8: 662–667.PubMedCrossRefGoogle Scholar
  60. 60.
    Winocour PH, Durrington PN, Ishola M, Anderson DC, Cohen H: Influence of proteinuria on vascular disease, blood pressure, and lipoproteins in insulin-dependent diabetes mellitus. BMJ 1987; 294: 1648–1651.PubMedCrossRefGoogle Scholar
  61. 61.
    Kahri J, Groop PH, Elliott T, Viberti GC, Taskinen M-R: Plasma cholesteryl ester transfer protein and its relationship to plasma lipoproteins and apolipoprotein A-I-containing lipoproteins in IDDM patients with microalbuminuria and clinical nephropathy. Diabetes Care 1994; 17: 412–419.PubMedCrossRefGoogle Scholar
  62. 62.
    Demant T, Carlson LA, Holmquist L, Karpe F, Nilsson-Ehle P, Packard CJ, Shepherd J. Lipoprotein metabolism in hepatic lipase deficiency: studies on the turnover of apolipoprotein B and on the effect of hepatic lipase on high density lipoprotein. J Lipid Res 1988; 29: 1603–1611.PubMedGoogle Scholar
  63. 63.
    Auwerx JH, Marzetta CA, Hokanson JE, Brunzell JD. Large buoyant LDL-like particles in hepatic lipase deficiency. Arteriosclerosis 1989; 9: 319–325.PubMedCrossRefGoogle Scholar
  64. 64.
    Zambon A., Austin MA, Brown BG, Hokanson JE, Brunzell JD. Effect of hepatic lipase on LDL in normal men and those with coronary artery disease. Arterioscler Thromb 1993; 13: 147–153.PubMedCrossRefGoogle Scholar
  65. 65.
    Watson TDG, Caslake MJ, Freeman DJ, Griffin BA, Hinnie J, Packard CJ, Shepherd J. Determinants of LDL subfraction distribution and concentrations in young normolipidemic subjects. Arterioscler Thromb 1994; 14: 902–910.PubMedCrossRefGoogle Scholar
  66. 66.
    Rhoads GG, Dahlén GH, Berg K, Morton NE, Dannenberg AL. Lp(a) lipoprotein as a risk factor for myocardial infarction. JAMA 1986; 256: 2540–2544.PubMedCrossRefGoogle Scholar
  67. 67.
    Dahlén GH, Guyton JR, Attar M, Farmer JA, Kautz JA, Gotto AM Jr. Association of levels of lipoprotein Lp(a), plasma lipids, and other lipoproteins with coronary artery disease documented by angiography. Circulation 1986; 74: 758–765.PubMedCrossRefGoogle Scholar
  68. 68.
    Durrington PN, Ishola M, Hunt L, Arrol S, Bhatnagar D. Apolipoproteins (a), A-I and B and parental history in men with early onset ischaemic heart disease. Lancet 1988; i: 1070–1073.CrossRefGoogle Scholar
  69. 69.
    Jenkins AJ, Steele JS, Janus ED, Best JD. Increased plasma apolipoprotein (a) levels in IDDM patients with microalbuminuria. Diabetes 1991; 40: 787–790.PubMedCrossRefGoogle Scholar
  70. 70.
    Kapelrud H, Bangstad H-J, Dahl-Jørgensen K, Berg K, Hanssen KF. Serum Lp(a) lipoprotein concentrations in insulin dependent diabetic patients with microalbuminuria. BMJ 1991; 303: 675–678.PubMedCrossRefGoogle Scholar
  71. 71.
    Winocour PH, Bhatnagar D, Ishola M, Arrol S, Durrington PN. Lipoprotein (a) and microvascular disease in Type 1 (insulin-dependent) diabetes. Diabetic Med 1991; 8: 922–927.PubMedCrossRefGoogle Scholar
  72. 72.
    Gall M-A, Rossing P, Hommel E, Voldsgaard AI, Andersen P, Nielsen FS, Dyerberg J, Parving H-H. Apolipoprotein (a) in insulin-dependent diabetic patients with and without diabetic nephropathy. Scand J Clin Lab Invest 1992; 52: 513–521.PubMedCrossRefGoogle Scholar
  73. 73.
    Groop PH, Viberti GC, Elliott T, Friedman R, Mackie A, Ehnholm C, Jauhiainen M, Taskinen M-R. Lipoprotein (a) in insulin dependent diabetic patients with renal disease. Diabetic Med 1994; 11: 961–967.PubMedCrossRefGoogle Scholar
  74. 74.
    Maser RE, Drash AL, Usher D, Kuller LH, Becker DJ, Orchard TJ. Lipoprotein (a) concentration shows little relationship to IDDM complications in the Pittsburgh Epidemiology of Diabetes Complications Study Cohort. Diabetes Care 1993; 16: 755–758.PubMedCrossRefGoogle Scholar
  75. 75.
    Ruotolo G, Zoppo A, Parlavecchia M, Giberti B, Micossi P. Apolipoprotein (a) levels in type 1 and type 2 diabetes mellitus. Acta Diabetol 1991; 28: 158–161.PubMedCrossRefGoogle Scholar
  76. 76.
    Schernthaner G, Kostner GM, Dieplinger H, Prager R, Mühlhauser I. Apolipoproteins (A-I, A-II, B), Lp(a), lipoprotein and lecithin: cholesterol acetyltransferase actvity in diabetes mellitus. Arteriosclerosis 1983; 49: 277–293.CrossRefGoogle Scholar
  77. 77.
    Guillausseau P-J, Peynet J, Chanson P, Legrand A, Altaian J-J, Poupon J, N’Guyen M, Rousselet F, Lubetski J. Lipoprotein (a) in diabetic patients with and without chronic renal failure. Diabetes Care 1992; 15: 976–979.PubMedCrossRefGoogle Scholar
  78. 78.
    Haffner SM, Morales PA, Stern MP, Gruber MK. Lp(a) concentrations in NIDDM. Diabetes 1992; 41: 1267–1272.PubMedCrossRefGoogle Scholar
  79. 79.
    Jenkins AJ, Steele JS, Janus ED, Santamaria JD, Best JD. Plasma apolipoprotein (a) is increased in type 2 (non-insulin-dependent) diabetic patients with microalbuminuria. Diabetologia 1992; 35: 1055–1059.PubMedCrossRefGoogle Scholar
  80. 80.
    Gjone E. »Familial lecithin: cholesterol acyltransferase deficiency — a new metabolic disease with renal involvement.« In Advances in Nephrology, Hamburger, Crosnier, Grunfeld, Maxwell, eds. Chicago: Year Book Medical Publishers, 1981; pp 167–185.Google Scholar
  81. 81.
    Keane WF, Kasiske BL, O’Donnell MP. Lipids and progressive glomerulosclerosis. Am J Nephrol 1988; 8: 261–271.PubMedCrossRefGoogle Scholar
  82. 82.
    Mulec H, Johnson S-A, Björck S. Relation between serum cholesterol and diabetic nephropathy. Lancet 1990; 335: 1537–1538.PubMedCrossRefGoogle Scholar
  83. 83.
    Gröne H-J, Walli A, Gröne E, Niedmann P, Thiery J, Seidel D, Helmchen U. Induction of glomerulosclerosis by dietary lipids. A functional and morphologic study in the rat. Lab Invest 1989; 60: 433–446.PubMedGoogle Scholar
  84. 84.
    Kasiske BL, O’Donnell MP, Lee H, Kim Y, Keane WF. Impact of dietary fatty acid supplementation on renal injury in obese Zucker rats. Kidney Int 1991; 39: 1125–1134.PubMedCrossRefGoogle Scholar
  85. 85.
    Kasiske BL, Cleary MP, O’Donnell MP, Keane WF. Effects of genetic obesity on renal structure and function in the Zucker rat. J Lab Clin Med 1985; 106: 598–604.PubMedGoogle Scholar
  86. 86.
    Kasiske BL, O’Donnell MP, Cleary MP, Keane WF. Treatment of hyperlipidemia reduces glomerular injury in obese Zucker rats. Kidney Int 1988; 33: 667–672.PubMedCrossRefGoogle Scholar
  87. 87.
    Hommel E, Andersen P, Gall M-A, Nielsen F, Jensen B, Rossing P, Dyerberg J, Parving H-H. Plasma lipoproteins and renal function during simvastatin treatment in diabetic nephropathy. Diabetologia 1992; 35: 447–451.PubMedCrossRefGoogle Scholar
  88. 88.
    Sasaki T, Kuratya H, Nomura K, Utsunomiya K, Ikeda Y. Amelioration of proteinuria with pravastatin in hypercholesterolemic patients with diabetes mellitus. Jpn J Med 1990; 29: 156–163.PubMedCrossRefGoogle Scholar
  89. 89.
    Parving H-H. Cholesterol-lowering therapy may retard the progression of diabetic nephropathy. Letter to the editors. Diabetologia 1996; 39: 367–373.Google Scholar
  90. 90.
    Lam KSL. Response from the authors. Diabetologia 1996; 39: 368.CrossRefGoogle Scholar
  91. 91.
    Bender R. The effect of cholesterol-lowering therapy on the progression of diabetic nephropathy is unproved. Letter to the editors. Diabetologia 1996; 39: 698–369.Google Scholar
  92. 92.
    Lam KSL, Lauder IJ. Response from the authors. Diabetologia 1996; 39: 369–370.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Per-Henrik Groop
    • 1
  1. 1.Department of MedicineHelsinki University Central HospitalHelsinkiFinland

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