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Diabetologia

, Volume 15, Issue 3, pp 143–152 | Cite as

Relation of diabetic control to development of microvascular complications

  • G. Tchobroutsky
Review Articles

Summary

This review seeks to supply the arguments which support or deny the relationship between the quality of control of blood glucose levels and the course of diabetic microangiopathy. The ideal study is impossible to do in man but most prospective studies suggest that the better the control the slower the rate of progression and severity of lesions. “Scientific” but indirect arguments from biochemical, enzymatic and functional studies have shown that insulin and/or blood glucose control reverse some early diabetic changes that are probably related to the late events. Recent studies suggest that observations on animals that have shown the beneficial effect of treatment are relevant to the problem of diabetic microvascular lesions in man. Heredity influences the development of diabetic microangiopathy in diabetics but retinal and/or glomerular lesions — which are definitely not pathognomonic for diabetes — do not appear in the absence of hyperglycaemia. Muscle capillary basement membrane thickening that seems not to be a specific abnormality was not observed by several investigators in recently diagnosed diabetics. Therefore most of the arguments that have been given to support the point of view that tight control is not justified may be rejected. The opinion of the author is that strict control of diabetes is worthwile in patients with long life expectancy and no psychological, social or cultural handicaps.

Key words

Diabetes control microangiopathy blood glucose vascular complications treatment of diabetes 

References

  1. 1.
    Keen, H., Jarrett, J. (Eds): Complications of Diabetes, 282 pp. London: Arnold 1975Google Scholar
  2. 2.
    McMillan, D.E., Ditzel, J. (Eds): Proceedings of a conference on diabetic microangiopathy. Diabetes 25 (Suppl. 2), 805–930 (1976)Google Scholar
  3. 3.
    Pathogenesis of diabetic microangiopathy (Leader). Br. Med. J. 1977 I, 1555–1556Google Scholar
  4. 4.
    Pyke, D.A., Tattersall, R.B.: Diabetic retinopathy in identical twins. Diabetes 22, 613–618 (1973)Google Scholar
  5. 5.
    Barbosa, J., Noreen, H., Emme, L., Goetz, F., Simmons, R., De Leiva, A., Najarian, J., Yunis, E.J.: Histocompatibility (H. L. A.) antigens and diabetic microangiopathy. Tissue Antigens 7, 233–237 (1976)Google Scholar
  6. 6.
    Becker, B., Shin, D.H., Burgess, D., Kilo, C., Piller, W.V.: His tocompatibility antigens and diabetic retinopathy. Diabetes 26, 997–999 (1977)Google Scholar
  7. 7.
    Egeberg, J., Frimodt-Moller, K., Sander, E., Svejgaard, A.: Basement membranes thickness, insulin antibodies and H. L. A. antigens in juvenile diabetics with and without proliferative retinopathy (abstract). Diabetologia 13, 391 (1977)Google Scholar
  8. 8.
    Möller, E., Persson, B., Sterky, G.: H. L. A. phenotypes and diabetic retinopathy. Diabetologia 14, 155–158 (1978)Google Scholar
  9. 9.
    Bondy, P.K., Felig, P.: Relation of diabetic control to development of vascular complications, Med. clin. North Am. 55, 889–897 (1971)Google Scholar
  10. 10.
    Siperstein, M.D., Foster, D.W., Knowles, H.C. Jr., Levine, R., Madison, L.L., Roth, J.: Control of blood glucose and diabetic vascular disease. N. Engl. J. Med. 296, 1060–1063 (1977)Google Scholar
  11. 11.
    Siperstein, M.D., Unger, R.H., Madison, L.L.: Studies of muscle capillary basement membranes in normal subjects, diabetic, and prediabetic patients. J. Clin. Invest. 47, 1973–1999 (1968)Google Scholar
  12. 12.
    Lefebvre, P., Millet, J., Luyckx, A.: Control of diabetes: an attempt to formulate policy guidelines in a department of medicine. Diabetologia 10, 201–204 (1974)Google Scholar
  13. 13.
    Tunbridge, Sir R.: Foreward. In: H. Keen, H. Jarrett (Eds): Complication of diabetes, pp. VII-IX. London: Arnold 1975Google Scholar
  14. 14.
    Knowles, H.C. Jr.: The problem of the relation of the control of diabetes to the development of vascular disease. Trans. Am. Clin. Climatol. Assoc. 76, 142–147 (1964)Google Scholar
  15. 15.
    Colwell, J.A.: Effect of diabetic control on retinopathy. Diabetes 15, 497–499 (1966)Google Scholar
  16. 16.
    Caird, F.I., Pirie, A., Ramsell, T.G.: Diabetes and the eye, 230 pp. Oxford: Blackwell Scientific Publ. 1969Google Scholar
  17. 17.
    Pometta, D.: La microangiopathie diabétique. Acta Endocrinol. [suppl. 156] (Kbh.) 67, 1–144 (1971)Google Scholar
  18. 18.
    Kaplan, M.H., Feinstein, A.R.: A critique of methods in reported studies of long-term vascular complications in patients with diabetes mellitus. Diabetes 22, 160–174 (1973)Google Scholar
  19. 19.
    Stowers, J.M.: Complications in relation to diabetic control. General review. In: H. Keen, J. Jarrett (Eds): Complications of diabetes, pp. 1–5. London: Arnold 1975Google Scholar
  20. 20.
    Kohner, E.M., Dollery, C.T.: Diabetic retinopathy. In: H. Keen, J. Jarrett (Eds): Complications of diabetes, pp. 7–98. London: Arnold 1975Google Scholar
  21. 21.
    Lauvaux, J.P.: Le rôle de l'hyperglycémie chronique dans l'apparition et la développement de la triopathie diabétique: neuropathie, néphropathie, rétinopathie. (Etude clinique). Thèse Université Libre de Bruxelles 1976Google Scholar
  22. 22.
    Pirart, J.: Diabetes mellitus and its degenerative complications: a prospective study of 4.400 patients observed between 1947 and 1973 (In three parts). Diabete Metab. 3, 97–107, 173–182, 245–256 (1977)Google Scholar
  23. 23.
    Raskin, Ph.: Diabetic regulation and its relationship to microangiopathy. Metabolism 27, 235–252 (1978)Google Scholar
  24. 24.
    Jackson, R.L., Hardin, R.C., Walker, G.L., Hendricks, A.B., Kelly, H.G.: Degenerative changes in young diabetic patients in relationship to levels of control. Pediatrics 5, 959 (1950)Google Scholar
  25. 25.
    Johnsson, S.: Retinopathy and nephropathy in diabetes mellitus: comparison of the effects of two forms of treatment. Diabetes 9, 1–8 (1960)Google Scholar
  26. 26.
    Constam, G.R.: Contrôle du diabète et prévention des complications. In: Journées Diabétol. Hôtel-Dieu, pp. 313–320. Paris: Flammarion 1972Google Scholar
  27. 27.
    Francois, R., Memelle, H., Leonetti, P., Jarlot, B., Gillet, P., David, L., Tardieu, M.: Complications dégénératives après 10 ans de diabète infantile. In: Journées Diabétol. Hôtel-Dieu, pp. 135–156. Paris: Flammarion 1976Google Scholar
  28. 28.
    Colwell, A.R.: Observed course of diabetes mellitus and inferences concerning its origin and progress. Arch. Intern. Med. 70, 523–531 (1942)Google Scholar
  29. 29.
    Mirsky, I.A.: Our challenge for the future (Editorial). Diabetes Abstracts (Cincinnati) 5, 71 (1946)Google Scholar
  30. 30.
    Dolger, H.: Clinical evaluation of vascular damage in diabetes mellitus. J. Amr. Md. As. 134, 1289–1291 (1947)Google Scholar
  31. 31.
    Muri, J.: Diabetic nephropathy and retinopathy. Acta Med. Scand. 149, 211–219 (1954)Google Scholar
  32. 32.
    Pirart, J.: Rigueur du traitement du diabète et complications rétiniennes. In: Journées Diabétol. Hôtel-Dieu, pp. 282–296. Paris: Flammarion 1977Google Scholar
  33. 33.
    Knowles, H.C., Guest, G.M., Lampe, J., Kessler, M., Skillman, T.G.: The course of juvenile diabetes treated with unmeasured diet. Diabetes 14, 239–273 (1965)Google Scholar
  34. 34.
    Gerritzen, F.M.: The course of diabetic retinopathy. Diabetes 22, 122–128 (1973)Google Scholar
  35. 35.
    U. G. D. P.: A study of the effects of hypoglycemic agents on vascular complications in patients with adult-onset diabetes. VI — Supplementary report on non fatal events in patients treated with tolbutamide. Diabetes 25, 1129–1151 (1976)Google Scholar
  36. 36.
    Malone, J.I., Van Cader, T.C., Edwards, W.C.: Diabetic vascular changes in children. Diabetes 26, 673–679 (1977)Google Scholar
  37. 37.
    Folk, M.L., Soskin, S.: The fundus oculi in diabetes mellitus. Am. J. Ophthalmol. 18, 432–437 (1935)Google Scholar
  38. 38.
    Boyd, J.D., Jackson, R.L., Allen, J.H.: Avoidance of degenerative lesions in diabetes mellitus. J. A. M. A. 118, 694–696 (1942)Google Scholar
  39. 39.
    Schlesinger, F.G., Franken, S., Van Lange, L.T.P., Schwartz, F.: Incidence and progression of retinal and vascular lesions in long-term diabetes. Acta Med. Scand. 168, 483–488 (1960)Google Scholar
  40. 40.
    Dollery, C.T., Oakley, N.W.: Reversal of retinal vascular changes in diabetes. Diabetes 14, 121–127 (1965)Google Scholar
  41. 41.
    Davis, M.D.: Natural course of diabetic retinopathy. In: S.J. Kimura, W.M. Caygill (Eds): Vascular complications of diabetes mellitus, pp. 139–169. Saint-Louis: Mosby 1967Google Scholar
  42. 42.
    Burditt, A.F., Caird, F.I., Draper, G.J.: The natural history of diabetic retinopathy. Q. J. Med. 37, 303–317 (1968)Google Scholar
  43. 43.
    Kohner, E.M., Fraser, T.R., Joplin, G.F., Oakley, N.W.: The effect of control on diabetic retinopathy. In: M.F. Goldberg, S.L. Fine (Eds): The treatment of diabetic retinopathy, pp. 119. Washington: U.S. Public Health Service Publ. No 1890 1969Google Scholar
  44. 44.
    Miki, E., Fukuda, M., Kuzuya, T., Kosaka, K., Nakao, K.: Relation of the course of retinopathy to control of diabetes, age and therepeutic agents in diabetic Japanese patients. Diabetes 18, 773–780 (1969)Google Scholar
  45. 45.
    Miki, E., Kuzuya, T., Ide, T., Nakao, K.: Frequency, degree and progression with time of proteinuria in diabetic patients. Lancet 1972 I, 922–924Google Scholar
  46. 46.
    Freyler, H., Hichorlis, St., Arnfelser, H., Egerer, I.: Welche faktoren beeinflussen die progredienz der diabetischen retinopathie? Wien. Klin. Wochenschr. 86, 621–624 (1974)Google Scholar
  47. 47.
    Takazakura, E., Nakamoto, Y., Hayakawa, H., Kawai, K., Muramoto, S., Yoshida, K., Shimizu, M., Shinoda, A., Takeuchi, J.: Onset and progression of diabetic glomerulosclerosis. Diabetes 24, 1–9 (1975)Google Scholar
  48. 48.
    Job, D., Eschwege, E., Guyot-Argenton, C., Aubry, J.P., Tchobroutsky, G.: Effect of multiple daily insulin infections on the course of diabetic retinopathy. Diabetes 25, 463–469 (1976)Google Scholar
  49. 49.
    Tchobroutsky, G.: How to achieve better diabetic control? Studies with insulin three times a day. In: W.J. Malaisse, J. Pirart, J. Valance-Owen: Diabetes, pp. 667–679. Amsterdam: Excerpta Med. Int. Congr. Ser. 312 1973Google Scholar
  50. 50.
    Tchobroutsky, G., Kopf, A., Eschwege, E., Assan, R.: Serial postprandial plasma insulin levels in 117 subjects with and without diabetes. Diabetes 22, 825–833 (1973)Google Scholar
  51. 51.
    Tchobroutsky, G., Lenormand, M.E., Michel, G., Assan, R.: Lack of post-prandial exercise-induced growth hormone secretion in normoglycemic insulin-treated diabetic men. Horm. Metab. Res. 6, 184–187 (1974)Google Scholar
  52. 52.
    Eschwege, E., Job, D., Guyot-Argenton, C., Aubry, J.P., Tchobroutsky, G.: Delayed progression of diabetic retinopathy by divided insulin administration: a further followup. Diabetologia (in press) (1978)Google Scholar
  53. 53.
    Alberti, K.G.M.M., Hockaday, T.D.R.: The biochemistry of the complications of diabetes mellitus. In: H. Keen, J. Jarrett (Eds): Complications of diabetes, pp. 221–264. London: Arnold 1975Google Scholar
  54. 54.
    O'Sullivan, J.B., Cosgrove, J., McCaughan, D.: Blood sugars, vascular abnormalities and survival. The Oxford study after 17 years. Postgrad. Med. J. 44 (Suppl), 955–959 (1961)Google Scholar
  55. 55.
    Jarrett, R.J., Keen, H.: Hyperglycaemia and diabetes mellitus. Lancet 1976 II, 1009–1012Google Scholar
  56. 56.
    Katsilambros, N.: Diabetic retinopathy and blood-sugar. Lancet 1976 II, 1253Google Scholar
  57. 57.
    Kamenetzky, S.A., Bennett, P.H., Dippe, S.E., Miller, M., Lecompte, P.M.: A clinical and histologic study of diabetic nephropathy in the Pima Indians. Diabetes 23, 61–68 (1974)Google Scholar
  58. 58.
    Hautecouverture, M., Monchi, A., Tchobroutsky, G., Assan, R., Slama, G., Derot, M.: Rétinopathie diabétique et sécrétion d'hormone de croissance chez 39 diabétiques non insulino-dépendants. Nouv. Presse Med. 2, 1817–1822 (1973)Google Scholar
  59. 59.
    Engerman, R., Bloodworth, J.M.B., Jr. Nelson, S.: Relationship of microvascular disease in diabetes to metabolic control. Diabetes 26, 760–769 (1977)Google Scholar
  60. 60.
    Gibbs, G.E., Wilson, R.B., Gifford, H.: Glomerulosclerosis in the long-term alloxan diabetic monkey. Diabetes 15, 258–261 (1966)Google Scholar
  61. 61.
    Lazarow, A.: Glomerular basement membrane thickening in diabetes. In: J. Östman, R.D.G. Milner (Eds): Diabetes, pp. 301–306. Amsterdam: Excerpta Med. Int. Congr. Ser. 172 1969Google Scholar
  62. 62.
    Leuenberger, P.M., Cameron, D., Stauffacher, W., et al.: Ocular lesions in rats rendered chronically diabetic with streptozotocin. Ophthalmol. Res. 2, 189–204 (1971)Google Scholar
  63. 63.
    Bloodworth, J.M.B., Jr., Engerman, R.L., Camerini-Davalos, R.A., Powers, K.L.: Variations in capillary basement membrane width produced by aging and diabetes mellitus. In: R.A. Camerini-Davalos, H.S. Cole (Eds): Early diabetes, pp. 279–295. New-York, London: Academic Press 1973Google Scholar
  64. 64.
    Cameron, D.P., Amherdt, M., Leuenberger, P., Orci, L., Stauffacher, W.: Microvascular alterations in chronically streptozotocin-diabetic rats. In: R.A. Camerini-Davalos, H.S. Cole (Eds): Early diabetes. pp. 257–269. New York, London: Academic Press 1973Google Scholar
  65. 65.
    Duhault, J., Boulanger, M., Lebon, F., Beert, L.: La microangiopathie diabétique expérimentale. Nouv. Presse Med. 2, 3013–3017 (1973)Google Scholar
  66. 66.
    Hägg, E.: On the pathogenesis of glomerular lesions in the alloxan diabetic rat. Acta Med. Scand. (Suppl.) 558, 1–31 (1974)Google Scholar
  67. 67.
    Stout, C., Kennedy, A., Folse, D., Beathard, G., Granholm, N., Padula, R., Williams, G.R., Whorton, E., Davis, E., Kimmelstiel, P.: Glomerulosclerosis in “secondary” diabetes in baboons (abstract). Diabetes 25 (Suppl. 1), 349 (1976)Google Scholar
  68. 68.
    Fox, C.J., Darby, S.C., Ireland, J.T., Sönksen, P.H.: Blood glucose control and glomerular capillary basement membrane thickening in experimental diabetes. Br. Med. J. 1977 II, 605–607Google Scholar
  69. 69.
    Rasch, R.: The effect of diabetic control on kidney weight, glomerular volume and glomerular basement membrane thickness (abstract). Diabetologia 13, 426 (1977)Google Scholar
  70. 70.
    Slater, D.N., Mangnall, Y., Smythe, A., Ward, A.M., Fox, M.: Neonatal islet cell transplantation in the diabetic rat: effect on the renal complications. Br. J. Pathol. 124, 117–124 (1978)Google Scholar
  71. 71.
    Mauer, S.M., Steffes, M.W., Brown, D.M.: Animal models of diabetic nephropathy. In: M. Maxwell (Ed): Advances in nephrology. Chicago: Year Book Med. 1978 (in press)Google Scholar
  72. 72.
    Bendayan, M., Sandborne, E., Rasio, E.: Concurrent studies on the morphology, the permeability and the metabolism of a blood capillary preparation (abstract). Diabetologia 10, 358 (1974)Google Scholar
  73. 73.
    McMillan, D.E., Mauer, S.M.: Diabetes and vascular disease. N. Engl. J. Med. 297, 392–393 (1977)Google Scholar
  74. 74.
    Federlin, K., Bretzel, R.G., Schmidtchen, U.: Islet transplantation in experimental diabetes of rat. 5 — Regression of glomerular lesions in diabetic rats after intraportal transplantation of isogeneic islets. Preliminary results. Horm. Metab. Res. 8, 404–406 (1976)Google Scholar
  75. 75.
    Bloodworth, J.M.B., Jr. Engerman, R.L.: Diabetic microangiopathy in the experimentally-diabetic dog and its prevention by careful control with insulin (abstract). Diabetes 22 (suppl. 1), 290 (1973)Google Scholar
  76. 76.
    Gray, B.N., Watkins, E.: Prevention of vascular complications of diabetes by pancreatic islet transplantation. Arch. Surg. 111, 254–257 (1976)Google Scholar
  77. 77.
    Lee, C.S., Mauer, S.M., Brown, D.M., Sutherland, D.E.R., Michael, A.F., Najarian, J.S.: Renal transplantation in diabetes mellitus in rats. J. Exp. Med. 139, 793–800 (1974)Google Scholar
  78. 78.
    Mauer, S.M., Sutherland, D.E.R., Steffes, M.W., Leonard, R.J., Najarian, J.S., Michael, A.F., Brown, D.M.: Pancreatic islet transplantation. Effects on the glomerular lesions of experimental diabetes in the rat. Diabetes 23, 748–753 (1974)Google Scholar
  79. 79.
    Orloff, M.J., Lee, S., Charters, A.C., III. Grambort, D.E., Storck, L.G., Knox, D.: Long term studies of pancreas transplantation in experimental diabetes mellitus. Ann. Surg. 182, 198–206 (1975)Google Scholar
  80. 80.
    Weil, R., Nozawa, M., Koss, M., Weber, C., Reemtsma, K.B., McIntosh, R.: Pancreatic transplantation in diabetic rats: renal function, morphology, ultrastructure and immunohistology. Surgery 78, 142–148 (1975)Google Scholar
  81. 81.
    Beisswenger, P.J., Spiro, R.G.: Studies on the human glomerular basement membrane. Composition, nature of the carbohydrate units and chemical changes in diabetes mellitus. Diabetes 22, 180–193 (1973)Google Scholar
  82. 82.
    Klein, L., Butcher, D.L., Sidilovsky, O., Kikkawa, R., Miller, M.: Quantification of collagen in renal glomeruli isolated from human non diabetic and diabetic kidneys. Diabetes 24, 1057–1065 (1975)Google Scholar
  83. 83.
    Reddi, A.S.: Diabetic microangiopathy. I — Current status of the chemistry and metabolism of the glomerular basement membrane. Metabolism 27, 107–124 (1978)Google Scholar
  84. 84.
    Ristelli, J., Koivisto, V.A., Akerblom, H.K., Kivirikko, K.I.: Intracellular enzymes of collagen biosynthesis in rat kidney in stretozotocin diabetes. Diabetes 25, 1066–1070 (1976)Google Scholar
  85. 85.
    Cohen, M.P., Khalifa, A.: Renal glomerular collagen synthesis in streptozotocin diabetes. Reversal of increased basement membrane synthesis with insulin therapy. Biochim. Biophys. Acta (in press)Google Scholar
  86. 86.
    Brownlee, M.: α 2-macroglobulin and reduced basement-membrane degradation in diabetes. Lancet 1976 I, 779–780Google Scholar
  87. 87.
    Lazarow, A., Speidel, E.: The chemical composition of the glomerular basement membrane and its relationship to the production of diabetic complications. In: M.D. Siperstein, A.R. Colwell, Sr., K. Meyer (Eds): Small Blood Vessel Involvement in Diabetes Mellitus, p. 127. Washington: American Institute of Biological Sciences 1964Google Scholar
  88. 88.
    Westberg, N.G., Michael, A.F.: Human glomerular basement membrane: chemical composition in diabetes mellitus. Acta Med. Scand. 194, 39–47 (1973)Google Scholar
  89. 89.
    Kefalides, N.A.: Biochemical properties of human glomerular basement membrane in normal and diabetic kidneys. J. Clin. Invest. 53, 403–407 (1974)Google Scholar
  90. 90.
    Duhault, J., Lonchampt, M.: Glucosyl transferase activity and diabetic microangiopathy. Biomedicine 27, 127–131 (1977)Google Scholar
  91. 91.
    Cohen, M.P., Khalifa, A.: Effect of diabetes and insulin on rat renal glomerular protocollagen hydroxylase activities. Biochim. Biophys. Acta 496, 88–94 (1977)Google Scholar
  92. 92.
    Fushimi, H., Tarui, S.: Kidney and serum beta-N-acetyl-glucosaminidase activities in streptozotocin diabetic rats and their responses to insulin and glucagon. J. Biochem. (Tokyo) 76, 225–227 (1974)Google Scholar
  93. 93.
    Spiro, R.G., Spiro, M.J.: Effect of diabetes on the biosynthesis of the renal glomerular basement membrane. Diabetes 20, 641–648 (1971)Google Scholar
  94. 94.
    Archer, J., Kaye, R.: Cultured skin fibroblasts and juvenile diabetes: senescence and collagen synthesis (abstract). Diabetes 26 (Suppl. 1), 361 (1977)Google Scholar
  95. 95.
    Parving, H.H.: Increased microvascular permeability to plasma proteins in short-and long-term juvenile diabetics. Diabetes 25 (Suppl. 2), 884–889 (1976)Google Scholar
  96. 96.
    Mogensen, C.E.: Renal function changes in diabetes. Diabetes 25 (Suppl. 2), 872–879 (1976)Google Scholar
  97. 97.
    Waltman, S.R., Oestrich, C.A., Hanish, S., et al.: Blood retinal barrier in experimental diabetes. Presented at the spring meeting of the Ass. for Research in Vision and Ophthalmology, Sarasota (Florida), April 1977Google Scholar
  98. 98.
    Cunha-Vaz, J.G., Faria de Abreu, J.R., Campos, A.J.: Early breakdown of the blood-retinal barrier in diabetes. Br. J. Ophthalmol. 59, 649–656 (1975)Google Scholar
  99. 99.
    Dorchy, H., Toussaint, D., Devroede, M., Ernould, C.: Angiofluorescein studies in infantile diabetic retinopathy. Intern. Study Group Diabetes in Children and Adolescents 10–11 (1977)Google Scholar
  100. 100.
    Waltman, S.R., Oestrich, C., Krupin, T., Hanish, S., Ratzan, S., Santiago, J., Kilo, Ch.: Quantitative vitreous fluorophotometry. A sensitive technique for measuring early breakdown of the blood-retinal barrier in young diabetic patients. Diabetes 27, 85–87 (1978)Google Scholar
  101. 101.
    Palmberg, P.F.: Diabetic retinopathy. Diabetes 26, 703–709 (1977)Google Scholar
  102. 102.
    Spiro, R.G.: Search for a biochemical basis of diabetic microangiopathy. Diabetologia 12, 1–14 (1976)Google Scholar
  103. 103.
    Williamson, J.R., Kilo, C.: Basement-membrane thickening and diabetic microangiopathy. Diabetes 25 (Suppl. 2), 925–927 (1976)Google Scholar
  104. 104.
    Westberg, N.G.: Biochemical alterations of the human glomerular basement membrane in diabetes. Diabetes 25 (Suppl. 2), 920–924 (1976)Google Scholar
  105. 105.
    Gundersen, H.J.G., Mogensen, C.E., Seyer-Hansen, K., Østerby, R., Lundbaek, K.: Early and late changes in the diabetic kidney. In: M. Maxwell (Ed): Advances in nephrology. Chicago: Year Book Med. Publ. 1978 (in press)Google Scholar
  106. 106.
    Parving, H.H., Noer, I., Deckert, T., Evrin, P.E., Nielsen, S.L., Lyngsøe, J., Mogensen, C.E., Rørth, M., Svendsen, P.Aa., Trap-Jensen, J., Lassen, N.A.: The effect of metabolic regulation on microvascular permeability to small and large molecules in short-term juvenile diabetes. Diabetologia 12, 161–166 (1976)Google Scholar
  107. 107.
    McMillan, D.E.: Plasma protein changes, blood viscosity and diabetic microangiopathy. Diabetes 25 (Suppl. 2), 858–864 (1976)Google Scholar
  108. 108.
    Koenig, R.J., Peterson, C.M., Kilo, C., Cerami, A., Williamson, J.R.: Hemoglobin Alc as indicator of the degree of glucose intolerance in diabetes. Diabetes 25, 230–232 (1976)Google Scholar
  109. 109.
    Ditzel, J.: Oxygen transport impairment in diabetes. Diabetes 25 (Suppl. 2), 832–838 (1976)Google Scholar
  110. 110.
    Schmid-Schönbein, H., Volger, E.: Red-cell aggregation and red-cell deformability in diabetes. Diabetes 25 (Suppl. 2), 897–902 (1976)Google Scholar
  111. 111.
    Lanoe, R., Thibult, N., Eschwege, E., Soria, J., Soria, C., Tchobroutsky, G.: Glycosylated haemoglobin concentrations and clinitest results in insulin dependent diabetes. Lancet 1977 II, 1156–1157Google Scholar
  112. 112.
    Preston, F.E., Ward, J.D., Marcola, B.H., Porter, N.R., Timperley, W.R., O'Malley, B.C.: Elevated β-thromboglobulin levels and circulating platelet aggregates in diabetic microangiopathy. Lancet 1978 I, 238–239Google Scholar
  113. 113.
    Platelet, Beta-thromboglobulin and diabetes mellitus. Lancet 1978 I, 250–251Google Scholar
  114. 114.
    Barnes, A.J., Locke, P., Scudder, P.R., Dormandy, T.L., Dormandy, J.A., Slack, J.: Is hyperviscosity a treatable component of diabetic microcirculatory disease? Lancet 1977 II, 789–781Google Scholar
  115. 115.
    Beaufils, M., Morel-Maroger, L.: Pathogenesis of renal disease in monoclonal gammopathies: current concepts. Nephron 20, 125–131 (1978)Google Scholar
  116. 116.
    Lundbaek, K.: Growth hormone's role in diabetic microangiopathy. Diabetes 25 (Suppl. 2), 845–849 (1976)Google Scholar
  117. 117.
    Kilo, C., Vogler, N., Williamson, J.R.: Muscle capillary basement membrane changes related to aging and to diabetes mellitus. Diabetes 21, 881–905 (1972)Google Scholar
  118. 118.
    Yodaiken, R.E., Menefee, M., Seftel, H.C., Dip, M.B., Kew, M.C., McClaren, M.J.: Capillaries of South African diabetics. IV — Relation to retinopathy. Diabetes 24, 286–290 (1975)Google Scholar
  119. 119.
    Vracko, R., Strandness, D.E.: Basal lamina of abdominal skeletal muscle capillaries in diabetics and non diabetics. Circulation 41, 271–283 (1970)Google Scholar
  120. 120.
    Williamson, J.R., Kilo, C.: Current status of capillary basement-membrane disease in diabetes mellitus. Diabetes 26, 65–75 (1977)Google Scholar
  121. 121.
    Larkins, R.G., Martin, F.I.R., Tait, B.D.: HLA patterns and diabetic retinopathy. Br. Med. J. 1978 I, 1111Google Scholar
  122. 122.
    Karam, J.H., Rosenthal, M., O'Donnel, J.J., Tsalikian, E., Lorenzi, M., Gerich, J.E., Siperstein, M.D., Forsham, P.H.: Discordance of diabetic microangiopathy in identical twins. Diabetes 25, 24–28 (1976)Google Scholar
  123. 123.
    Ganda, O.P., Soeldner, J.S., Gleason, R.E., Smit, T.M., Kilo, C., Williamson, T.R.: Monozygotic triplets with discordance for diabetes mellitus and diabetic microangiopathy. Diabetes 26, 469–479 (1977)Google Scholar
  124. 124.
    Mauer, S.M. Steffes, M.W., Azar, S., Kupcho-Sandberg, S., Brown, D.M.: The effects of goldblatt hypertension on the development of glomerular lesions of diabetes mellitus in the rat. (in press). Cited by Mauer [71]Google Scholar
  125. 125.
    Steffes, M.W., Brown, D.M., Mauer, S.M.: Diabetic glomerulopathy following unilateral nephrectomy in rat. Diabetes 27, 35–41 (1978)Google Scholar
  126. 126.
    Olsen, S.: Mesangial thickening and nodular glomerular sclerosis in diabetes mellitus and other diseases. Acta Pathol. Microbiol. Scand. [A] 80, (Suppl. 233), 203–216 (1972)Google Scholar
  127. 127.
    Schubert, G.E., Adam, A.: Glomerular nodules and long-spacing collagen in kidneys of patient with multiple myeloma. J. Clin. Pathol. 27, 800–805 (1974)Google Scholar
  128. 128.
    Harrington, A.R., Hare, H.G., Chambers, W.M., Valmin, H.: Nodular glomerulosclerosis suspected during life in a patient without demonstrable diabetes mellitus. N. Engl. J. Med. 275, 206–208 (1966)Google Scholar
  129. 129.
    Strauss, F.G., Argy, W.P., Jr., Schreiner, G.E.: Diabetic glomerulosclerosis in the absence of glucose intolerance. Ann. Intern. Med. 75, 239–242 (1971)Google Scholar
  130. 130.
    Tchobroutsky, G.: Can one prevent and how to treat diabetic nephropathy. In: M. Maxwell (Ed): Advances in nephrology. Chicago: Year Book Med. Publ. 1978 (in press)Google Scholar
  131. 131.
    Fajans, S.S., Taylor, C.I., Floyd, J. C, Jr., Conn, J.W.: Some aspects of the natural history of diabetes mellitus. In: W.J. Malaisse, J. Pirart, J. Vallance-Owen (Eds): Diabetes, pp. 329–340. Amsterdam: Excerpta Med. Int. Congr. Ser. 1974Google Scholar
  132. 132.
    Lazarow, A.: Glomerular basement membrane thickening in diabetes. In: J. Östman, R.D.G. Milner (Eds): Diabetes, pp. 301–306. Amsterdam: Excerpta Med. Int. Congr. Ser. 1969Google Scholar
  133. 133.
    Ireland, J.T.: Diagnostic criteria in the assessment of glomerular capillary basement membrane lesions in newly diagnosed juvenile diabetics. In: R.A. Camerini Davalos, H.S. Cole (Eds): Early Diabetes, pp. 273–278. New York: Academic Press 1970Google Scholar
  134. 134.
    Osterby, R.: Course of diabetic glomerulopathy. In: K. Lundbaek, H. Keen (Eds), Blood vessel disease in diabetes mellitus, Acta Diabetol. Lat. 8 (Suppl. 1), 179–191 (1971)Google Scholar
  135. 135.
    Pardo, V., Perez-Stable, E., Alzamora, D.B., Cleveland, W.W.: Incidence and significance of muscle capillary basal lamina thickness in juvenile diabetes. Am. J. Pathol. 68, 67–78 (1972)Google Scholar
  136. 136.
    Cameron, J.S., Ireland, J.T., Watkins, P.J.: The kidney and renal tract. In: H. Keen, J. Jarrett (Eds), Complications of diabetes, pp. 99–150. London: Arnold 1975Google Scholar
  137. 137.
    Ireland, J.T., Patnaik, B.K., Duncan, L.J.P.: Glomerular ultrastructure in secondary diabetics and normal subjects. Diabetes 16, 628–642 (1967)Google Scholar
  138. 138.
    Lyra de Lacerda, S., Bernades, P., Lenriot, J.P., Feingold, J., Tchobroutsky, G.: Les facteurs génétiques interviennent-ils dans la genèse du diabète sucré des pancréatopathies chroniques? In: Journées Diabétol. Hôtel-Dieu, pp. 45–52. Paris: Flammarion 1978Google Scholar
  139. 139.
    Raskin, P., Marks, J.F., Burns, M., Jr., Plumer, M.E., Siperstein, M.D.: Capillary basement membrane width in diabetic children. Am. J. Med. 58, 365–372 (1975)Google Scholar
  140. 140.
    Jackson, R., Guthrie, R., Esterly, J., Bilginturan, N., James, R., Yeast, J., Saathof, J., Guthrie, D.: Muscle capillary basement membrane changes in normal and diabetic children (abstract). Diabetes 24 (Suppl. 2), 400 (1975)Google Scholar
  141. 141.
    Sheikholislam, B.M., Irias, J.J., Lin, H.J., Lowrey, G.H., Stephenson, S.R., Peterson, G.E., Devereux, D.F., Volk, T.L.: Carbohydrate metabolism and capillary basement-membrane thickness in children. I — Cross-sectional studies. Diabetes 25, 650–660 (1976)Google Scholar
  142. 142.
    Sheikholislam, B.M., Irias, J.J., Lowrey, G.H., Lin, H.J.: Carbohydrate metabolism and capillary basement-membrane thickness in children. II — Longitudinal studies. Diabetes 25, 661–666 (1976)Google Scholar
  143. 143.
    Thomas, P.K., Ward, J.D.: Diabetic neuropathy. In: H. Keen, J. Jarrett (Eds): Complications of diabetes, pp. 151–177. London: Arnold 1975Google Scholar
  144. 144.
    Ingelfinger, F.J.: Debates on diabetes. N. Engl. J. Med. 296, 1228–1229 (1977)Google Scholar
  145. 145.
    Knibbs, S., Jackson, J.G.L.: Social and emotional complications of diabetes. In: H. Keen, J. Jarrett (Eds): Complications of diabetes, pp. 265–277. London: Arnold 1975Google Scholar
  146. 146.
    Guthrie, R.A.: Young people and diabetes-control makes sense. Diabetes Forecast 30, 18–21 (1977)Google Scholar
  147. 147.
    Shepherd, G.R.: Diabetes mellitus of juvenile onset with 40 years'survival and no gross damage. Arch. Intern. Med. 128, 284–290 (1971)Google Scholar
  148. 148.
    Krall, L.P.: For Peter Forsham M. D. — The accent is on living. Diabetes Forecast 30, 14–16 (1977)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • G. Tchobroutsky
    • 1
  1. 1.Service de DiabétologieHôtel-Dieu HospitalParisFrance

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