A chronic grey matter penumbra, lateral microvascular intussusception and venous peduncular avulsion underlie diabetic vitreous haemorrhage

British Journal of Ophthalmology

Volumn 91, Issue 5, 2007, Pages 677-689

  McLeod, David ^a  

^a MANCHESTER ROYAL EYE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; DIABETIC RETINOPATHY; GRAY MATTER; HUMAN; HYPOXIA; INTUSSUSCEPTION; OPTIC DISK; PRIORITY JOURNAL; RETINA ISCHEMIA; REVIEW; UPREGULATION; VITREOUS BODY DETACHMENT; VITREOUS HEMORRHAGE;

CAPILLARIES; CONSTRICTION, PATHOLOGIC; DIABETIC ANGIOPATHIES; DIABETIC RETINOPATHY; HUMANS; ISCHEMIA; NEOVASCULARIZATION, PHYSIOLOGIC; OPTIC NERVE DISEASES; RETINAL VESSELS; VITREOUS HEMORRHAGE;

EID: 34248174810     PISSN: 00071161     EISSN: None     Source Type: Journal    
DOI: 10.1136/bjo.2006.109199     Document Type: Review

References (127)

1. Davis MD, Blodi BA. Proliferative diabetic retinopathy. In: Ryan SJ, ed, Retina 3rd edn.St Louis:Mosby, 2001:1309-49.
2. Ballantyne AJ. The state of the retina in diabetes mellitus. Doyne Memorial Medal Lecture. Trans Ophthalmol Soc UK 1946;66:503-43.
3. Ballantyne AJ, Michaelson IC. Textbook of the fundus of the eye. Edinburgh, London: E&S Livingstone, 1965.
4. Cogan DG, Toussaint D, Kuwabara T. Retinal vascular patterns IV. Diabetic retinopathy. Arch Ophthalmol 1961;66:366-78.
5. Davis MD. The natural history of diabetic retinopathy. Trans Am Acad Ophthalmol Otolaryngol 1968;72:237-40.
6. Wise GN. Retinal neovascularisation. Trans Am Ophthalmol Soc 1956;54:729-826.
7. Dobree JH. Proliferative diabetic retinopathy: evolution of the retinal lesions. Br J Ophthalmol 1964;48:637-49.
8. Wise GN, Dollery CT, Henkind P. The retinal circulation. New York: Harper and Row, 1971; 265-78, 422-53).
9. Bek T. Venous loops and reduplications in diabetic retinopathy: prevalence, distribution, and pattern of development. Acta Ophthalmol Scand 1999;77:130-4.
10. Djonov V, Schmid M, Tschanz SA, et al. Intussusceptive angiogenesis: its role in embryonic vascular network formation. Circ Res 2000;86:286-92.
11. Augustin HG. Tubes, branches and pillars: the many ways of forming a new vasculature. Circ Res 2001;89:645-7.
12. Burri PH, Hlushchuk R, Djonov V. Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev Dyn 2004;231:474-88.
13. Patan S, Munn LL, Tanda S, et al. Vascular morphogenesis and remodeling in a model of tissue repair: blood vessel formation and growth in the ovarian pedicel after ovariectomy. Circ Res 2001;89:723-31.
14. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003;3:401-10.
15. Davis GE, Senger DR. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 2005;97:1093-107.
16. Williams JM Sr, de Juan E Jr, Machemer R. Ultrastructural characteristics of new vessels in proliferative diabetic retinopathy. Am J Ophthalmol 1988;105:491-9.
17. Gass JDM. Stereoscopic atlas of macular disease: diagnosis and treatment, 4th edn. St Louis: Mosby, 1997:516-22.
18. Michaelson IC. The mode of development of the vascular system of the retina, with some observations on its significance for certain retinal diseases. Trans Ophthalmol Soc UK 1948;68:137-80.
19. Grant MB, May WS, Caballero S, et al. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med 2002;8:607-12.
20. Hill CR, Kissun RD, Weiss JB, et al. Angiogenic factor in vitreous from diabetic retinopathy. Experientia 1983;39:583-5.
21. Grant M, Russell B, Fitzgerald C, et al. Insulin-like growth factors in vitreous. Studies in control and diabetic subjects with neovascularization. Diabetes 1986;35:416-20.
22. Taylor CM, Kissun RD, Schor AM, et al. Endothelial cell-stimulating angiogenesis factor in vitreous from extraretinal neovascularisations. Invest Ophthalmol Vis Sci 1989;30:2174-8.
23. Sivalingam A, Kenney J, Brown GC, et al. Basic fibroblast growth factor levels in the vitreous of patients with proliferative diabetic retinopathy. Arch Ophthalmol 1990;108:869-72.
24. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 1994;331:1480-7.
25. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol 1994;118:445-50.
26. Khaliq A, Foreman D, Ahmed A, et al. Increased expression of placenta growth factor in proliferative diabetic retinopathy. Lab Invest 1998;78:109-16.
27. Canton A, Burgos R, Hernandez C, et al. Hepatocyte growth factor in vitreous and serum from patients with proliferative diabetic retinopathy. Br J Ophthalmol 2000;84:732-5.
28. Watanabe D, Suzuma K, Matsui S, et al. Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med 2005;353:782-92.
29. Patel JI, Hykin PG, Gregor ZJ, et al. Angiopoietin concentrations in diabetic retinopathy. Br J Ophthalmol 2005;89:480-3.
30. Kohner EM, Hamilton AM, Joplin GF, et al. Florid diabetic retinopathy and its response to treatment by photocoagulation or pituitary ablation. Diabetes 1976;25:104-10.
31. Kuiper EJ, de Smet MD, van Meurs JC, et al. Association of connective tissue growth factor with fibrosis in vitreoretinal disorders in the human eye. Arch Ophthalmol 2006;124:1457-62.
32. Thieme H, Aiello LP, Takagi H, et al. Comparative analysis of vascular endothelial growth factor receptors on retinal and aortic vascular endothelial cells. Diabetes 1995;44:98-103.
33. Aiello LP, Northrup JM, Keyt BA, et al. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol 1995;113:1538-44.
34. Shima D, Adamis AP, Ferrara N, et al. Hypoxic induction of endothelial cell growth factors in retinal cells: identification and characterisation of vascular endothelial growth factor (VEGF) as the sole mitogen. Mol Med 1995;2:182-93.
35. Tolentino MJ, McLeod DS, Taomoto M, et al. Pathologic features of vascular endothelial growth factor-induced retinopathy in the nonhuman primate. Am J Ophthalmol 2002;133:373-85.
36. Aiello LP, Pierce EA, Foley ED, et al. Suppression of retinal neovascularisation in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci USA 1995;92:10457-61.
37. Amin RH, Frank RN, Kennedy A, et al. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 1997;38:36-47.
38. Boulton M, Foreman D, Williams G, et al. VEGF localisation in diabetic retinopathy. Br J Ophthalmol 1998;82:561-8.
39. Smith G, McLeod D, Foreman D, et al. Immunolocalisation of the VEGF receptors FLT-1, KDR, and FLT-4 in diabetic retinopathy. Br J Ophthalmol 1999;83:486-94.
40. Eriksson U, Alitalo K. VEGF receptor 1 stimulates stem-cell recruitment and new hope for angiogenesis therapies. Nat Med 2002;8:775-7.
41. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 2003;161:1163-77.
42. Ashton N. Injection of the retinal vascular system in the enucleated eye in diabetic retinopathy. Br J Ophthalmol 1950;34:38-41.
43. Ashton N. Arteriolar involvement in diabetic retinopathy. Br J Ophthalmol 1953;37:282-92.
44. Bresnick GH, Engerman R, Davis MD, et al. Patterns of ischaemia in diabetic retinopathy. Trans Am Acad Ophthalmol Otolaryngol 1976;81:694-709.
45. Shimizu K, Kobayashi Y, Muraoka K. Mid-peripheral fundus involvement in diabetic retinopathy. Ophthalmology 1981;88:601-12.
46. Cogan DG, Kuwabara T. Capillary shunts in the pathogenesis of diabetic retinopathy. Diabetes 1963;12:293-300.
47. Lee PF. Clinical and histological findings in diabetic retinopathy. Am J Ophthalmol 1968;65:688-95.
48. Tanaka T, Muraoka K, Tokui K. Retinal arteriovenous shunt at the arteriovenous crossing. Ophthalmol 1998;105:1251-8.
49. Grunwald JE, Brucker AJ, Grunwald SE, et al. Retinal haemodynamics in proliferative diabetic retinopathy; a laser Doppler velocimetry study. Invest Ophthalmol Vis Sci 1993;34:66-71.
50. Barouch FC, Miyamoto K, Allport JR, et al. Integrin-mediated neutrophil adhesion and retinal leukostasis in diabetes. Invest Ophthalmol Vis Sci 2000;41:1153-8.
51. Ashton N. Retinal vascularization in health and disease. Am J Ophthalmol 1957;44:7-17.
52. Archer DB. Neovascularisation of the retina (Treacher Collins Prize Essay 1976). Trans Ophthalmol Soc UK 1976;96:471-93.
53. Boulton ME, McLeod D, Garner A. Vasoproliferative retinopathies: clinical, morphogenetic and modulatory aspects. Eye, 1988;2, S124-39.
54. Hersh PS, Green WR, Thomas JV. Tractional venous loops in diabetic retinopathy. Am J Ophthalmol 1981;92:661-71.
55. Kohner EM, McLeod D, Marshall J. Diabetic eye disease. In: Keen H, Jarrett J, eds, Complications of diabetes.London:Edward Arnold, 1982.
56. Wise GN. Factors influencing retinal new vessel formation. Am J Ophthalmol 1961;52:637-50.
57. Michels RG. Vitreous surgery. London: CV Mosby, 1981, 174, 222..
58. Gerhardinger C, Brown LF, Roy S, et al. Expression of vascular endothelial growth factor in the human retina and in non-proliferative diabetic retinopathy. Am J Pathol 1998;152:1453-62.
59. Pe'er J, Folberg R, Itin A, et al. Upregulated expression of vascular endothelial growth factor in proliferative diabetic retinopathy. Br J Ophthalmol 1996;80:241-5.
60. Astrup J, Siesjo BK, Symon L. Thresholds in cerebral ischaemia-the ischaemic penumbra. Stroke 1982;12:723-5.
61. Kidwell CS, Alger JR, Saver JL. Evolving paradigms in neuroimaging of the ischemic penumbra. Stroke 2004;35:2662-5.
62. Issa R, Krupinski J, Bujny T, et al. Vascular endothelial growth factor and its receptor, KDR, in human brain tissue after ischemic stroke. Lab Invest 1999;79:417-25.
63. Slevin M, Krupinski J, Slowik A, et al. Activation of MAP kinase (ERK-1/ERK-2), tyrosine kinase and VEGF in the human brain following acute ischaemic stroke. Neuroreport 2000;11:2759-64.
64. Marti HJ, Bernaudin M, Bellail A, et al. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 2000;156:965-76.
65. Zhang ZG, Zhang L, Tsang W, et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002;22:379-92.
66. Ashton N. Studies of the retinal capillaries in relation to diabetic and other retinopathies. Br J Ophthalmol 1963;47:521-38.
67. Komoto G. The pathological anatomy of the retina and choroid after complete and partial removal of their respective blood supplies. Trans Ophthalmol Soc UK 1915;35:295-308.
68. Hayreh SS, Weingeist TA. Experimental occlusion of the central artery of the retina. IV: retinal tolerance time to acute ischaemia, Br J Ophthalmol 1980;64:818-25.
69. Hayreh SS, Zimmerman MB. Central retinal artery occlusion: visual outcome. Am J Ophthalmol 2005;140:376-91.
70. Oji EO, McLeod D. Partial central retinal artery occlusion. Trans Ophthalmol Soc UK 1978;98:156-9.
71. McLeod D, Oji EO, Kohner EM, et al. Fundus signs in temporal arteritis. Br J Ophthalmol 1978;62:591-4.
72. McLeod D. Why cotton-wool spots should not be regarded as retinal nerve fibre layer infarcts. Br J Ophthalmol 2005;89:229-37.
73. Neupert JR, Brubaker RF, Kearns TP, et al. Rapid resolution of venous stasis retinopathy after carotid endarterectomy. Am J Ophthalmol 1976;81:600-2.
74. Muraoka K, Shimizu K. Intraretinal neovascularization in diabetic retinopathy. Ophthalmology 1984;91:1440-6.
75. Nork TM, Wallow IH, Sramek SJ, et al. Muller's cell involvement in proliferative diabetic retinopathy. Arch Ophthalmol 1987;105:1424-9.
76. Bek T. Transretinal histopathological changes in capillary-free areas of diabetic retinopathy. Acta Ophthalmol (Copenh), 1994;72:409-415.
77. Bek T. Localised scotomata and types of vascular occlusion in diabetic retinopathy. Acta Ophthalmol (Copenh), 1991;69:11-18.
78. Stitt AW, Gardiner TA, Archer DB. Retinal and choroidal responses to panretinal photocoagulation: an ultrastructural perspective. Graefes Arch Clin Exp Ophthalmol 1995;233:699-705.
79. Stefansson E. Ocular oxygenation and the treatment of diabetic retinopathy. Surv Ophthalmol 2006;51:364-80.
80. Blankenship GW. A clinical comparison of central and peripheral argon laser panretinal photocoagulation for proliferative diabetic retinopathy. Ophthalmology 1988;95:170-7.
81. McLeod D. Microsurgical management of neovascularisation secondary to posterior segment iscnaemia. Eye 1991;5:252-9.
82. Taylor E, Dobree JH. Proliferative diabetic retinopathy: site and size of initial lesions. Br J Ophthalmol 1970;54:11-18.
83. Verdaguer J, le Clercq N, Holuigue J, et al. Nonproliferative diabetic retinopathy with significant capillary nonperfusion. Graefes Arch Clin Exp Ophthalmol 1987;225:157-9.
84. Kurz H, Burri PH, Djonov VG. Angiogenesis and vascular remodeling by intussusception: from form to function. News Physiol Sci 2003;18:65-70.
85. Garcia-Cardena G, Comander J, Anderson KR, et al. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci USA 2001;98:4478-85.
86. Bek T. A clinicopathological study of venous loops and reduplications in diabetic retinopathy. Acta Ophthalmol Scand 2002;80:69-75.
87. Davis MD. Vitreous contraction in proliferative diabetic retinopathy. Arch Ophthalmol 1965;74:741-51.
88. Tolentino FI, Lee PF, Schepens CL. Biomicroscopic study of vitreous cavity in diabetic retinopathy. Arch Ophthalmol 1966;75:238-46.
89. Faulborn J, Bouala S. Microproliferations in proliferative diabetic retinopathy and their relationship to the vitreous: corresponding light and electron microscopic studies. Graefes Arch Clin Exp Ophthalmol 1985;223:130-8.
90. Hamilton CW, Chandler D, Klintworth GK, et al. A transmission and scanning electron microscopic study of surgically excised preretinal membrane proliferations in diabetes mellitus. Am J Ophthalmol 1982;94:473-88.
91. Dawson DW, Volpert OV, Gillis P, et al. Pigment epithelium-derived growth factor: a potent inhibitor of angiogenesis. Science 1999;285:245-8.
92. Cai J, Jiang WG, Grant MB, et al. Pigment epithelium-derived factor inhibits angiogenesis via regulated intracellular proteolysis of vascular endothelial growth factor receptor 1. J Biol Chem 2006;281:3604-13.
93. Reardon AJ, Le Goff M, Briggs MD, et al. Identification in vitreous and molecular cloning of opticin, a novel member of the family of leucine-rich repeat proteins of the extracellular matrix. J Biol Chem 2000;275:2123-9.
94. Ramesh S, Bonshek RE, Bishop PN. Immunolocalisation of opticin in the human eye. Br J Ophthalmol 2004;88:697-702.
95. Foos RY. Vitreoretinal juncture - simple epiretinal membranes. Graefes Arch Clin Exp Ophthalmol 1974;189:231-50.
96. Charles S. Vitreous microsurgery. Baltimore: Williams and Wilkins, 1981.
97. McLeod D, Hiscott PS, Grierson I. Age-related cellular proliferation at the vitreoretinal juncture. Eye 1987;1:263-81.
98. Duke Elder S, Dobree JH. System of ophthalmology. London: Henry Kimpton, 1967:422-48.
99. Lincoff H, Serag Y, Chang S, et al. Tractional elevations of the retina in patients with diabetes. Am J Ophthalmol 1992;113:235-42.
100. Machemer R. Pathogenesis of proliferative neovascular retinopathies and the role of vitrectomy. A hypothesis. Int Ophthalmol 1978;1:1-3.
101. Akiba J, Arzabe CW, Trempe CL. Posterior vitreous detachment and neovascularization in diabetic retinopathy. Ophthalmology 1990;97:889-91.
102. Casaroli Marano RP, Preissner KT, Vilaro S. Fibronectin, laminin, vitronectin and their receptors at newly-formed capillaries in proliferative diabetic retinopathy. Exp Eye Res 1995;60:5-17.
103. Luna J, Tobe T, Mousa SA, et al. Antagonists of integrin alpha v beta 3 inhibit retinal neovascularization in a murine model. Lab Invest 1996;75:563-73.
104. Friedlander M, Theesfeld CL, Sugita M, et al. Involvement of integrins alpha v beta 3 and alpha v beta 5 in ocular neovascular diseases. Proc Natl Acad Sci USA 1996;93:9764-9.
105. Soldi R, Mitola S, Strasly M, et al. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 1999;18:882-92.
106. McLeod D. Closed intraocular microsurgery for advanced diabetic eye disease. In: Kanski JJ, Morse PH, eds. Disorders of the vitreous, retina and choroid. London: Butterwoths, 1983.
107. Wong HC, Sehmi KS, McLeod D. Abortive neovascular outgrowths discovered during vitrectomy for diabetic vitreous haemorrhage. Graefes Arch Clin Exp Ophthalmol 1989;227:237-40.
108. Hiscott P, Cooling RJ, Rosen P, et al. The pathology of abortive neovascular outgrowths from the retina. Graefes Arch Clin Exp Ophthalmol 1992;230:531-6.
109. Finkelstein D, Patz A, Fine SL, et al. Abortive foveal retinal neovascularisation in diabetic retinopathy. Retina 1981;1:62-66.
110. McLeod D, James CR. Viscodelamination at the vitreoretinal juncture in severe diabetic eye disease. Br J Ophthalmol 1988;72:413-19.
111. Asaria RHY, Kon CH, Bunce C, et al. Silicone oil concentrates fibrogenic growth factors in the retro-oil fluid. Br J Ophthalmol 2004;88:1439-42.
112. Wang J, McLeod D, Henson DB, et al. Age-dependent changes in the basal retinovitreous adhesion. Invest Ophthalmol Vis Sci 2003;44:1793-800.
113. Kuwabara T, Cogan DG. Studies of retinal vascular patterns I: normal architecture. Arch Ophthalmol 1960;64:904-11.
114. Lewis H, Abrams GW, Foos RY. Clinicopathological findings in anterior hyaloidal fibrovascular proliferation after diabetic vitrectomy. Am J Ophthalmol 1987;104:614-18.
115. Terasaki H, Miyake Y, Mori M, et al. Fluorescein angiography of extreme peripheral retina and rubeosis iridis in proliferative diabetic retinopathy. Retina 1999;19:302-8.
116. Stefansson E, Novack RL, Hatchell DL. Vitrectomy prevents retinal hypoxia in branch retinal vein occlusion. Invest Ophthalmol Vis Sci 1990;31:284-9.
117. McLeod D, Marshall J, Kohner EM, et al. The role of axoplasmic transport in the pathogenesis of retinal cotton-wool spots. Br J Ophthalmol 1977;61:177-91.
118. Holekamp NM, Shui YB, Beebe D. Lower intraocular oxygen tension in diabetic patients: possible contribution to decreased incidence of nuclear sclerotic cataract. Am J Ophthalmol 2006;141:1027-32.
119. Itokura H, Kishi S, Kotajima N, et al. Persistent secretion of vascular endothelial growth factor into the vitreous cavity in proliferative diabetic retinopathy after vitrectomy. Ophthalmology 2004;111:1880-4.
120. Barry PJ, Hiscott PS, Grierson I, et al. Reparative epiretinal fibrosis after diabetic vitrectomy. Trans Ophthalmol Soc UK 1985;104:285-96.
121. Foos RY, Roth AM. Surface structure of the optic nerve head 2. Vitreopapillary attachments and posterior vitreous detachment. Am J Ophthalmol 1073;76:662-71.
122. Foos RY, Kreiger AE, Forsythe AB, et al. Posterior vitreous detachment in diabetic subjects. Ophthalmol 1980;87:122-8.
123. Henkind P. Ocular neovascularisation. (The Krill Memorial Lecture). Am J Ophthalmol 1978;85:287-301.
124. Asdourian GK, Goldberg MF, Busse B. Optic disc neovascularization of uveal (choroidal or posterior ciliary) origin. Arch Ophthalmol 1977;95:998-1003.
125. Jacobs NA, Steele CA, Mills KB. Origin of disc new vessels assessed by videofluorography. Br J Ophthalmol 1988;72:394-8.
126. McLeod D, Restori M. Ultrasonic examination in severe diabetic eye disease. Br J Ophthalmol 1979;63:533-8.
127. Pendergast SD, Martin DF, Proia AD, et al. Removal of optic disc stalks during diabetic vitrectomy. Retina 1995;15:25-8.