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January 1996, Vol 114, No. 1 >
ARTICLE | January 1996

Structure and Function of the Corneal Endothelium in Diabetes Mellitus Type I and Type II FREE

Lill-Inger Larsson, MD; William M. Bourne, MD; John M. Pach, MD; Richard F. Brubaker, MD
Arch Ophthalmol. 1996;114(1):9-14. doi:10.1001/archopht.1996.01100130007001
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Objective:  To measure and compare corneal endothelial morphologic characteristics and function in subjects with diabetes mellitus types I and II.

Design:  Forty-nine patients with diabetes mellitus type I and 60 patients with diabetes mellitus type II were recruited from the active practice of the Mayo Clinic, Rochester, Minn. Thirty-one normal subjects, divided by age into two overlapping groups of 20 each, served as controls. Corneal endothelial permeability and corneal autofluorescence were measured by fluorophotometry. Central corneal endothelial photographs were taken with a wide-field specular microscope, which also measured the corneal thickness.

Results:  Neither the type I nor the type II diabetics differed from their controls in endothelial permeability and endothelial cell density. The type I diabetics had polymegethism, pleomorphism, increased corneal thickness, and increased corneal autofluorescence compared with their controls. Similar measured values were found in the type II diabetics, but they did not differ significantly from those of their age-matched controls. The type II diabetics were older than the type I diabetics, and the older control group showed changes similar to those seen in the diabetics; these changes were presumably associated with aging. The severity of retinopathy was significantly correlated only with corneal autofluorescence.

Conclusions:  The corneas of patients with type I diabetes mellitus exhibit abnormalities in endothelial cell morphologic characteristics and corneal autofluorescence. The changes resemble those that occur with aging in normal subjects, making them difficult to discern as abnormal in type II diabetics, who are usually older. We found no abnormalities in endothelial permeability in either type I or type II diabetics.

REFERENCES

1 +
Perry HD, Foulks GN, Thoft RA, Tolentino FI.  Corneal complications after closed vitrectomy through pars plana . Arch Ophthalmol . 1978;;96:1401-1403.
2 +
Michels RG, Ryan SJ.  Results and complications of 100 consecutive cases of pars plana vitrectomy . Am J Ophthalmol . 1975;;80:24-36.
3 +
Foulks GN, Thoft RA, Perry HD, Tolentino FI.  Factors related to corneal epithelial complications after closed vitrectomy in diabetics . Arch Ophthalmol . 1979;;97:1076-1078.
4 +
Göbbels M, Spitznas M, Oldendoerp J.  Impairment of corneal epithelial barrier function in diabetics . Graefes Arch Clin Exp Ophthalmol . 1989;;227:142-144.
5 +
Stolwijk TR, van Best JA, Boot JP, Lemkes HHPJ, Oosterhuis JA.  Corneal epithelial barrier function after oxybuprocaine provocation in diabetics . Invest Ophthalmol Vis Sci . 1990;;31:436-439.
6 +
Olsen T, Busted N, Schmitz O.  Corneal thickness in diabetes mellitus . Lancet . 1980;;1:883.
7 +
Busted N, Olsen T, Schmitz O.  Clinical observations on the corneal thickness and the corneal endothelium in diabetes mellitus . Br J Ophthalmol . 1981;;65:687-690.
8 +
Herse P, Hooker B.  Corneal edema recovery dynamics in diabetes: is the alloxan induced rabbit a useful model? Invest Ophthalmol Vis Sci . 1994;;35:310-313.
9 +
Weston BC, Bourne WM, Polse KA, Hodge DO.  Corneal hydration control in diabetes mellitus . Invest Ophthalmol Vis Sci . 1995;;36:586-595.
10 +
Schultz RO, Matsuda M, Yee RW, Edelhauser HF, Schultz KJ.  Corneal endothelial changes in type I and type II diabetes mellitus . Am J Ophthalmol . 1984;;98:401-410.
11 +
Keoleian GM, Pach JM, Hodge DO, Trocme SD, Bourne WM.  Structural and functional studies of the corneal endothelium in diabetes mellitus . Am J Ophthalmol . 1992;;113:64-70.
12 +
Itoi M, Nakamura T, Mizobe K, Kodama Y, Nakagawa N, Itoi M.  Specular microscopic studies of the corneal endothelium of Japanese diabetics . Cornea . 1989;;8:2-6.
13 +
Matsuda M, Ohguro N, Ishimoto I, Fukuda M.  Relationship of corneal endothelial morphology to diabetic retinopathy, duration of diabetes and glycemic control . Jpn J Ophthalmol . 1990;;34:53-56.
14 +
Yee RW, Matsuda M, Kern TS, Engerman RL, Edelhauser HF.  Corneal endothelial changes in diabetic dogs . Curr Eye Res . 1985;;4:759-766.
15 +
Rao GN, Shaw EL, Arthur EJ, Aquavella JV.  Endothelial cell morphology and corneal deturgescence . Ann Ophthalmol . 1979;;11:885-899.
16 +
Bourne WM, Brubaker RF, O'Fallon WM.  Use of air to decrease endothelial cell loss during intraocular lens implantation . Arch Ophthalmol . 1979;;97:1473-1475.
17 +
Carlson KH, Bourne WM.  The clinical measurement of endothelial permeability . Cornea . 1988;;7:183-189.
18 +
Lass JH, Spurney RV, Dutt RM, et al.  A morphologic and fluorophotometric analysis of the corneal endothelium in type I diabetes mellitus and cystic fibrosis . Am J Ophthalmol . 1985;;100:783-788.
19 +
Watsky MA, McDermott ML, Edelhauser HF.  In vitro corneal endothelial permeability in rabbit and human: the effects of age, cataract surgery and diabetes . Exp Eye Res . 1989;;49:751-767.
20 +
Ederer F.  Shall we count numbers of eyes or numbers of subjects? Arch Ophthalmol . 1973;;89:1-2.
21 +
Rosner B.  Statistical methods in ophthalmology: an adjustment for the intra-class correlation between eyes . Biometrics . 1982;;38:105-114.
22 +
Ray WA, O'Day DM.  Statistical analysis of multi-eye data in ophthalmic research . Invest Ophthalmol Vis Sci . 1985;;26:1186-1188.
23 +
Katz J.  Two eyes or one? The data analyst's dilemma . Ophthalmic Surg . 1988;;19:585-589.
24 +
McLaren JW, Brubaker RF.  A two-dimensional scanning ocular fluorophotometer . Invest Ophthalmol Vis Sci . 1985;;26:144-152.
25 +
Diabetic Retinopathy Study Research Group.  Report No. 7: a modification of the Airlie House classification of diabetic retinopathy . Invest Ophthalmol Vis Sci . 1981;;21:210-226.
26 +
Early Treatment Diabetic Retinopathy Study Research Group. Manual of Operations . Springfield, Va: US Dept of Commerce, National Technical Information Service; 1985;. Accession No. PB85 223006/AS.
27 +
Bourne WM, Enoch JM.  Some optical principles of the clinical specular microscope . Invest Ophthalmol Vis Sci . 1976;;15:29-32.
28 +
Carlson KH, Bourne WM, McLaren JW, Brubaker RF.  Variations in human corneal endothelial cell morphology and permeability to fluorescein with age . Exp Eye Res . 1988;;47:27-41.
29 +
Baratz KH, Trocme SD, Bourne WM.  Cold-induced corneal edema in patients with trigeminal nerve dysfunction . Am J Ophthalmol . 1991;;112:548-556.
30 +
Ota Y, Mishima S, Maurice DM.  Endothelial permeability of the living cornea to fluorescein . Invest Ophthalmol . 1974;;13:945-949.
31 +
Chang S-W, Hu F-R.  Changes in corneal autofluorescence and corneal epithelial barrier function with aging . Cornea . 1993;;12:493-499.
32 +
Stolwijk TR, van Best JA, Boot JP, Oosterhuis JO.  Corneal autofluorescence in diabetic and penetrating keratoplasty patients as measured by fluorophotometry . Exp Eye Res . 1990;;51:403-409.
33 +
Stolwijk TR, van Best JA, Oosterhuis JA, Swarr W.  Corneal autofluorescence: an indicator of diabetic retinopathy . Invest Ophthalmol Vis Sci . 1992;;33:92-97.
34 +
Kuppens E, Stolwijk T, van Best J, de Keizer R.  Topical timolol, corneal epithelial permeability and autofluorescence in glaucoma by fluorophotometry . Graefes Arch Clin Exp Ophthalmol . 1994;;232:215-220.
35 +
Boets EPM, van Best JA.  Corneal autofluorescence and epithelial barrier function . Cornea . 1994;;13:373-374.
36 +
Larsen M, Kjer B, Bendtson I, Dalgaard P, Lund-Andersen H.  Lens fluorescence in relation to metabolic control of insulin-dependent diabetes mellitus . Arch Ophthalmol . 1989;;107:59-62.
37 +
Laing RA, Fischbarg J, Chance B.  Noninvasive measurements of pyridine nucleotide fluorescence from the cornea . Invest Ophthalmol Vis Sci . 1980;;19:96-102.
38 +
Masters BR.  In vivo redox fluorometry . In: Masters BR, ed. Noninvasive Diagnostic Techniques in Ophthalmology . New York, NY: Springer-Verlag Inc; 1990;:223-247.
39 +
Master BR, Falk S, Chance B.  In vivo flavoprotein redox measurements of rabbit corneal normoxic-anoxic transitions . Curr Eye Res . 1981;;1:623-627.

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1 +
Perry HD, Foulks GN, Thoft RA, Tolentino FI.  Corneal complications after closed vitrectomy through pars plana . Arch Ophthalmol . 1978;;96:1401-1403.
2 +
Michels RG, Ryan SJ.  Results and complications of 100 consecutive cases of pars plana vitrectomy . Am J Ophthalmol . 1975;;80:24-36.
3 +
Foulks GN, Thoft RA, Perry HD, Tolentino FI.  Factors related to corneal epithelial complications after closed vitrectomy in diabetics . Arch Ophthalmol . 1979;;97:1076-1078.
4 +
Göbbels M, Spitznas M, Oldendoerp J.  Impairment of corneal epithelial barrier function in diabetics . Graefes Arch Clin Exp Ophthalmol . 1989;;227:142-144.
5 +
Stolwijk TR, van Best JA, Boot JP, Lemkes HHPJ, Oosterhuis JA.  Corneal epithelial barrier function after oxybuprocaine provocation in diabetics . Invest Ophthalmol Vis Sci . 1990;;31:436-439.
6 +
Olsen T, Busted N, Schmitz O.  Corneal thickness in diabetes mellitus . Lancet . 1980;;1:883.
7 +
Busted N, Olsen T, Schmitz O.  Clinical observations on the corneal thickness and the corneal endothelium in diabetes mellitus . Br J Ophthalmol . 1981;;65:687-690.
8 +
Herse P, Hooker B.  Corneal edema recovery dynamics in diabetes: is the alloxan induced rabbit a useful model? Invest Ophthalmol Vis Sci . 1994;;35:310-313.
9 +
Weston BC, Bourne WM, Polse KA, Hodge DO.  Corneal hydration control in diabetes mellitus . Invest Ophthalmol Vis Sci . 1995;;36:586-595.
10 +
Schultz RO, Matsuda M, Yee RW, Edelhauser HF, Schultz KJ.  Corneal endothelial changes in type I and type II diabetes mellitus . Am J Ophthalmol . 1984;;98:401-410.
11 +
Keoleian GM, Pach JM, Hodge DO, Trocme SD, Bourne WM.  Structural and functional studies of the corneal endothelium in diabetes mellitus . Am J Ophthalmol . 1992;;113:64-70.
12 +
Itoi M, Nakamura T, Mizobe K, Kodama Y, Nakagawa N, Itoi M.  Specular microscopic studies of the corneal endothelium of Japanese diabetics . Cornea . 1989;;8:2-6.
13 +
Matsuda M, Ohguro N, Ishimoto I, Fukuda M.  Relationship of corneal endothelial morphology to diabetic retinopathy, duration of diabetes and glycemic control . Jpn J Ophthalmol . 1990;;34:53-56.
14 +
Yee RW, Matsuda M, Kern TS, Engerman RL, Edelhauser HF.  Corneal endothelial changes in diabetic dogs . Curr Eye Res . 1985;;4:759-766.
15 +
Rao GN, Shaw EL, Arthur EJ, Aquavella JV.  Endothelial cell morphology and corneal deturgescence . Ann Ophthalmol . 1979;;11:885-899.
16 +
Bourne WM, Brubaker RF, O'Fallon WM.  Use of air to decrease endothelial cell loss during intraocular lens implantation . Arch Ophthalmol . 1979;;97:1473-1475.
17 +
Carlson KH, Bourne WM.  The clinical measurement of endothelial permeability . Cornea . 1988;;7:183-189.
18 +
Lass JH, Spurney RV, Dutt RM, et al.  A morphologic and fluorophotometric analysis of the corneal endothelium in type I diabetes mellitus and cystic fibrosis . Am J Ophthalmol . 1985;;100:783-788.
19 +
Watsky MA, McDermott ML, Edelhauser HF.  In vitro corneal endothelial permeability in rabbit and human: the effects of age, cataract surgery and diabetes . Exp Eye Res . 1989;;49:751-767.
20 +
Ederer F.  Shall we count numbers of eyes or numbers of subjects? Arch Ophthalmol . 1973;;89:1-2.
21 +
Rosner B.  Statistical methods in ophthalmology: an adjustment for the intra-class correlation between eyes . Biometrics . 1982;;38:105-114.
22 +
Ray WA, O'Day DM.  Statistical analysis of multi-eye data in ophthalmic research . Invest Ophthalmol Vis Sci . 1985;;26:1186-1188.
23 +
Katz J.  Two eyes or one? The data analyst's dilemma . Ophthalmic Surg . 1988;;19:585-589.
24 +
McLaren JW, Brubaker RF.  A two-dimensional scanning ocular fluorophotometer . Invest Ophthalmol Vis Sci . 1985;;26:144-152.
25 +
Diabetic Retinopathy Study Research Group.  Report No. 7: a modification of the Airlie House classification of diabetic retinopathy . Invest Ophthalmol Vis Sci . 1981;;21:210-226.
26 +
Early Treatment Diabetic Retinopathy Study Research Group. Manual of Operations . Springfield, Va: US Dept of Commerce, National Technical Information Service; 1985;. Accession No. PB85 223006/AS.
27 +
Bourne WM, Enoch JM.  Some optical principles of the clinical specular microscope . Invest Ophthalmol Vis Sci . 1976;;15:29-32.
28 +
Carlson KH, Bourne WM, McLaren JW, Brubaker RF.  Variations in human corneal endothelial cell morphology and permeability to fluorescein with age . Exp Eye Res . 1988;;47:27-41.
29 +
Baratz KH, Trocme SD, Bourne WM.  Cold-induced corneal edema in patients with trigeminal nerve dysfunction . Am J Ophthalmol . 1991;;112:548-556.
30 +
Ota Y, Mishima S, Maurice DM.  Endothelial permeability of the living cornea to fluorescein . Invest Ophthalmol . 1974;;13:945-949.
31 +
Chang S-W, Hu F-R.  Changes in corneal autofluorescence and corneal epithelial barrier function with aging . Cornea . 1993;;12:493-499.
32 +
Stolwijk TR, van Best JA, Boot JP, Oosterhuis JO.  Corneal autofluorescence in diabetic and penetrating keratoplasty patients as measured by fluorophotometry . Exp Eye Res . 1990;;51:403-409.
33 +
Stolwijk TR, van Best JA, Oosterhuis JA, Swarr W.  Corneal autofluorescence: an indicator of diabetic retinopathy . Invest Ophthalmol Vis Sci . 1992;;33:92-97.
34 +
Kuppens E, Stolwijk T, van Best J, de Keizer R.  Topical timolol, corneal epithelial permeability and autofluorescence in glaucoma by fluorophotometry . Graefes Arch Clin Exp Ophthalmol . 1994;;232:215-220.
35 +
Boets EPM, van Best JA.  Corneal autofluorescence and epithelial barrier function . Cornea . 1994;;13:373-374.
36 +
Larsen M, Kjer B, Bendtson I, Dalgaard P, Lund-Andersen H.  Lens fluorescence in relation to metabolic control of insulin-dependent diabetes mellitus . Arch Ophthalmol . 1989;;107:59-62.
37 +
Laing RA, Fischbarg J, Chance B.  Noninvasive measurements of pyridine nucleotide fluorescence from the cornea . Invest Ophthalmol Vis Sci . 1980;;19:96-102.
38 +
Masters BR.  In vivo redox fluorometry . In: Masters BR, ed. Noninvasive Diagnostic Techniques in Ophthalmology . New York, NY: Springer-Verlag Inc; 1990;:223-247.
39 +
Master BR, Falk S, Chance B.  In vivo flavoprotein redox measurements of rabbit corneal normoxic-anoxic transitions . Curr Eye Res . 1981;;1:623-627.

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