Brit. J. Ophthal. (1975) 59, 59

Secondary anterior crocodile shagreen of Vogt

R. C. TRIPATHI AND A. J. BRONFrom the Department of Pathology, Institute of OphthalmologyvNuffield Laboratory of Ophthalmology, Oxford

Vogt (1930) described a bilateral central opacifica-tion of the cornea at the level of Bowman's layercomprising a mosaic of polygonal grey opacitiesseparated by clear tissue. The changes occurred in an80-year-old man and were regarded as degenerative;Vogt termed this manifestation "crocodile shagreen ofBowman's membrane". A peripheral variety of thecondition is commonly seen as a senile change (Bron,i968). The axial form has been reported in youthin a man whose father had band-shaped keratopathy(Valerio, 1939, 1942) and has also been described asa dominantly inherited disorder (Kopsa and Marusic,1958). Secondary forms have been described aftertrauma (Muller, I949; Franceschetti and Forni,1950), associated with megalocornea (Boles-Carenini,196I; Malbrafn, D'Alessandro, and Valenzuela,i965), and associated with iris malformation andband-shaped keratopathy (Collier, i962).The morbid anatomical basis for crocodile sha-

green is uncertain. Bron and Tripathi (i 969,1970) have suggested that the anatomical structuresresponsible for the manifestation of the anteriorcorneal mosaic determine the polygonal organiza-tion of the mosaic degeneration. Moro and Amidei(I953) demonstrated a granular stippling of Bow-man's layer similar to that seen in band-shapedkeratopathy, and Muller (I949) reported in a post-traumatic case, an intermittent depression of Bow-man's layer towards the stroma with rupture of thislayer in the valleys so formed.The present report describes a case of secondary

anterior crocodile shagreen occurring in a blinddegenerate globe. The histo-pathological findingsand their significance are discussed.

Case reportA 73-year-old woman came to the Casualty Depart-ment of Moorfields Eye Hospital complaining of a red,painful right eye of 2 weeks' duration. The eye had beenblind since the age of I5 when the patient suffered anepisode of inflammation said to be due to infection.There was no perception of light in the right eye and

the vision in the left eye was 6/i8 improving to 6/12 with

Address for reprints: R. C. Tripathi, M.S., Ph.D., Institute of Ophthal-mology, Judd Street, London, WCIH 9QS

University of London, and the

a pin-hole. The right cornea was diffusely opaque andulcerated centrally. Around the ulcerated zone the centralportion of the superficial cornea showed a dense whitereticular opacity within the confines of which were poly-gonal zones of a fainter opacification. The changessuggested a mosaic degeneration of the cornea (Fig. I).The anterior chamber was observed to be flat and al-though no leakage of aqueous was observed initially,frank perforation and prolapse of the iris occurred withina few days.The left eye was normal in appearance apart from a

minor peripheral corneal opacity; no sign of mosaicdegeneration was present.The right eye, being blind, irritable, and phthisical, was

eventually enucleated August I I, 1971. The cornea wastrephined and fixed for histological study.

HISTOPATHOLOGY

Special attention was paid to the portion of thecornea corresponding to the mosaic degenerationseen clinically. The most prominent changes werefound in the superficial cornea. Bowman's layer wasthrown into prominent ridges variably spaced from100 to 400 um apart (Fig. 2a, b). The epithelium ac-commodated itself to these ridges, and over the apicesthe epithelial cells were compressed and flattened,so that only minor surface irregularity was present(Fig. 2a, b). Bowman's layer was somewhat variablein thickness and ruptured in a few places. A granulardeposit was present irregularly in Bowman's layer;it heavily encrusted the peak of each fold and oftenthe entire ridge (and occasionally the connectivetissue beneath), but was spread only sparsely in thevalleys, usually confined to the subepithelial surfaceof Bowman's layer (Fig. 2b). Histochemically thedeposit stained black with von Kossa, deep purplewith quinalizarine, bright blue with Alcian blue,blue with colloidal iron, and orange red with ali-zarine, and showed a negative reaction with periodicacid-Schiff. These staining characteristics indicatedthe presence of calcium. The separation of the ridgesseen by light microscopy corresponded to those of thereticular pattern seen on biomicroscopy. The stromaas a whole was thinned and scarred, and anteriorlyfollowed the undulating contour of Bowman's layerand showed superficial vascularization peripherally.

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6o British Journal of Ophthalmology

FIG. I Mosaic pattern on corneal surface seen clinically.

Descemet's membrane was of irregular thickness andthe endothelium was degenerate and in placesabsent. The central cornea was perforated. Sectionsof the remainder of the eye showed anterior peri-pheral synechiae occluding the angle of the anteriorchamber. The iris and ciliary body were atrophic andinfiltrated by inflammatory cells. The choroidshowed marked atrophic changes and some thicken-ing of Bruch's membrane with drusen formation.The retina was totally detached and showed areas

of haemorrhage, atrophy, cystoid degeneration, andgliosis. Retinitis proliferans was present in associationwith vitreous haemorrhage. The lens was calcified,cataractous, disorganized, and dislocated. The opticnerve was gliosed.

Discussion

It appears from our present study and those ofMuller (I 949) and Moro and Amidei (I 953) that thegeneral level of opacification seen clinically is due tocalcification at the level of Bowman's layer. Sharplyangulated folds, directed towards the stroma, havebeen described as the basis of a variety of superficial

striate corneal opacities and as a sequelae of retinaldetachment, trauma, fistula, and atrophy or phthisisof the globe (Schirmer, I896; Parsons, 1904; Caspar,I9I6; Fuchs, I9I8; Reis, I92I).Although the mosaic degeneration seen in our case

may be regarded at variance with the report ofMuller (I949), the dimensions and general mor-phology of the pattern are similar to those describedby other authors. The dimensions are of the sameorder as those of the normal corneal mosaic (Bron,I968; Bron and Tripathi, I969, I970). This is ofparticular significance in view of the relationshipwe have postulated between the anterior cornealmosaic and the anterior mosaic degeneration. It canbe shown experimentally and clinically that relaxa-tion of tension in the cornea, such as that producedby buckling the cornea backwards or lowering oculartension, induces a ridge pattern at the surface ofthe cornea which corresponds to the anterior cornealmosaic. These ridges are thought to result from thearrangement of collagen bundles near the surfaceof the cornea (Bron and Tripathi, I970). The inter-lacing of collagen fibrils and adjacent lamellae ofnormal stroma is minimal in many vertebrates

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Secondary anterior crocodile shagreen of Vogt 6I

aFIG. 2a Survey photomicrograph of the cornea in a histological section passing through the region of mosaic degeneration.The corneal stroma is thin, and Bowman's layer thrown into folds, is irregularly encrusted with calcareous deposits. x 75

b<sp. , , . ,C! E ' 4 , j , ; ; ,, B ,,, ..

S<i >iC/ y S b W- m;-I;.....4t &k.S>;'kB 'gS S

FIG. 2b Higher magnification of anterior cornea, showing pronounced ridges in Bowman's layer (arrows) projecting intothe epithelium. The latter has accommodated itself over these undulations and hence there is only minor surface irregularity.The ridges show a variable encrustation with a calcareous granular deposit. x 475

(Virchow, I 9 I O; Payrau, Pouliquen, Faure, andOffret, I967). In man, however, the anterior thirdof the stroma shows pronounced branching and inter-weaving of lamellae and many of these are directedtowards Bowman's layer from the deeper levels(Tripathi, I974a) (Fig. 3). At normal intraocularpressure, Bowman's zone is under tension and viewedfrom the anterior surface appears smooth. By releas-ing the tension, however, a reproducible polygonalridged mosaic pattern becomes manifest. The struc-tural basis for this pattern probably lies in the par-ticular arrangement of the prominent collagenlamellae that continue obliquely from the deeperlayers of the anterior stroma into Bowman's zone. Theterminations of such fascicles expand as they mergeinto Bowman's layer. It would seem, therefore, that

the general statement that individual collagen fibrilswithin the stromal lamellae pass from limbus tolimbuswithoutinterruption (Tripathi, 1972, 1974a,b)cannot apply universally in the anterior stroma.

In the posterior stroma, where the lamellae havea more parallel arrangement, such a possibilitydistinctly exists. In the case described, the whitebranching mosaic opacity is partly explained by theincreased density of the calcium deposits at the apicesof the folds in Bowman's layer and partly by thefact that these folds are viewed 'end-on' duringbiomicroscopy.A mechanism for the production of the mosaic

degeneration in the present case may therefore beproposed as follows. The eye was initially blindedas a result of infection and later became phthisical.

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62 British Journal of Ophthalmology

FIG. 3 Transverse section of normal anterior cornea seen in semipolarized light, showing marked irregularity, variablethickness, and criss-crossing of corneal lamellae. Arrows denote the anterior termination of some lamellae in Bowman's layer,while a progressively horizontal course is taken by the lamellae (asterisk) in the deeper stroma. Adult human eye. Semi-thinAraldite section. x 5oo

Hypotony resulted in a relaxation of tension at thesurface of the cornea so that the ridge pattern wasinduced permanently. Calcification of Bowman'slayer probably followed later, this being not anuncommon secondary event in a phthisical eye.

SummaryThe clinicopathological features and pathogenesis ofsecondary mosaic degeneration ofthe cornea (anteriorcrocodile shagreen of Vogt) are described. Thestructural basis for the normal anterior cornealmosaic pattern seems to lie in the particular arrange-ment of many prominent collagen lamellae of theanterior stroma that take an oblique course to gaininsertion into Bowman's layer. Since, at normal

intraocular pressure, Bowman's layer is under tension,when viewed from the anterior surface the corneaappears smooth. By releasing the tension, however,a reproducible polygonal ridge pattern becomesmanifest. It is suggested that a prolonged phthisicalstate of the eye is one condition wherein the mosaicpattern may become permanent and that, as asecondary event, this is followed by irregular calcifi-cation of Bowman's layer which particularly involvesthe ridges projecting into the epithelium.

Biomicroscopically these ridges corresponded to thebranching reticular arrangement of the mosaicopacities.

Our thanks are due to Professor Norman Ashton, F.R.S.,for his encouragement, and Miss Augusta de Wit forsecretarial assistance.

ReferencesBOLES-CARENINI, B. B. (I96I) Brit. J. Ophthal., 45, 64BRON, A. J. (I968) Ibid., 52, 659

and TRIPATHI, R. C. (I969) Ibid., 53, 760-- (I970) Brit. J. physiol. Optics, 25, 8

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Secondary-anterior crocodile shagreen of Vogt 63

CASPAR, L. (I 9 I 6) Klin. Mbl. Augenheilk., 57, 385COLLIER, M. (I962) Arch. Ophtal. (Paris), 22, 799FRANCESCHETTI, A., and FORNI, S. (1950) "Acta XVI Int. Congr. Ophthal. London," vol. I, p. I93. B.M.A.London

FUCHS, E. (1918) v. Graefes Arch. Ophthal., 96, 315KOPSA, M., and MARUgIC, K. (1958) Ophthalmologica (Basel), 136, 83.MALBRAN, E., D'ALESSANDRO, C., and VALENZUELA, J. (I965) Ibid., 149, I6I

MORO, F., and AMIDEI, B. (1953) G. ital. Oftal., 6, 444MULLER, P. (1949) Ann. Oculist. (Paris), 182, 122PARSONS, J. (1904) "Pathology of the Eye", vol. I, p. I82. Hodder and Stoughton, LondonPAYRAU, P., POULIQUEN, Y., FAURE, J. P., and OFFRET, G. (I967) "La transparence de la cornee. Les mecanismes

de ses alterations". Masson, ParisREIS, W. (I92 I) v. Graefes Arch. Ophthal., 105, 6I 7SCHIRMER, O. (i 896) Ibid., 42 (3), ITRIPATHI, R. C. (1972) "Ultrastructure of the Normal Cornea", Chap. 3, in "Comeal Grafting", ed. T. A.

Casey, p. 38. Butterworths, London(1974a) Trans. ophthal. Soc. U.K., 94, 662(I974b) "Applied Physiology and Anatomy: Tears, Conjunctiva, Cornea and Ocular Adnexa",

Chap. 3 in "Contact Lens Practice", ed. M. Ruben. Bailli&e, Tindall, London (In press)VALERIO, M. (I939) Boll. Oculist., i8, 659

(1942) Arch. Ottal., 49, I, 76VIRCHOW, H. (I9IO) "Graefe-Saemisch Handbuch der gesammten Augenheilkunde", 2nd ed., vol. I. Engel-mann, Leipzig

VOGT, A. (I930) "Lehrbuch und Atlas der Spaltlampenmikroskopie", 2nd. ed., vol. I, p. II4. Springer,Berlin

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