BritishJournal ofOphthalmology 1994; 78: 99-102

Shape of the neuroretinal rim and position of thecentral retinal vessels in glaucoma

Jost B Jonas, Martfn C Fernandez

AbstractGlaucomatous neuroretinal rim loss can occurin a sequence of sectors with the temporalinferior disc sector as the first and the nasalsuperior disc sector as the last to be affected.This study evaluated whether the position ofthe central retinal vessel trunk is correlatedwith this pattern of glaucomatous rim loss.Morphometrically stereo colour optic discphotographs of 157 glaucomatous eyes and 67normal eyes were checked. In the normal andglaucomatous eyes, the central retinal vesseltrunk was located eccentrically in the uppernasal quadrant of the optic disc. Taking intoaccount the vertically oval disc shape, thedistance to the central vessel trunk was largestfor the temporal inferior disc region and short-est for the nasal superior disc area. An abnor-mal form ofthe glaucomatous neuroretinal rimwas found in eyes with an atypical location ofthe retinal vessel trunk. Also in these glauco-matous eyes, the rim loss was usually most andleast marked in that sector with the longest andshortest distance, respectively, to the centralretinal vessel trunk. One could infer that thesequence of rim loss in glaucoma is dependentupon the distance of the region to the centralretinal vessel trunk; the further away the regionfrom the retinal vessel trunk, the more likely itis to be affected by rim loss. This suggests thatthe distance from the central retinal vessels isone factor among others that is correlated withthe regional vulnerability of the neuroretinalrim to the glaucomatous process.(BrJ Ophthalmol 1994; 78: 99-102)

Department ofOphthalmology and EyeHospital, UniversityErlangen-Ninberg,GermanyJ B JonasM C FernindezCorrespondence to:Dr J Jonas, University EyeHospital, Schwabachanlage 6,D-91054 Erlangen, Germany.Accepted for publication17 August 1993

Glaucoma is associated with a diminution ofopticnerve fibres leading to a decrease of neuroretinalrim area.'2 This rim loss occurs in all sectors ofthe optic disc with regional preferences depend-ing on the stage of the disease. In eyes withmodest glaucomatous damage, rim loss is foundpredominantly at the inferotemporal andsuperotemporal disc regions.' In eyes withmoderately advanced glaucomatous atrophy, thetemporal horizontal disc region is the locationwith relatively the most marked rim loss. In veryadvanced glaucoma, the rim remnants are

located mainly in the nasal disc sector, with a

larger rim portion in the upper nasal region thanin the lower nasal region.6 This sequence of discsectors (inferotemporal - superotemporal -

temporal horizontal - nasal inferior - nasalsuperior) correlates with the progression ofvisualfield defects with early perimetric changes in thenasal upper quadrant of the visual field and a lastisland of vision in the temporal inferior part ofthe visual field in eyes with almost absoluteglaucoma. The present study was performed to

evaluate whether the position of the centralretinal vessel trunk is correlated with this patternofglaucomatous neuroretinal rim loss.

Materials and methodsA total of 157 glaucomatous eyes (78 right eyes,79 left eyes) of 87 glaucoma patients (35 men, 52women; mean age: 65-1 (SD 10-9) years; range:27-83 years, mean refractive error: +0 02 (2 06)dioptres; range: -5 6 to +6 5 dioptres), and 78normal eyes (40 right eyes, 38 left eyes) of 48subjects (27 men, 21 women, with a mean age of51-0 (17-0) years; range: 8-78 years; and a meanrefractive error of +0 39 (1-44) dioptres; range:-2-25 to 4-0 dioptres) were included in thestudy.These were randomly selected eyes out of a set

of normal and glaucomatous eyes in which theexit of the retinal vessel trunk on the laminacribrosa surface was clearly visible. Eyes with amyopic refractive error exceeding -8 dioptreswere excluded because of a different optic discmorphology.7 Additionally, 53 glaucomatouseyes with tilted discs were evaluated. They weredefined by a horizontally oval optic disc shapewith the horizontal disc diameter being at least10% longer than the vertical one. The ratio of theminimal disc diameter to the maximal discdiameter was at maximum 0 90.

Criteria for the diagnosis of glaucoma were anelevated intraocular pressure to readings ofmorethan 21 mm Hg, glaucomatous changes of theoptic nerve head such as an abnormally smallneuroretinal rim area in relation to the optic discsize, larger vertical than horizontal cup to discratios, splinter-shaped optic disc haemorrhages,reduced visibility of the retinal nerve fibrebundles including localised defects, and glauco-matous visual field defects.For all eyes, 15 degree colour stereo optic disc

photographs had been taken using a telecentricZeiss fundus camera equipped with an Allenstereo separator. The disc transparencies wereprojected in a scale of 1 to 15. The outlines of theoptic disc and optic cup were plotted on paperand morphometrically analysed. We measuredarea and horizontal, vertical, minimal, and maxi-mal diameters of the disc and cup, and width ofthe neuroretinal rim every 30 degrees. The exitposition of the central retinal artery and vein onthe lamina cribrosa surface was measured as thedistance between the centre of the vessel and thevertical optic disc axis and the horizontal opticdisc axis. The optic cup was stereoscopicallydefined on the basis of contour and not of pallor.The border of the optic disc was identical to theinner side of the peripapillary scleral ring. Thelatter was a thin white band encircling the opticdisc. To obtain values in absolute size units (mm

99

on June 16, 2020 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.78.2.99 on 1 February 1994. D

ownloaded from

Jonas, Ferndndez

or mm2) the ocular and photographic magnifica-tion was corrected according to Littmann'smethod taking into account the ametropia andthe anterior corneal curvature.8 The method hasalready been described in detail.29'0 The photo-graphs were evaluated in a masked fashionwithout knowledge of the clinical diagnosis andthe visual field data.For interindividual comparison, only one ran-

domly selected eye per patient and subject wastaken for statistical analysis. To examine thesignificance of differences, Wilcoxon and Mann-Whitney tests were applied.

Results

POSITION OF THE CENTRAL RETINAL VESSELTRUNKIn all normal and glaucomatous eyes, the retinalartery was located nasal to the retinal vein. In thenormal eyes, the exits of the retinal artery andvein were located 021 (013) mm and 0 00(0- 12) mm, respectively, nasal to the verticaloptic disc axis. For the glaucomatous eyes,similar values were obtained (artery: 024 (020)mm; vein: 005 (019) mm nasal to vertical discaxis) with no significant difference (p=0 39(artery); p=0 18 (vein)) between the normal andglaucomatous eyes. Concerning the position invertical direction, both the artery and vein exitswere located on an average 0-02 (O -11) mmsuperior to the horizontal optic disc axis. Theamount ofthe superior and nasal displacement ofthe central retinal vessel trunk was positively andsignificantly (p<001) correlated with the opticdisc size. The larger the optic disc, the morepronounced was the displacement. The shape ofthe optic disc was slightly vertically oval with thevertical disc diameter (1-89 (025) mm) beingabout 6% longer than the horizontal one (1-78(O- 19) mm). Taking into account this disc formand comaparing the different disc sectors witheach other, the temporal inferior disc border isthe location with the longest distance to thecentral retinal vessel trunk. The nasal superiordisc border shows the shortest distance to thecentral vessel trunk.With respect to an abnormal position of the

retinal vessels we compared glaucomatous eyes(n=53) with the retinal vessel trunk located inthe superior disc half and eyes with the retinalvessel exit positioned in the inferior disc half(n= 35). The neuroretinal rim at the superior discmargin was significantly (p<005) wider andlarger in the glaucomatous eyes with the retinalvessel trunk located in the superior disc regionthan in the eyes with the retinal vessel exitpositioned in the inferior disc area (rim width at12 o'clock: 0-22 (O@12) mm versus 0-17 (010)mm; rim area in the temporal superior discsector: 0-28 (0 14) mm2 versus 0-22 (0-12) mm2).Concerning an unusual location of the retinalvessel trunk in the horizontal direction, theneuroretinal rim in the temporal horizontal discregion was wider in the eyes with the retinalvessel trunk located in the temporal disc half(n=22) than in the eyes with the retinal vesselexit positioned in the nasal disc half(n=65) (O 17(008) mm versus 0-14 (0 11) mm). The rim in

the nasal disc sector was wider in the glau-comatous eyes with the retinal vessel trunk in thenasal disc half (n=65) than in the eyes with theretinal vessels exiting in the temporal disc half(n=22) (024 (011) mm versus 021 (009)mm). Total neuroretinal rim area did not differsignificantly between the glaucoma subgroupswith varying vessel location.With respect to an abnormal optic disc shape,

53 glaucomatous eyes with tilted discs wereevaluated. Due to the selection, they were char-acterised by a horizontally oval optic disc shapeand an exit of the retinal vessels at the superiordisc border. In these eyes, the neuroretinal rimwas significantly (p<0 01) smaller in the inferiordisc region than in the superior one (width: 023(021) mm versus 029 (021) mm; rim area inthe temporal inferior disc sector: 024 (015)mm2 versus rim area in the temporal superior discsector: 029 (0'13) mm2). In the eyes with tilteddiscs and far advanced glaucoma, the rim rem-nants were significantly (p<001) larger at thesuperior disc border than in the nasal, inferior,and temporal disc regions.For the normal eyes, the configuration and

width of the neuroretinal rim were statisticallyindependent of the location of the retinal vesselexit. The optic disc size was not significantlydifferent between the normal group (2-73 (0 59)mm2) and the glaucoma group (2 77 (0 78) mM2).These values are larger than those reported forunselected normal eyes (2'69 (0 70) mm2; notsignificant; Wilcoxon and Mann-Whitney test)'0and glaucomatous eyes (2-57 (0 60) mm2;p<O-01).'8

DiscussionVariables that may be associated with the patternof glaucomatous rim loss' are: (1) the physio-logical configuration of the rim being broader atthe inferior and superior disc poles than at thenasal and temporal poles'0; (2) the morphology ofthe inner surface of the lamina cribrosa with thelarger pores and the higher ratio of pore tointerpore connective tissue area in the inferiorand superior regions compared with the temporaland nasal regions"'3; a high ratio of pore area tototal area is considered to predispose to glauco-matous nerve fibre loss; (3) the glaucomatousbowing of the lamina cribrosa to the outsidemainly in the inferior and superior disc regions asshown on scanning electron microscope photo-graphs of glaucomatous eyes'4; and (4) theregional distribution of thin and thick retinalnerve fibres with thin nerve fibres coming fromthe foveola, passing mainly through the temporalaspect of the optic disc and being less glaucomasusceptible than thick nerve fibres which origin-ate predominantly in the fundus periphery, leadto the inferior, superior, and nasal disc regions5 16and are more glaucoma sensitive than thin retinalganglion cell axons.'7 The latter parameter mayexplain why glaucomatous rim loss occurs later inthe temporal horizontal disc sector with predom-inantly thin nerve fibres than in the temporalinferior or temperal superior disc sectors contain-ing thin and thick axons. It is contradictory to thefact that in far advanced glaucoma rim remnantsare usually located in the nasal disc sector. There,

100

on June 16, 2020 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.78.2.99 on 1 February 1994. D

ownloaded from

Shape ofthe'neuroretinal rim and position of the central retinal vessels in glaucoma

preferentially thick retinal ganglion cell axonsleave the eye. 15 16As an additional parameter for the pattern of

glaucomatous rim loss, the distance from thecentral retinal vessel trunk in the lamina cribrosamay be considered. In both the normal andglaucomatous eyes of the present study, theretinal vessel trunk was slightly decentred intothe nasal upper disc quadrant. Similar resultshave been obtained in a histomorphometricstudy of the lamina cribrosa surface. " In thelatter investigation, the exits of the retinal arteryand vein were located 0-15 (O 09) mm and 0 07(0- 14) mm, respectively, nasal to the verticaloptic disc axis and 0-02 (0-11) mm and 005(O 09) mm, respectively, superior to the horizon-tal optic disc axis. Taking into account thevertically oval optic disc shape,'" one may inferthat the distance between the retinal vessels inthe lamina cribrosa and the neuroretinal rim maybe associated with the pattern of glaucomatousrim loss. The sector distant to the retinal vesseltrunk is the temporal inferior disc region fol-lowed by the superior temporal and temporalhorizontal disc regions. The nasal disc sector isthe one closest to the retinal vessels with the nasalupper portion located closer to the retinal vesseltrunk than the nasal inferior portion. In the samesequence, the glaucomatous rim loss has beenreported to take place: temporal inferior -

temporal superior and temporal horizontal -

nasal inferior - nasal superior.' Corres-pondingly, glaucomatous neuroretinal rimnotches do not occur on an average at the inferiorand superior disc poles but at about 13 degreestemporal to the vertical optic disc axis.'8 These

Figure I Optic discphotographs ofglaucomatous right eyes.Atypical positions of thecentral retinal vessel trunkcorrelated with an abnormalshape of the glaucomatousneuroretinal rim.

(A) Atypical rim notching in the nasal superior disc sector,retinal vessel trunk originating in the temporal inferior discsector.

(B) Rim notching in the superior disc region, retinal vesseltrunk located in the inferior disc region. Note: Correspondingto the rim loss, the parapapillary atrophy is larger in thesuperior region than in the inferior region.

locations are more distant to the retinal vesseltrunk than the vertical disc poles at the 6 o'clockand 12 o'clock position.For strengthening the hypothesis that the local

glaucoma susceptibility is correlated with thedistance to the retinal vessel trunk, the followingfacts can be listed:

(1) In glaucomatous eyes with an unusuallocation ofthe retinal vessel trunk or an abnormaloptic disc shape, the rim had an unusual form.Conversely, in eyes with an unusual glauco-matous rim configuration, the retinal vesseltrunk was abnormally positioned (Figs lA-C).Also in these glaucomatous eyes, the rim loss wasusually most and least marked in that sector withthe longest and shortest distance to the centralretinal vessel trunk, respectively.

(2) The location of early glaucomatous visualfield defects in the upper nasal or lower nasal fieldquadrants close to the horizontal line'9-22 indicatesa ganglion cell loss in the region of the temporalfundus raphe. The axons of these ganglion cellslie in the deepest part of the retinal nerve fibrelayer.2324 They are closest to the optic disc border.Within the optic disc, they are more distant to thecentral retinal vessel trunk than ganglion cellaxons originating in the vicinity of the optic nervehead. These are located more centrally in theoptic nerve head and are lost in a later stage of thedisease.

Diagnostically, it may indicate that in eyeswith an abnormal position of the central retinalvessels or an unusual optic disc form, earlyglaucomatous rim changes should be looked fornot only in the temporal inferior disc sector butalso in that disc sector that is most distant to thecentral retinal vessel trunk. It may explain whyeyes with open angle glaucoma and a temporalcilioretinal artery retain longer central visual fieldthan open angle glaucomatous eyes without atemporal cilioretinal artery.25

Pathogenetically, one may infer that the retinalvessel trunk could act as a stabilising element. Itcould render more difficult a mechanical distor-tion and backward bowing of the lamina cribrosain glaucoma. This hypothesis is supported byphotographs of a W-shaped lamina cribrosa inglaucomatous eyes. 4 The lamina cribrosa is morecondensed and bowed more to the back in theinferior and superior disc regions than close tothe lamina cribrosa centre where the retinalvessels emerge. If the vessel trunk is decentred

(C) Atypical position ofthe retinal vessel trunk in the inferiordisc region correlating with rim remnants in the same discarea. Note: Corresponding to the rim loss, the parapapillaryatrophy is larger in the superior region than in the inferiorregion.

101

on June 16, 2020 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.78.2.99 on 1 February 1994. D

ownloaded from

Jonas, Fermundez

into the superior half of the optic disc, theinferior disc portion without vessel trunk sup-port is larger than the superior one. Conse-quently, it can be deformed to a greater extentthan the smaller superior disc part. It couldexplain the greater frequency of neuroretinal rimnotches in the inferior temporal disc regioncompared with the superior temporal area.'8As a variation to this mechanical theory, one

could also speculate that in the close vicinity ofthe retinal vessel trunk the vascular supply to theadjacent tissue is better than in the periphery. Avitally important participation ofbranches of thecentral retinal vessels in the nourishment of theoptic nerve fibres in the lamina cribrosa, how-ever, has not yet been demonstrated.26As a factor limiting the scope of the present

study one can mention that the position of thecentral retinal vessel trunk was measured in eyesin which the trunk on the lamina cribrosa surfacewas clearly detectable. This is possible only indiscs showing central cupping. Due to the cor-relation between optic cup and optic discsize' 27 28 it implies that these selected optic discswere on average larger than normal optic nerveheads. In another histomorphometric investiga-tion on the lamina cribrosa surface, however, theretinal vessel trunk was also located in the uppernasal quadrant.'3 That study consisted of eyes ofvarying optic size including also small opticdiscs.

This study is part of a project of the Deutsche Forschungs-gemeinschaft (Klinische Forschergruppe 'Glaukome', DFGNa 55/6-1/Jo).

1 Betz Ph, Camps F, Collignon-Brach J, Lavergne G, WeekersR. Biometric study of the disc cup in open-angle glaucoma.Graefes Arch Clin Exp Ophthalmol 1982; 218: 70-4.

2 Airaksinen PJ, Drance SM, Schulzer M. Neuroretinal rim areain early glaucoma. AmJ Ophthanmo( 1985; 99: 1-4.

3 Kirsch RE, Anderson DR. Clinical recognition of glau-comatous cupping. AmJ Ophthalmol 1973; 75: 442-54.

4 Pederson JE, Anderson DR. The mode of progressive disccupping in ocular hypertension and glaucoma. Arch Oph-thalmol 1980; 98: 490-5.

5 Tuulonen A, Airaksinen PJ. Initial glaucomatous optic diskand retinal nerve fiber layer abnormalities and the mode oftheir progression. AmJ Ophthalmol 1991; 111: 485-90.

6 Jonas JB, Fernandez M, Sturmer J. Pattern of glaucomatousneuroretinal rim loss. Ophthalmology 1993; 99: 63-8.

7 Jonas JB, Gusek GC, Naumann GOH. Optic disc morpho-metry in high myopia. (A clinical study of 51 eyes.) GraefesArch Exp Ophthalmol 1988; 226: 587-90.

8 Littmann H. Zur Bestimmung der wahren grosse einesObjektes auf dem Hintergrund des lebenden Auges. KlinMonatsblAugenheilkd 1982; 180: 286-9.

9 Britton RJ, Drance SM, Schulzer MD, Douglas GR, MawsonDK. The area of the neuroretinal rim of the optic nerve innormal eyes. AmJ Ophthalmol 1987; 103: 497-504.

10 Jonas JB, Gusek GC, Naumann GOH. Optic disc, cup, andneuroretinal rim size, configuration, and correlations innormal eyes. Invest Ophthalmol Vis Sci 1988; 29: 1151-8.

11 Quigley HA, Addicks EM. Regional differences in the struc-ture ofthe lamina cribrosa and their relation to glaucomatousoptic nerve damage. Arch Ophthalmol 1981; 99: 137-43.

12 Radius RL. Regional specificity in anatomy at the laminacribrosa. Arch Ophthalmol 1981; 99: 478-80.

13 Jonas JB, Mardin CY, Schl6tzer-Schrehardt U, NaumannGOH. Histomorphometry of the human lamina cribrosasurface. Invest Ophthalmol Vis Sci 1991; 32: 401-5.

14 Quigley HA, Addicks EM, Green WR, Maumenee AE. Opticnerve damage in human glaucoma. II. The site of injury andsusceptibility to damage. Arch Ophthalmol 1981; 99: 635-49.

15 Sanchez RM, Dunkelberger GR, Quigley HA. The numberand diameter distribution of axons in the monkey opticnerve. Invest Ophihalmol VisSci 1986; 27: 1342-50.

16 Jonas JB, Muller-Bergh JA, Schltzer-Schrehardt UM,Naumann GOH. Histomorphometry of the human opticnerve. Invest Ophihalmol Vis Sci 1990; 31: 736-44.

17 Quigley HA, Sanchez RM, Dunkelberger GR, L'HernaultNL, Baginski TA. Chronic glaucoma selectively damageslarge optic nerve fibres. Invest Ophthalmol Vis Sci 1987; 28:913-20.

18 Jonas JB, Gusek GC, Naumann GOH. Optic disc morpho-metry in chronic primary open-angle glaucoma. I. Morpho-metric intrapapillary characteristics. Graefes Arch Clin ExpOphthalmol 1988; 226: 522-30.

19 Drance SM. The early field defects in glaucoma. InvestOphthalmol 1969; 8: 84-91.

20 Hart WM Jr, Becker B. The onset and evolution of glauco-matous visual field defects. Ophthalmology 1982; 89: 268-79.

21 Gramer E, Gerlach R, Krieglstein GK, Leydhecker W.Topography of early visual field defects in computerizedperimetry. Klin Monatsbl Augenheilkd 1982; 180: 515-23.

22 Caprioli J, Sears M, Miller JM. Patterns of early visual fieldloss in open-angle glaucoma. Am J Ophthalmol 1987; 103:512-7.

23 Radius RL, Anderson DR. The course of axons through theretina and the optic nerve head. Arch Ophthalmol 1979; 97:1154-8.

24 Minckler DS. The organisation of nerve fiber bundles in theprimate optic nerve head. Arch Ophthalmol 1980; 98:1630-6.

25 Lee SS, Schwartz B. Role of the temporal cilioretinal artery inretaining central visual field in open-angle glaucoma.Ophthalmology 1992; 99: 696-9.

26 Lieberman MF, Maumenee EA, Green RW. Histologicstudies of the vasculature of the anterior optic nerve.AmJ Ophthalmol 1976; 82: 405-23.

27 Bengtsson B. The variation and covariation of cup and discdiameters. Acta Ophthalmol 1976; 54: 804-18.

28 Caprioli J, Miller JM. Optic disc rim area is related to disc sizein normal subjects. Arch Ophthalmol 1987, 105: 1683-5.

102

on June 16, 2020 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.78.2.99 on 1 February 1994. D

ownloaded from