Detachment of ciliary body—anatomicaland physical considerations

Robert A. Moses

The scleral attachments of the ciliary body and choroid were found to be densest from theequator to the posterior pole, less dense at the ora serrata, and practically nonexistent underthe ciliary body and between the ora and equator. The elasticity of the choroid is such thatin the excised human eye about 2 mm. Hg pressure is necessary to distend the uvea againstthe sclera. The tensile strength of the choroid was found to be greater than 5 Gin. per centi-meter. It was concluded that although the interciliary zomdes are under stress in vivo theelastic behavior of the ciliary body could not be entirely attributed to these zomdes. It issuggested that, since pressure in the suprachoroidal space is lower than intraocular pressuredue to the elasticity of ciliary body and choroid, in the presence of ocular hypotony thesuprachoroidal pressure may fall below atmospheric pressure, encouraging transudation intothe space. The distribution of the transudate is explained by the distribution of the supra-choroidal lamellae.

Separation of the ciliary body and cho-roid from the sclera is a common sequelto severe ocular hypotony. Detachment ofthe choroid can be readily appreciatedophthalmoscopically, but separation of theciliary body was recognized only in his-tological sections until Chandler and Mau-menee1 pointed to the fact that as a rule,in hypotonic eyes fluid is found anywhereover the ciliary body.

The present paper deals with some ofthe anatomical and physical features of

From the Department of Ophthalmology and theOscar Johnson Institute, Washington UniversitySchool of Medicine, St. Louis, Mo.

This investigation was supported in part by agrant to the Washington University School ofMedicine by the Alfred P. Sloan Foundation,Inc. The grant was made upon recommendationof the Council for Research in Glaucoma andAllied Diseases. Neither the Foundation northe Council assumes any responsibility for thepublished findings in this study.

the choroid and ciliary body which pre-dispose to their separation from the sclera.Eye Bank eyes no more than 72 hourspost mortem were used.

1. In the three eyes studied, the attach-ments of the uvea to the sclera by supra-choroidal lamellae were found to be veryscant in the region of the ciliary body,somewhat more dense at the ora serrata,apparently absent from the ora to just pos-terior to the equator, and increasinglydense from there to the optic nerve. Therelative distribution and predominantcourse of the lamellae are shown schemat-ically in Fig, 1. These findings are similarto those of Salzmann.2n

2. The gross elasticity of the choroid2l)

was confirmed in three eyes. In any sectionof the posterior segment the choroid re-tracted, exposing a rim of sclera. If thechoroid was stretched out, it retractedagain when released. The fact that thechoroid retracts implies that even in thedead eye it is under tension.

935

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936 Moses Investigative OphthalmologyOctober 1965

Fig. 1. Schematic cross section of eye. The uveais separated from the sclera to show the distribu-tion of supraciliary and suprachoroidal lamellae.

A definite tendency of the cut edge ofsclera to roll inward was noted. This waspartially relieved by breaking the supra-choroidal lamellae.

3. The tensile strength and elasticity ofthe choroid were measured.

A. A strip of the ocular coats was cutfrom anterior to posterior pole. The por-tion of sclera posterior to the equator wascut away. A suture was sewed into the cor-nea and the cut end of the choroid wasplaced between the jaws of a fixed, smallclothespin-like plastic clamp. The cornealsuture was attached to a spring balance(Fig. 2). As the spring balance was raisedor lowered change of length of the cho-roidal strip was noted with the aid of amicroscope on a micrometer stand. Mea-

Fig. 2. Scheme of arrangement for determiningstress-strain relations of choroid. The microscopeis mounted on a stand with a micrometer verticaladjustment.

surements were made from the clamp tothe posterior tip of a ciliary process.

When overstressed the strips tore, usu-ally at the ora serrata. Seven eyes wereused in this investigation.

B. Equatorial strips of choroid weresimilarly measured using a second, mov-able clamp to hold the upper end of thestrip. Strips from five eyes were measured.

The results are summarized in TableI. Although the stress-strain curves arenot strictly linear, values for complianceand the related Young's modulus werecomputed from measurements in physio-logical range of tension.

4. The lamellae running from the post-equatorial choroid to the sclera also dem-onstrated elasticity and an aggregate ten-sile strength of the same order as thechoroid. A strip of ocular coats was cutin an anteroposterior direction. The corneawas clamped while a suture connectedsclera to spring balance. The sclera wasthen divided anterior to the equator (Fig.3). The breaking force of this preparation

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Detachment of ciliary body 937

Fig. 3. Method of measuring strength of supra-choroiclal lamellae. The sclera has been dividednear the equator.

in two eyes was 5.5 and 7.0 Gm. per cen-timeter strip width. Tearing occurred atthe ora serrata.

5. The effect of temperature on the elas-tic properties of the choroid was testedin one meridional preparation (eye No.6, second strip in Table I). Comparingthe more meaningful second stretching itwas found that at25° C, compliance was .20 mm./Gm. orM = 2.5 x 10" Gm./cm.2

33° C, compliance was .13 mm./Gm. orM = 3.7 x 104 Gm./cm.2

6. Separation of the ciliary body in vitrowas demonstrated in three eyes. The eyewas first injected with saline through aneedle placed in the optic nerve in orderto restore the normal turgor. The eye wasthen embedded in four per cent agar,frozen, and sawed in two in a meridionalplane. The choroid and ciliary body werefound to be closely applied to the sclera.The lens was removed from one half of theeye and both halves of the agar-embeddedeye were allowed to thaw. In both halvesthe uvea separated in a characteristicfashion, remaining attached at the sclera]spur, or a millimeter or two behind it ifanterior ciliary vessels perforated at that

Table I

Eye Age

Dayspost

mortem

Compliance(mm./Gm.)"

Initial Second

Youngs modulus(Gm./cm.s)f

Initial Second

Breakingstrain

(Gm./cm.)

Meridional strips1 732 853 604 615 756 77

Second strip7 27

Equatorial strips3 604 615 756 777 27Soft rubber

.11

.15

.22

.17

.10

.17

.27

.20

.35

.39

.44

.35

.42

.26

.18

.07

.20

.12

.37

.42

5.03.32.22.94.62.91.92.5

1.41.31.11.41.21.9

X

X

XX

X

X

X

X

X

X

X

X

X

X

10+10+10+10+10+10+10+10+

10+10+10+10+10+10+

2.7

6.9

2.54.2

1.3

1.2

X

X

X

X

X

X

10+

10+

10+10+

10+

10+

8<

6 <6<

10 <4<5 <5<

9 <9<7<6<6<

Cb<

CbCb: b: b <: b <Cb

: b <: b <Cb<: b <Cb

: 10

; 5; e

: io: io: 8; 7

"Calculated for choroidal strip 1 cm. wide and 1 cm. long.... , . . , , force X lengthtYoung s modulus, M = —width X thickness X elongation

The thickness of the choroid is assumed to be .002 cm.

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938 Moses In oest.igalioe OphthalmologyOctober 1965

point, and just posterior to the equator,but forming a chord between these twopoints as seen in the cross section (Fig.4). That the separation progressed entirelyaround the half eye forming a truncatedcone could be shown by pressing any-where on the pars plana with a bluntinstrument and observing the dimplingproduced and the appearance of fluid andbubbles in the separated area of the sec-tion. When the instrument was removedthe anterior uvea again retracted from thesclera. The findings were the same in allthree eyes.

7. The intraocular pressure necessary todistend the ciliary body against the sclerawas found to be about 3 cm. FLO (2mm. Hg). This result was obtained bycutting a scleral window over the ciliarybody in a cannulated eye. When the intra-ocular pressure was reduced below 3 cm.H2O a drop of water in the window wasseen to become concave as it sucked intothe supraciliary space. The drop reap-peared in its convex form when the pres-sure was raised. Two eyes were investi-gated in this manner with similar resultsin both eyes.

8. An attempt was made to assess thecontribution of the interciliary zonules(Fig. 5) to the elasticity of the ciliarybody.

It was found, however, that even in rel-atively fresh eyes the ciliary epitheliumhad autolyzed so that the internal limit-ing membrane and zonules pulled awayrather readily. The detached membraneshortened and rolled inward, indicatingits elasticity and that of the interciliaryzonules.

In two fresh monkey anterior segmentsthe ciliary body detached very markedly.When the lens was removed by cuttingthe suspensory zonules the detachmentpersisted (Fig. 6). Chymotrypsin did notrelieve the separation, although the inter-ciliary zonules were dissolved, so it isinferred that in the monkey other ciliarybody structures are sufficiently under ten-sion to maintain ciliary separation.

Fig. 4. A distended eye is embedded in agar,frozen, and bisected. When allowed to thaw theciliary body and anterior choroid separate fromthe sclera.

Fig. 5. Meridional section of the pars plana ofthe ciliary body showing interciliary zonules, bothends of which attach to the ciliary body. (Theposterior tip of a ciliary process is to the left.)

Comment

The choroid, like many other body tis-sues, appears to be an elastomer.* Thatis, it does not obey Hooke's lawf pre-cisely, but repeated stress-strain determi-nations on the same specimen show clos-

° "Rubber-like substances . . . (which) display some de-gree of plastic flow and of relaxation effects."3 FromGlasser, Otto, editor: Medical Physics, Chicago, Copyright© 1950, Year Book Medical Publishers, Inc., p. 189.Used by permission of Year Book Medical Publishers.

deformation is proportioned to the deforming force.

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Detachment of ciliary body 939

1.2

Fig. 6. Meridional section of anterior segment offresh monkey eye showing marked separation ofthe ciliary body.

ing hysteresis loops* (Fig. 7). Young'smodulus f was calculated only for roughcomparison of results and is similar tothat of soft rubber. Like other elastomerschoroid shows a decreased compliancewith rise of temperature.3

It has been shown that the dead cho-roid displays considerable tensile strength,more than 5 Grn. per centimeter. It wasalso found that about 3 cm. H2O wasnecessary to distend the uvea against thesclera. van Alphen'1 measured the pressurein the suprachoroidaJ space by direct can-nulation in living cat eyes and found val-ues very similar to the present ones. Sincein a sphere tension = Vz pressure x radius,the tension in the distended choroid is

I .4

Eye*7Meridional strip6mm wide, 16mm long

°"A retardation of the effect, when the forces acting upona body are changed, as if from viscosity or internal fric-tion," Webster's New Collegiate Dictionary, G. & C.Meriinm Co., 1959.fThe force per unit area divided by the extension perunit length.

GRAMS

Fig. 7. Stress-strain determinations on a meridi-onal strip of choroid. The relation between stressand elongation of the strip is not linear. Repeatedcycles of stress and relaxation show closing hys-teresis loops.

V2 x 3 Gm./cm.- x 1.1 cm. = 1.6 Gm./cm.The ciliary muscle may contract 5.0 - 1.6= 3.4 Gm./cm. in accommodation beforedamage to the choroid might be expected.

If the low compliance of 0.1 mm. pergram, is assumed, it is readily calculatedthat the ora serrata may be moved forward0.7 mm. before the minimal breaking strainof 5 Gm. per centimeter is reached. It ishighly doubtful that the ora moves thismuch even in an extreme accommodation.It seems clear then that the choroid isstrong enough to serve as an attachmentof the ciliary muscle, and is not the ex-tremely delicate structure Henderson"5 sup-posed.

The elasticity of the ciliary body andchoroid suggests that when the intraocularpressure falls to atmospheric, as during acataract extraction, the pressure in thesuprachoroidal potential space falls to asmuch as 2 mm. Hg below atmospheric.It is not surprising that transudate appearsin the space in many such cases. Hudson"also pointed to the fact that the nearlyspherical sclera tends to maintain itsdomed shape when intraocular pressure isdropped to atmospheric. Meller7 and Ha-

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940 Moses Inocstigatioe OphthalmologyOctober 1965

gens pointed to the loss of elasticity ofthe sclera with age as a reason why cho-roidal separation is often seen with hy-potony in older adults but not often inthe young. Thus the thinness and elastic-ity of the rabbit's sclera may account forthe lack of choroidal separation on fistuli-zation of the anterior chamber found byCapper and Leopold.9 That the choroidaldetachment so formed tends to be limitedposteriorly just behind the equator is de-pendent upon the fairly firm epichoroidalattachment to the sclera from this pointto the optic nerve. The vortex veins tiethe choroid to the sclera in the equatorialregion, and combined detachments tendto occur in the vertical and horizontalplanes between the vortices.

The strength of the epichoroidal lamel-lae was quite unsuspected. Even thougheach lamella is very fragile, when thelamellae are stressed in aggregate and inthe direction imposed in life they arecapable of withstanding considerable ten-sion. The vortex veins, short posterior cil-iary arteries, and nerves passing betweensclera and choroid undoubtedly augmentthe epichoroidal lamellae in holding theposterior choroid to the sclera. The virtualabsence of attachment of the ciliary bodyto the sclera except at the spur and atpoints of perforation of anterior ciliaryvessels allows transudate (or in the caseof cyclodialysis, aqueous) to become dis-tributed throughout the supraciliary space.

A therapeutic implication of the presentfindings is that treatment of separation ofthe ciliary body and choroid might beaided by cycloplegic drugs since in relaxa-tion of the ciliary muscle tension on theuvea should be minimal.10

Separation of the choroid and ciliarybody seen in histological sections may bedeclared to have existed in vivo only ifproteinaceous material can be demon-strated between uvea and sclera. However,the artifactual detachment commonly seenin sections is very likely the result of ten-sion already existing in the uvea and not

the result of differential shrinkage causedby the fixative.

Combined detachment depends essen-tially on tension existing within the uvea,and not upon the pull of the suspensoryligament of the lens as was shown by pro-duction of detachment in the absence ofthe lens (sections 3, 4), although lenszonule traction probably augments theeffect. The ciliary structures are also un-der tension, and, when intraocular pres-sure is reduced, tend to cause the ciliarybody to curl inward.

In the foregoing, no reference was madeto the fact that in the excised eye thechoroid is not distended with blood andthat the elastic relations might be alteredby such distention. This is undoubtedlytrue. From geometrical considerations itis seen that in the blood-distended choroidthe inner layer (Bruch's membrane) willbe under less tension. The tissue betweenthe vessels, however, may be under greatertension when the choroid is filled withblood, since the collapsed vessels can bedrawn out to oblated circles (in cross sec-tion), the diameters of which are con-siderably longer than the diameters of ves-sels rounded by blood filling.

REFERENCES1. Chandler, P. A., and Maumenee, A. E.: A

major cause of hypotony, Am. J. Ophth. 52:609, 1961.

2a. Salzmann, M.: The anatomy and histologyof the human eyeball, translated by E. V. K.Brown, Chicago, 1912, University of ChicagoPress, p. 48.

2b. Salzmann, M.: The anatomy and histologyof the human eyeball, translated by E. V. K.Brown, Chicago, 1912, University of ChicagoPress, p. 52.

3. King, A. L., and Lawton, R. W.: In Glasser,O., editor, Medical physics, Vol. 2, Chicago,1950, Year Book Publishers, Inc., p. 306.

4. van Alphen, G. W. H. M.: On emmetropiaand ametropia, Ophthalmologica 142::(suppl.) 49, 1961.

5. Henderson, T.: The anatomy and physiologyof accommodation in mammalia, Tr. Ophth.Soc. U. Kingdom 46: 280, 1926.

6. Hudson, A. C : Serous detachment of thechoroid and ciliary body as an accompani-

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volume 4 Detachment of ciliary bodu 941Number 5 J J

ment of perforating lesions of the eyeball, oidealablosung und ihre Pathogenese, Klin.Roy. London Ophth. Hosp. Rep. 19: 301, Monatsbl. f. Augenh. 66: 161, 1921.1914. 9. Capper, S. A., and Leopold, L. H.: Mech-

7. Meller, J.: t)ber postoperative und spontane anism of choroidal detachment, Arch. Ophth.Chorioidealabhebung, Arch. Ophth. 80: 170, 55: 101, 1956.1912. 10. Chandler, P. A., and Grant, W. M.: Mydri-

8. Hagen, S.: Die serose postoperative Chori- atic cycloplegic treatment in malignant glau-coma, Arch. Ophth. 68: 353, 1962.

Erratum

In the article, "Changes associated with tlie appearance of mature sugar cataracts," by Drs.Patterson and Bunting, in the April issue of this JOURNAL, page 167, Figs. 1' and 2 are re-versed, so that the legend for Fig. 1 applies to Fig. 2 and vice versa. The footnote of Table Ishould have read as follows: 'Corrected hydration index equals (wet weight in milligramsminus [milligrams of dulcitol per lens multiplied by 16.5]) divided by (the diy weight of thelens in milligrams minus milligrams of dulcitol per lens).

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