Corneal and Retinal Complications after Cataract Extraction The Mechanical Aspect of Endophthalmodonesis

C. D. BINKHORST, MD

Abstract: Removal of the crystalline lens deprives the eye of the stabilizing effect of the lens-zonule barrier. lntracapsular extraction also causes loss of stability inside the vitreous cavity itself (vitreodonesis). The lack of stability inside the aphakic eye is defined as endophthalmodonesis. Oscillations induced by saccadic eye movements cause turbulences in the aqueous humor and in liquid pools present in the vitreous cavity. Therefore, endophthalmodonesis is a continuing trauma to the eye. The hypothesis that corneal and retinal complications of cataract extraction, other than those of surgical origin, are due to the mechanical aspect of endophthalmodonesis is discussed. This hypothesis explains why, after complete removal of the lens-zonule barrier, the intracapsular aphakic eye suffers more from "barrier deprivation" than the extracapsular aphakic eye after incomplete removal of this barrier. [Key words: barrier deprivation, endophthalmodonesis, extracapsular extraction, intracapsular extraction.] Ophthalmology 87:609-617, 1980

Cataract surgery may be the cause of compli­cations, and these complications manifest themselves in the early postoperative period. One example is the occurrence of retinal edema due to postoperative inflammation. Another example is an early corneal edema due to surgi­cal endothelial trauma. A transient corneal edema may also be followed by a late corneal

From the Department of Ophthalmology, Zeeuws­VIaanderen Hospital Group, the Netherlands.

Presented at the Eighty-Fourth Annual Meeting of the American Academy of Ophthalmology, San Francisco, November 5-9, 1979.

Reprint requests to C. D. Binkhorst, MD, Axelsestraat 54, 4537 AI Terneuzen, Netherlands.

breakdown with an interval of varying duration, due to the physiological age-dependent de­crease of endothelial viability. 1

In this article, however, the pathogenesis of late corneal and retinal complications is dis" cussed which apparently has nothing to do with surgery as such, but has to do with the condi­tion of aphakia. Well-known late complications of aphakia are corneal decompensation, edem­atous maculopathy, papilledema, peripheral retinal degeneration, and retinal detachment. Despite these serious conditions, the aphakic eye was always regarded as a healthy eye. Corneal and retinal complications were con­sidered independent of each other. Corneal complications, if not surgically-induced, gen-

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erally were badly understood and their patho­genesis never aroused much interest. Retinal complications, however, for a long time, were the subject of discussions, that are condensed in various theories about their origin. Cystoid macular edema was explained by vitreous trac­tion,2·3 or by inflammation.4

POSTOPERATIVE COMPLICATIONS

With the advent of intraocular lens implanta­tion, there was a re-evaluation of postoperative complications. This was necessary because there was a tendency to ascribe certain compli­cations to the lens implant proper instead of to the cataract surgery. N ordlohne found that the concurrence of cystoid macular edema and cor­neal decompensation was not a mere coinci­derice.5 Nordlohne's corneoretinal syndrome became the subject of a further search for a common denominator.

The revival of planned extracapsular extrac­tion offered a unique opportunity to compare intracapsular and extracapsular aphakic eyes. The clinical specular microscope revealed im­portant Information about corneal endothelium that suggested that endothelial cell destruction continued in many intracapsular aphakic eyes, but did not continue in extracapsular aphakic eyes.

It was suggested that aqueous turbulences could play a role in this process of cell destruc­tion.6·7 It was also realized that intracapsular extraction resulted in the instability of the vit­reous, and that it could be responsible for reti­nal damage, supposedly due to microconcus­sion of the retina. 8 ·9 This hypothesis was con­sistent with the clinical finding that cystoid macular edema and retinal detachment were Jess frequent after extracapsular extraction than after intracapsular extraction. 10•

11 The fact that corneal and retinal complications can occur in otherwise "normal" aphakic eyes after unevent­ful cataract surgery led us to assume a mechan­ical origin. It is felt that the loss of the stabi­lizing function of the lens- zonule "barrier" and the subsequent increased mobility inside the eye, called endophthalmodonesis, could be the basis of late corneal and retinal complica­tions.12·13 Clinical and experimental observa­tions are available to support this view.

The mechanical aspect of endophthalmodo­nesis does not exclude the existence of a bio­chemical aspect of endophthalmodonesis. Bio­chemical substances, as a consequence of end­ophthalmodonesis, are likely to spread more easily and to a larger extent inside the eye, thus having remote effects. This applies to physio­logical substances as well as to pathological

substances, initiating or accompanying "inflam­mation." Here the sequelae are symptoms of ''barrier deprivation,'' in a molecular sense, with the lens-zonule system and the normal vitreous being important diffusion barriers. 14- 16

LENS-ZONULE BARRIER

Roughly speaking, the eyeball is divided into an anterior and posterior segment, that are sepa­rated from each other by the crystalline lens, including the zonular fibers. This lens- zonule system, in addition to its optical function, func­tions as a stabilizing framework inside the eye ball. The lens-zonule system is a barrier pro­hibiting displacement of the contents of the an­terior and posterior segment. In intracapsular cataract extraction, this barrier is completely removed, while in extracapsular cataract ex­traction, it is only partly removed. Barrier deprivation has many morphologic and patho­physiologic consequences that together consti­tute the barrier deprivation syndrome. 12,i3 Sev­eral symptoms of barrier deprivation apparently are of no clinical significance and not noticed by the patient, while others are of a more serious nature for the eye and for the patient.

ANTERIOR SEGMENT ENDOPHTHALMODONESIS

The aqueous hydrodynamics of the normal eye depend on the interaction of several im­pulses: the bulk-flow; a superimposed second­ary pressure circulation due to pressure varia­tions deriving from the pulse beat, the respira­tion, and muscle activity; and a thermal aqueous circulation, due to the temperature difference between the iris and the cornea. 17 The hy­drodynamic pattern of the aqueous is also influ­enced by the position of the eye. The resulting currents and turbulences in the aqueous, as can be seen with slit-lamp examination after injec­tion of fluorescein dye or in the presence of floating particles, are extremely slow and of mild nature. The aqueous exerts a relatively constant pressure on the exposed tissues. Sac­cadic movements of the eye are not likely to cause significant oscillations of the aqueous mass, as the iris is well-supported by the crys­talline lens (Fig 1).

CONSEQUENCES

Yet, these mild aqueous currents and turbu­lences have consequences. Turk already men­tioned them as one explanation for the localiza­tion of leukocyte deposits (Ehrlich-Turk line)

Fig 1. Saccadic movement of a phakic eye with intact vit­reous gel. The aqueous mass and the vitreous gel move with the eye and oscillations are not generated.

and pigmentary deposits (Axenfeld- Kruken­berg spindle) in otherwise normal eyes. 18

Erggelet later confirmed this on the basis of slit-lamp observations. He stated that these phenomena represent a "drop-out" in the "quiet" areas of turbulences. 19 However, one would expect this to happen in areas of "slack," but not in areas of turbulences.

Turbulences alter the surface of endothelial cells, making it easier for floating particles to adhere. This opinion is also expressed by Duke-Elder: "it is probable that the location is determined primarily by changes in the en­dothelium, the diseased or denuded cells al­lowing material to adhere. " 20 The Axenfeld­Krukenberg spindle, because it is more fre­quently seen with increasing age, supports this view, not only in its usual vertical arrangement, but also in its atypical localization. Vogt de­scribed a "mosaic pigmentation" of the hexa­gonal cell borders, which may point in the same direction. These observations are to be consid­ered as signs of a mild physiological "turbu­lence endotheliopathy.'' In pathologic condi­tions, turbulence endotheliopathy can have a more pronounced character. Massive pigmen­tary deposits frequently accompany degenera­tive conditions of the cornea, such as cornea guttata. Conditions with marked pigmentary deposits, partly due to endothelial changes and partly to increased pigment dispersion, are diabetes, chronic glaucoma, trauma, and in­traocular surgery.

DISTURBANCES

Cataract extraction disturbs the anatomy and consequently the hydrodynamics inside the eye. The mild character of the physiological aqueous currents and turbulances is changed into a completely different pattern. Saccadic movements of the eye now generate aqueous oscillations, made possible by the lack of iris support from the lens. These oscillations are most pronounced after intracapsular extraction and to a lesser degree after extracapsular ex­traction, the capsular membrane providing some resistance behind the iris (Figs 2, 3). Os­cillations of the aqueous betray themselves as iridodonesis, that is known to have the largest amplitude in intracapsular aphakic eyes. Jagger and Jacobi21 analyzed aqueous oscillations in intracapsular and extracapsular eyes, using the excursions of the reflexes on an intraocular lens as a reference. This study also confirmed that there is much more energy involved in aqueous oscillations in the intracapsular eye than in the extracapsular eye. During oscillations of the aqueous, turbulences exist in the outer lamina of the aqueous which is in contact with the slightly uneven surface of the corneal en­dothelium. These turbulences can easily be demonstrated under experimental conditions (Fig 4). This makes it understandable that the

Fig 2. Saccadic movement of an intracapsular aphakic eye with vitreous degeneration. The aqueous mass and the liquefied vitreous clearly lag behind the eye movement. An oscillatory movement is started, in which the oscillation of the aqueous and the vitreous reinforce each other. The iris diaphragm allows a large amplitude and a long duration.

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Fig 3. Saccadic movement of an extracapsular aphakic eye. Oscillation of the aqueous mass has a small amplitude and is of short duration due to the resistance of the capsular membrane and the zonular system behind the iris dia­phragm. With an intact vitreous gel, the hydrodynamic pattern in the posterior segment is normal. With liquified vitreous, oscillation in the posterior segment would also have a small amplitude due to the presence of the capsular membrane and the zonular system.

Fig 4. Rotation of a glass sphere filled with water elicits a rotational movement of the water mass in opposite direc­tion. The outer lamina of the water mass adjacent to the glass (stippled) shows turbulences that can be made visible by dispersion of small floating particles in the water. The more uneven the glass, the more violent the turbulences.

Fig 5. Patch of pigmentation of the corneal endothelium opposite a peripheral iris coloboma. This illustrates how aberrant aqueous flow through the coloboma can damage the endothelium and prepare it for pigment uptake.

risk for severe "turbulance endotheliopathy," surface alteration of the endothelium, destruc­tion of endothelial cells, and decompensation of the endothelial function, is highest after in­tracapsular cataract extraction.

A phenomenon that apparently is caused by aberrant aqueous flow and damage to the corneal endothelium, never described as such, is the patches of pigmentation not infrequently occurring opposite a peripheral iris coloboma (Fig 5). We assume that aberrant aqueous flow through the coloboma, carrying pigment par­ticles or iris clump cells and damaging the cor­neal endothelium, is the explanation for this phenomenon.

ENDOTHELIAL CELL DENSITY

Another example of turbulence endothe­liopathy is the long-term corneal endothelial condition after intracapsular cataract extrac­tion.6·7 In two comparative retrospective studies of intracapsular and extracapsular pseudo­phakic eyes, a marked discrepancy was noted between the central endothelial cell density in both series. The series compared were as closely matched as possible as to age and period of observation. In all eyes, surgery and recov­ery had been uneventful. The first series con­sisted of 13 eyes after intracapsular extraction and 13 eyes after extracapsular extraction of different patients. The average age of the pa­tients was 71 years (intracapsular eyes) and 65 years for the extracapsular eyes. The average postoperative period was 63 months and 61 months respectively. The average cell density in the intracapsular eyes was only 1495 cells/ mm2 and in the extracapsular eyes 2408 cells/ mm2

, a difference of 38%. A second series of bilaterally treated patients made the compari­son possible of 23 eyes after intracapsular ex­traction and 23 eyes after extracapsular extrac­tion of the same patients. The average age of the patients was 71 years. The average postopera­tive period was 86.8 months for the intracapsu­Iar eyes and 65.7 months for the extracapsular eyes. The average cell density of the intracap­sular and extracapsular eyes was 1064 cells/ mm2 and 2166 cells/mm2 respectively. Here the difference was 50.8 per cent. The lowest cell densities occurred in the intracapsular eyes.

Because a retrospective study of a personal series of intracapsular aphakic eyes was not possible, the permission was requested and obtained to examine a series of 67 eyes of 41 patients that were operated on for intracapsular cataract extraction by Professor Jules Francois of Ghent, Belgium. This was a positive selection of eyes with extremely smooth surgery, un­eventful recovery, clear corneas and full visual acuity. The average age of the patients at the

time of surgery was 68.9 years and the average postoperative period was 73.2 months. The av­erage central endothelial cell density in this selected series was 1740 cells/mm2 with a cell density in four eyes ofless than 1000 cells/mm2 •

These figures are significantly lower than the average cell density in the extracapsular pseudophakic eyes in our own series and can hardly be explained by assuming mere opera­tive trauma.

A prospective, as yet unpublished, compara­tive study also suggested continuing endothelial cell destruction after intracapsular cataract ex­traction. Eight patients underwent surgery on both eyes on the same day, one eye with in­tracapsular extraction, the other eye with ex­tracapsular extraction. Surgery and the imme­diate postoperative period were uneventful in all eyes. The average age of the patients was 79 years. All eyes were periodically examined with the clinical specular microscope. There was no significant difference between operative cell loss in both eyes. Successive cell counts begin­ning at about three months postoperatively over a period of 24 months, however, suggested an increased cell loss in at least three intracapsular eyes, as compared with the extracapsular eyes. (Figs 6A, B).

Continuing endothelial cell loss after cataract surgery other than through aging has also been suggested by others. Hirst et al reported a trend toward continuing cell loss after intracapsular surgery. 22 They explained this cell loss was due to the existence of mild inflammation and a re­distribution of cells after the surgical trauma. We are inclined to explain continuing endothe­lial cell loss after intracapsular cataract extrac­tion with aqueous turbulences as part of the generalized endophthalmodonesis inside the aphakic eye.

CORNEAL DECOMPENSATION

Corneal turbulence endotheliopathy may well be the cause of many cases of late corneal de­compensation after intracapsular cataract ex­traction. Turbulence endotheliopathy may also be responsible for graft failure in cases of per­forating keratoplasty in intracapsular aphakic eyes. Jaffe states: "Another impression I have gained is that these grafts show a tendency to late clouding. In these circumstances the re­currence of corneal edema is not usually as­sociated with a readherence of vitreous to the back ofthe cornea," and also: " ... some eyes that were successfully grafted developed prob­lems after three to five years. " 23 The milder character of aqueous turbulences after ex­tracapsular extraction may explain the better results with perforating keratoplasty in ex­tracapsular aphakic eyes, and in combined

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penetrating keratoplasty and extracapsular cataract extraction. These better results are not only our own experience, but also that of other corneal surgeons. 24

•25

POSTERIOR SEGMENT ENDOPHTHALMODONESIS

It is generally recognized that retinal compli­cations after cataract surgery are due to post­operative changes in the vitreous. 26 Although the morphologic changes in the vitreous after cataract surgery are well known, their exact

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21 24 MONTHS PO.

relationship with retinal complications is still obscure. Tolentino and Schepens believe that traction bands in the posterior vitreous are re­sponsible for producing macular edema. 2 Gass and Norton, however, could not find clinical proof for vitreous traction, but remained con­vinced that changes in the vitreous play an im­portant role in the pathogenesis of cystoid macular edema. 4

The work done by Balazs in the Eye Re­search Institute of the Retina Foundation in Boston, and by Osterlin in Sweden, has pro­vided us with valuable information about the macromolecular composition of the normal and

the pathological vitreous, which is necessary to understand the properties of normal vitreous, the nature of vitreous changes after cataract surgery, and the consequences for the retina. According to Balazs, the vitreous contains two interwoven networks, a coarse netWork of col­lagen filaments, and a finer network of hyaluronic acid. 27 The highest concentration of hyaluronic acid is present in the outer layer of the vitreous, adjacent to the retina, where it is probably produced. Its concentration gradually decreases toward the lens-zonule barrier, a decrease that is assumed to be a diffusion gra­dient. 28 It is generally accepted that the hyaluronic acid functions as the stabilizer of the vitreous gel and thus is a protection against mechanical damage to the retina. As Osterlin formulated: "the visco-elasticity of the hyal­uronic acid makes the vitreous an ideal shock and vibration isolator. " 29

CHANGES IN THE VITREOUS

In a comparative study on phakic and aphakic postmortem human eyes, and in studies on aphakic monkey eyes, Osterlin found a marked deficit of hyaluronic acid in the vitreous of the aphakic eye only after intracapsular extraction and not after extracapsular extraction.29·30 Intra­capsular extraction caused the escape of hyal­uronic acid from the vitreous, whereas the in­tact posterior capsule of the lens after extracap­sular extraction turned out to be an important diffusion barrier for this substance. The obser­vations of Osterlin agree with the instability of the vitreous after intracapsular extraction which manifests itself by the aggregation of the col­lagen filaments, the formation of liquid pools, and retraction of the vitreous. Not infrequently, the posterior vitreous detaches and the anterior vitreous membrane rupturesY The mobility of the vitreous is increased (vitreodonesis), which can be demonstrated clinically.

The exact correlation of the vitreous changes with retinal pathology has only been partly elucidated. Altered vitreous dynamics have been referred to in the beginning of this century in connection with retinal detachment by Best and by Gonin (cited by Rosengren and Oster­lin32). Gonin already thought that, apart from vitreoretinal traction, "fluctuations" of the de­tached vitreous could be an additional cause of retinal detachment. Lindner did model experi­ments to illustrate that in case of an existing retinal hole, rotational movements of the eye could cause an elevation of the retina. Similar experiments recently were described by Rosen­gren and Osterlin. 32 The same opinion is shared by others. 33·34

The hypothesis is presented here that sac­cadic movements of the eye in the posterior

segment induce oscillations as soon as the vit­reous gel is retracted and a preretinal liquid pool has formed (Figs 2, 3). The liquid pooi oscillates in phase with the aqueous and in an intracapsu­lar aphakic eye, they reinforce each other. Due to the slightly irregular profile of the retina, the outer lamina of the liquid pool, as can be shown in experiments, is subject to turbulences (Fig 4). Turbulences finally cause microconcussions of the retina. Jagger and Jacobi21 estimated the energy absorbed by the retina after one saccade was 200 times greater than the energy absorbed in the anterior chamber. The results of repeated concussions are leakage of capillary endothelia and the formation of edema in the same way that pressure variations such as contusion of the eye may. cause retinal edema. The localization of retinal edema may have to do with multiple factors such as the thickness and the loose structure of the nerve fiber layer, and the a vas­cularity of certain areas prohibiting adequate resorption of the edema.35

TOPICAL VARIATIONS

An intriguing factor in this respect, however, is the topographical variation of the thickness of the inner limiting lamina of the retina. 36 This lamina generally is a thick structure, but is ex­tremely thin exactly in the macular area, the papillary area, and the ora serrata area. Even degenerative holes and ruptures have been de­scribed in these areas. The retinal capillaries seem to be much less protected against concus­sions in these areas. In this way, the develop­ment of edematous patches in the macula, of cystic degeneration of the macula, of lamellar and even penetrating holes in the macula, of papilledema, and perhaps of patches of edema and subsequent retinal holes at the ora serrata can be explained. Even if it is true that some formed vitreous remains attached to the retinal periphery, this vitreous is supposedly not any more the ideal shock absorber the normal vitre­ous represents. Floating vitreous remnants may even enhance hydfodynamical injury to the retinal periphery. Retinal edema is a manifesta­tion of turbulance endotheliopathy in the poste­rior segment, not infrequently seen after in­tracapsular cataract extraction.

THE CORNEA-RETINAL SYNDROME

By presuming that endophthalmodonesis and turbulence endotheliopathy are the common de­nominator of corneal and retinal complications after cataract extraction, we may expect a not haphazardly sirimltaneous occurrence. There

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are several observations available to document this statement. Nordlohne was the first to note that the occurrence of corneal dystrophy and cystoid macular edema after cataract extraction was not an independent one. In a series of 694 intracapsular cataract extractions with lens im­plantation, Nordlohne found cystoid macular edema in 3.31% and corneal dystrophy in 6.05% of the cases.

In terms of independency of both conditions, the incidence of simultaneous occurrence would therefore be 0.2%. He found, how­ever, both conditions present in at least seven eyes, being 1. 01%, an incidence five times higher.5 Several authors have reported a high incidence of cystoid macular edema in intracap­sular aphakic eyes that were subjected to per­forating keratoplasty. Jaffe states: "For some as yet unexplained reason, there appears to be a relatively high incidence of cystoid macular edema following aphakic keratoplasty. " 23 It is often suggested that cystoid macular edema in these cases is a consequence of keratoplasty. We have, however, diagnosed preoperatively cys­toid macular edema in eyes with corneal dys­trophy several times using the entoptic Haidinger brush phenomenon, which we feel is a useful diagnostic tool in these cases.

The retrospective study of 23 patients with one intracapsular and one extracapsular pseudophakic eye, mentioned before, revealed a parallel between low corneal endothelial cell counts and macular lesions. In 11 of the 23 intracapsular eyes, there was a clinically man­ifested maculopathy and an average endothelial cell count of only 871 cells/mm2 compared with an average of 1239 cells/mm2 in the remaining 12 cases without maculopathy. The extracapsular fellow eyes of these 23 patients had no macu­lopathy and an average endothelial cell count of 2166 cells/mm2

•

In the prospective study of eight patients with one intracapsular and one extracapsular eye, also mentioned earlier, retinal complications occurred in two of the intracapsular eyes. One patient developed cystoid macular edema five months after surgery. A second patient devel­oped retinal detachment 19 months after surgery. The regression of the corneal endothe­lial cell density in these two intracapsular eyes was steep; none of the eight extracapsular fel­low eyes developed retinal problems (Fig 6).

CONCLUSION

Corneal decompensation and retinal compli­cations are the most dreaded late complications of cataract extraction. They constitute the clini­cally most important symptoms of the aphakic

barrier deprivation syndrome. 12.13 In fact, the aphakic barrier deprivation syndrome com­prises all clinical arid subclinical manifestations of barrier deprivation, whether of no impor­tance or of serious nature, whether noticed by the patient or not. The following is a summary of signs that belong or may belong to the aphakic barrier deprivation syndrome.

1. Aphakia. 2. Forward displacement of the vitreous, even­

tually with herniation into the anterior chamber.

3. Forward displacement of the iris root and nar-rowing of the anterior chamber angle.

4. Iridodonesis. 5. Rupture of the anterior hyaloid membrane. 6. Degeneration (condensation, liquefaction) of

the vitreous with increased vitreodonesis. 7. Posterior detachment of the vitreous. 8. Aqueous "'flare," eventually ciliary flush. 9. Pigment dispersion .

10. Aphakic glaucoma. 11. Iris atrophy. 12. Corneal decompensation (continuing damage

to endothelial cells). 13. Maculopathy (subclinical macular edema,

cystoid macular edema, macula hole) . 14. Peripheral retinal degeneration. 15. Retinal detachment.

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