- Email: [email protected]
Corneal and Retinal Complications after Cataract Extraction
Corneal and Retinal Complications after Cataract Extraction The Mechanical Aspect of Endophthalmodonesis
(/)
z
0
i=
<{
0 ::J a._
::2 0 0
C. D. BINKHORST, MD
_J
<{
z
i== w
a:
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
0
z<{ _J
<{
w
z
a:
0
0
•
1(/)
a:
0
I y:
z
CD
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.
0160-6420/80/0700/0609/$00.95
©
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-
American Academy of Ophthalmology
609
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
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 POSTOPERATIVE COMPLICATIONS
,._• co
LlJ ~
::J _j
0
>
•
0
co CJl
>_j
::J
-,
•
>(_') 0 _j 0
~ _j
<(
I II
Cl...
0
610
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
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,i 3 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)
DISTURBANCES
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.
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 Jacobi 21 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
U)
z
0
i=
<(
u
::::i 0... ~
0
u _.J
<(
z
i= w a: 0
z
<( _.J
<(
w
z
a:
0
u
•
1Ul
a:
0
I
:,::
z
m
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.
611
1'-
a: w
aJ
::2:
::J
z
•
r-
eo
w
::2:
::J _J
0
>
•
0
co en
~
::J --,
•
>-
(.')
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.
0 _J 0 ::2: _J
<(
I
I-
I
0...
0
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.
612
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/ mm 2 and in the extracapsular eyes 2408 cells/ mm 2 , 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.
(j)
z
0
i=
::::J
Q_
~
0 0
_J
z
i= w
a: 0
z
z a: 0 0
•
r--
(j)
a: 0 I
~
z
Ill
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 613
Fig 6A. Corneal endothelial cell
~-._;:;:::::..-.:::::~o:::;;;;;;;=::::-------
density of eight intracapsular pseudophakic eyes in a period from 3 months to 24 months after surgery. In at least three eyes there is a steep regression of the cell density, in two of which there were serious retinal problems (cases 6 and 8). Surgery was uneventful.
7
--------8
,.._
a: w
[JJ
::;;: :)
z
•
,.._
3
6
9
12
15
21 ~NTHS
w
::;;:
:) __j
0
>
•
0
(J)
P.O.
.....
~
~ Ill ..J .J
..... u
>__j
:::J
7
--,
• >-
6
Fig 6B. No such steep regression of the cell density was found in 8 the eight extracapsular pseudophakic fellow eyes during the same period. Surgery on both eyes was performed on the same day. There were no retinal problems in any of the extracapsular eyes.
~
0
__j
0
::;;: __j
<(
I
1-
I
0...
0
3
6
9
12
15
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
614
1e
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 Jacobi 21 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.
(j)
z
0
i= <(
0
:::J ()_
~
0 0
_j
<(
z
i= w
a:
0
z
<( _j
<(
w z a:
0 0
•
1--
(j)
a:
0 I
::.:: z CD
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
615
1'--
a: w
[lJ
~
::::J
z
•
r-eo w ~
::::J _j
0
>
•
0
co
0)
>_j
::::J -,
•
>-
(')
0
_j
0
~ _j
<(
I
I-
I
Q_
0
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
616
barrier deprivation syndrome. 1 2.1 3 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, eventually with herniation into the anterior chamber. 3. Forward displacement of the iris root and narrowing 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.
REFERENCES 1. Binkhorst CD. The iridocapsular (two-loop) lens and the iris-clip (four-loop) lens in pseudophakia. Trans Am Acad Ophthalmol Otolaryngol 1973; 77 589-617. 2. Tolentino Fl, Schepens CL. Edema of posterior pole after cataract extraction. A biomicroscopic study. Arch Ophthalmol 1965; 74:781-6. 3. Jaffe NS. Vitreous traction at the posterior pole of the fundus due to alterations in the vitreous posterior. Trans Am Acad Ophthalmol Otolaryngol 1967; 71:642-52. 4. Gass JDM, Norton EWD. Cystoid macular edema and papilledema following cataract extraction. A fluorescein fundoscopic and angiographic study. Arch Ophthalmol1966; 76:646-61. 5. Nordlohne ME. The intraocular implant lens. Development and result with special reference to the Binkhorst lens. Doc Ophthalmol 1974; 38:1-269. 6. Binkhorst CD, Loones LH, Nygaard P. Biomicroscopical observations on corneal endothelium in pseudophakia. Trans Ophthalmol Soc UK 1977; 97:67-73. 7. Binkhorst CD, Nygaard P, Loones LH. Specular microscopy of the corneal endothelium and lens implant surgery. Am J Ophthalmol 1978; 85:597-605. 8. Binkhorst CD, Kats A, Tjan TT, Loones LH. Retinal accidents in pseudophakia-lntracapsular vs extracapsular surgery. Trans Am Acad Ophthalmol Otolaryngol 1976; 120-7. 9. Binkhorst CD. Pseudophaka. lntracapsular or extracapsular technique? Doc Ophthalmol Proc Ser 1976; 7:251-63.
10. Binkhorst CD, Kats A, Leonard PAM. Extracapsular pseudophakia. Results in 100 two-loop iridocapsular lens implantations. Am J Opthalmol1972; 73:625-36. 11. Binkhorst CD. Five hundred planned extracapsular extractions with irido-capsular lens and iris clip lens implantations in senile cataract. Ophthalmic Surg 1977; 8(3):37 -44. 12. Binkhorst CD. The Barrier deprivation syndrome. Presented at the International Symposium on Intraocular Lens Implantation. Tel-Aviv, Israel, March 1977. 13. Binkhorst CD. Personal interview between the editor and CD Binkhorst. (The barrier deprivation syndrome). Highlights Ophthalmol 1978-1979; 15:308. 14. Kolker AE, Becker B. Epinephrine maculopathy. Arch Ophthalmol 1968; 79:552-62. 15. Ozaki L. Permeability of the posterior lens capsule in connection with intraocular lens implant surgery. Concilium Ophthalmologicum, XXIII, Kyoto, 1978; Acta 2:1407-10. 16. Balazs EA. In: Jeanloz RW, Balazs EA, eds. The Amino Sugars: The Chemistry and Biology of Compounds Containing Amino Sugars. New York: Academic Press, 1965; 2A:401. 17. Duke-ElderS, ed. System of Ophthalmology. Vol. IV: Physiology of the Eye and of Vision. London: Kimpton, 1968; 118-20. 18. Turk S. Untersuchungen uber eine Stromung in der vorderen Augenkammer. Albrecht von Graefes Archiv Ophthalmol 1906; 64:481-501. 19. Erggelet H. Klinische Befunde bei fokaler Beleuchtung mit der Gullstrandschen Nernst-Spaltlampe. Klin Monatsbl Augenheilkd 1914; 53:449-70. 20. Duke-ElderS, ed. System of Ophthalmology. Vol. VIII: Diseases of the Outer Eye. London: Kimpton, 1965; 718. 21. Jagger WS, Jacobi KW. An analysis of pseudophakodonesis and iridodonesis. J Am lntraocul Implant Soc 1979; 5:203-6. 22. Hirst LW, Snip RC, Stark WJ, Maumenee AE. Quantitative corneal endothelial evaluation in intraocular lens implantation and cataract surgery. Am J Ophthalrnol 1977; 84:775-80. 23. Jaffe NS. Cataract Surgery and Its Complications. 2nd ed. St. Louis: CV Mosby, 1976.
24. van Loenen Martinet AHJ. Perforating corneal graft combined with extracapsular cataract extraction. Presented at the Netherlands Ophthalmological Society Annual Meeting, 171st. Amsterdam, 30 March-1 April1977. 25. Kok-van Alphen CC, VOiker-Dieben HJM. Indications and contra-indications for perforating keratoplasty. Doc Ophthalmol 1977; 44:35-8. 26. Jaffe NS, Light OS. Vitreous changes produced by cataract surgery. A study of 1,058 aphakic eyes. Arch Ophthalmol 1966; 76:541-53. 27. Balazs EA. Molecular morphology of the vitreous body. In: Smelser GK, ed. Structure of the Eye. New York: Academic Press, 1961; 293-310. 28. Osterlin SE, Balazs EA. Macromolecular composition and fine structure of the vitreous in the owl monkey. Exp Eye Res 1968; 7:534-45. 29. Osterlin S. Changes in the macromolecular composition of the vitreous produced by removal of the lens. Concilium Ophthalmologicum, XXI, Mexico, 1970; Acta 2:1620-3. 30. Osterlin S. Macromolecular composition of the vitreous in the aphakic owl monkey eye. Exp Eye Res 1978; 26:77-84. 31. Foos RY. Posterior vitreous detachment. Trans Am Acad Ophthalmol Otolaryngol 1972; 76:480-97. 32. Rosengren B, Osterlin S. Hydrodynamic events in the vitreous space accompanying eye movements. Significance for the pathogenesis of retinal detachment. Ophthalmologica 1976; 173:513-24 33. Osterlin S. On the molecular biology of the vitreous in the aphakic eye. Acta Ophthalmol (Copenh) 1977; 55 353-61. 34. Osterlin S. Vitreous changes after cataract extraction. In: Freeman HM, Hirose T, Schepens CL, eds. Vitreous Surgery and Advances in Fundus Diagnosis and Treatment. New York: Appleton-Century-Crofts, 1977; 15-21. 35. Duke Elder S, ed. System of Ophthalmology. Vol. X: Diseases of the Retina. London: Kimpton, 1967; 121-7. 36. Foos RY. Vitreoretinal juncture; topographical variations. Invest Ophthalmol 1972; 11:801-8.
en z
0
i=
<(
0 :=J 0..
~
0 0
....J
<(
z
f-
w a:: 0
z<( ....J
<(
w
z
a::
0 0
•
f-
en
a::
0
I y:
z
[l)
617
(/)
z
0
i=
<{
0 ::J a._
::2 0 0
C. D. BINKHORST, MD
_J
<{
z
i== w
a:
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
0
z<{ _J
<{
w
z
a:
0
0
•
1(/)
a:
0
I y:
z
CD
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.
0160-6420/80/0700/0609/$00.95
©
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-
American Academy of Ophthalmology
609
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
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 POSTOPERATIVE COMPLICATIONS
,._• co
LlJ ~
::J _j
0
>
•
0
co CJl
>_j
::J
-,
•
>(_') 0 _j 0
~ _j
<(
I II
Cl...
0
610
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
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,i 3 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)
DISTURBANCES
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.
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 Jacobi 21 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
U)
z
0
i=
<(
u
::::i 0... ~
0
u _.J
<(
z
i= w a: 0
z
<( _.J
<(
w
z
a:
0
u
•
1Ul
a:
0
I
:,::
z
m
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.
611
1'-
a: w
aJ
::2:
::J
z
•
r-
eo
w
::2:
::J _J
0
>
•
0
co en
~
::J --,
•
>-
(.')
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.
0 _J 0 ::2: _J
<(
I
I-
I
0...
0
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.
612
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/ mm 2 and in the extracapsular eyes 2408 cells/ mm 2 , 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.
(j)
z
0
i=
::::J
Q_
~
0 0
_J
z
i= w
a: 0
z
z a: 0 0
•
r--
(j)
a: 0 I
~
z
Ill
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 613
Fig 6A. Corneal endothelial cell
~-._;:;:::::..-.:::::~o:::;;;;;;;=::::-------
density of eight intracapsular pseudophakic eyes in a period from 3 months to 24 months after surgery. In at least three eyes there is a steep regression of the cell density, in two of which there were serious retinal problems (cases 6 and 8). Surgery was uneventful.
7
--------8
,.._
a: w
[JJ
::;;: :)
z
•
,.._
3
6
9
12
15
21 ~NTHS
w
::;;:
:) __j
0
>
•
0
(J)
P.O.
.....
~
~ Ill ..J .J
..... u
>__j
:::J
7
--,
• >-
6
Fig 6B. No such steep regression of the cell density was found in 8 the eight extracapsular pseudophakic fellow eyes during the same period. Surgery on both eyes was performed on the same day. There were no retinal problems in any of the extracapsular eyes.
~
0
__j
0
::;;: __j
<(
I
1-
I
0...
0
3
6
9
12
15
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
614
1e
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 Jacobi 21 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.
(j)
z
0
i= <(
0
:::J ()_
~
0 0
_j
<(
z
i= w
a:
0
z
<( _j
<(
w z a:
0 0
•
1--
(j)
a:
0 I
::.:: z CD
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
615
1'--
a: w
[lJ
~
::::J
z
•
r-eo w ~
::::J _j
0
>
•
0
co
0)
>_j
::::J -,
•
>-
(')
0
_j
0
~ _j
<(
I
I-
I
Q_
0
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
616
barrier deprivation syndrome. 1 2.1 3 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, eventually with herniation into the anterior chamber. 3. Forward displacement of the iris root and narrowing 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.
REFERENCES 1. Binkhorst CD. The iridocapsular (two-loop) lens and the iris-clip (four-loop) lens in pseudophakia. Trans Am Acad Ophthalmol Otolaryngol 1973; 77 589-617. 2. Tolentino Fl, Schepens CL. Edema of posterior pole after cataract extraction. A biomicroscopic study. Arch Ophthalmol 1965; 74:781-6. 3. Jaffe NS. Vitreous traction at the posterior pole of the fundus due to alterations in the vitreous posterior. Trans Am Acad Ophthalmol Otolaryngol 1967; 71:642-52. 4. Gass JDM, Norton EWD. Cystoid macular edema and papilledema following cataract extraction. A fluorescein fundoscopic and angiographic study. Arch Ophthalmol1966; 76:646-61. 5. Nordlohne ME. The intraocular implant lens. Development and result with special reference to the Binkhorst lens. Doc Ophthalmol 1974; 38:1-269. 6. Binkhorst CD, Loones LH, Nygaard P. Biomicroscopical observations on corneal endothelium in pseudophakia. Trans Ophthalmol Soc UK 1977; 97:67-73. 7. Binkhorst CD, Nygaard P, Loones LH. Specular microscopy of the corneal endothelium and lens implant surgery. Am J Ophthalmol 1978; 85:597-605. 8. Binkhorst CD, Kats A, Tjan TT, Loones LH. Retinal accidents in pseudophakia-lntracapsular vs extracapsular surgery. Trans Am Acad Ophthalmol Otolaryngol 1976; 120-7. 9. Binkhorst CD. Pseudophaka. lntracapsular or extracapsular technique? Doc Ophthalmol Proc Ser 1976; 7:251-63.
10. Binkhorst CD, Kats A, Leonard PAM. Extracapsular pseudophakia. Results in 100 two-loop iridocapsular lens implantations. Am J Opthalmol1972; 73:625-36. 11. Binkhorst CD. Five hundred planned extracapsular extractions with irido-capsular lens and iris clip lens implantations in senile cataract. Ophthalmic Surg 1977; 8(3):37 -44. 12. Binkhorst CD. The Barrier deprivation syndrome. Presented at the International Symposium on Intraocular Lens Implantation. Tel-Aviv, Israel, March 1977. 13. Binkhorst CD. Personal interview between the editor and CD Binkhorst. (The barrier deprivation syndrome). Highlights Ophthalmol 1978-1979; 15:308. 14. Kolker AE, Becker B. Epinephrine maculopathy. Arch Ophthalmol 1968; 79:552-62. 15. Ozaki L. Permeability of the posterior lens capsule in connection with intraocular lens implant surgery. Concilium Ophthalmologicum, XXIII, Kyoto, 1978; Acta 2:1407-10. 16. Balazs EA. In: Jeanloz RW, Balazs EA, eds. The Amino Sugars: The Chemistry and Biology of Compounds Containing Amino Sugars. New York: Academic Press, 1965; 2A:401. 17. Duke-ElderS, ed. System of Ophthalmology. Vol. IV: Physiology of the Eye and of Vision. London: Kimpton, 1968; 118-20. 18. Turk S. Untersuchungen uber eine Stromung in der vorderen Augenkammer. Albrecht von Graefes Archiv Ophthalmol 1906; 64:481-501. 19. Erggelet H. Klinische Befunde bei fokaler Beleuchtung mit der Gullstrandschen Nernst-Spaltlampe. Klin Monatsbl Augenheilkd 1914; 53:449-70. 20. Duke-ElderS, ed. System of Ophthalmology. Vol. VIII: Diseases of the Outer Eye. London: Kimpton, 1965; 718. 21. Jagger WS, Jacobi KW. An analysis of pseudophakodonesis and iridodonesis. J Am lntraocul Implant Soc 1979; 5:203-6. 22. Hirst LW, Snip RC, Stark WJ, Maumenee AE. Quantitative corneal endothelial evaluation in intraocular lens implantation and cataract surgery. Am J Ophthalrnol 1977; 84:775-80. 23. Jaffe NS. Cataract Surgery and Its Complications. 2nd ed. St. Louis: CV Mosby, 1976.
24. van Loenen Martinet AHJ. Perforating corneal graft combined with extracapsular cataract extraction. Presented at the Netherlands Ophthalmological Society Annual Meeting, 171st. Amsterdam, 30 March-1 April1977. 25. Kok-van Alphen CC, VOiker-Dieben HJM. Indications and contra-indications for perforating keratoplasty. Doc Ophthalmol 1977; 44:35-8. 26. Jaffe NS, Light OS. Vitreous changes produced by cataract surgery. A study of 1,058 aphakic eyes. Arch Ophthalmol 1966; 76:541-53. 27. Balazs EA. Molecular morphology of the vitreous body. In: Smelser GK, ed. Structure of the Eye. New York: Academic Press, 1961; 293-310. 28. Osterlin SE, Balazs EA. Macromolecular composition and fine structure of the vitreous in the owl monkey. Exp Eye Res 1968; 7:534-45. 29. Osterlin S. Changes in the macromolecular composition of the vitreous produced by removal of the lens. Concilium Ophthalmologicum, XXI, Mexico, 1970; Acta 2:1620-3. 30. Osterlin S. Macromolecular composition of the vitreous in the aphakic owl monkey eye. Exp Eye Res 1978; 26:77-84. 31. Foos RY. Posterior vitreous detachment. Trans Am Acad Ophthalmol Otolaryngol 1972; 76:480-97. 32. Rosengren B, Osterlin S. Hydrodynamic events in the vitreous space accompanying eye movements. Significance for the pathogenesis of retinal detachment. Ophthalmologica 1976; 173:513-24 33. Osterlin S. On the molecular biology of the vitreous in the aphakic eye. Acta Ophthalmol (Copenh) 1977; 55 353-61. 34. Osterlin S. Vitreous changes after cataract extraction. In: Freeman HM, Hirose T, Schepens CL, eds. Vitreous Surgery and Advances in Fundus Diagnosis and Treatment. New York: Appleton-Century-Crofts, 1977; 15-21. 35. Duke Elder S, ed. System of Ophthalmology. Vol. X: Diseases of the Retina. London: Kimpton, 1967; 121-7. 36. Foos RY. Vitreoretinal juncture; topographical variations. Invest Ophthalmol 1972; 11:801-8.
en z
0
i=
<(
0 :=J 0..
~
0 0
....J
<(
z
f-
w a:: 0
z<( ....J
<(
w
z
a::
0 0
•
f-
en
a::
0
I y:
z
[l)
617