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Extracapsular surgery in lens implantation (binkhorst lecture) part iv. some anatomical and pathophysiological implications
extracapsular surgery In lens implantation (binkhorst lecture) part iv. some anatomical and pathophysiological implications Jan Worst Haren (Gr) Holland Some Anatomical and Patho-physiological Implications The remarkable clinical observation of Binkhorst that extracapsular surgery is highly effective in preventing cystoid macular edema, an observation which has been confirmed by me in a short comparative series of extra- and intracapsular cases, has prompted anatomical and patho-physiological research. I assume that the disruption of the compartmentalizarion of the eye - into an anterior and a posterior segment - was the anatomical basis for cystoid macular edema, regardless of whatever biophysical effects finally produced this edema. It has been noted that the common denominator in cystoid macular edema is a broken anterior vitreous surface. One may assume that the function of extracapsular surgery is to preserve the vitreous face and probably vitreous integrity by leaving the posterior capsule intact. With disruption of the anterior vitreous surface I assume that anterior chamber influences reached the macula where they exerted their patho-physiological effects. A theory to that effect (The ABC TheoryS) has been proposed by the author. The physiological or patho-physiological routes of the anterior chamber influences on the macula have been the subject of an anatomical study. From this study a number of completely new anatomical facts about the vitreous body have emerged. The most remarkable observation is the presence of a large fluid filled space in front of the macula, the so-called BURSA PREMACULARIS. The Bursa Premaculans The anatomical presence of the bursa premacularis has been demonstrated by means of selective white Indian ink injections. This new anatomical structure (Fig. 1) is a sacklike, slightly oval, horizontally oriented space within the vitreous cavity filled with a clear fluid with the physical properties of water. Because of its connections, it is assumed that this fluid is identical to or at least closely related to aqueous humour. The bursa premacularis communicates with the area of MARTEGIANI by way of a short "canal". A second more conspicuous "canal" enters the premacular bursa from CLOQUET's canal.
Fig. 1. (Worst, J .G.F.) Schematic drawing to demonstrate the bursa premacularis. (1) bursa canal (2) Cloquet's canal (3) Ligamentum hyaloidea capsulare of Wieger.
The bottom of the bursa rests on an oval convex elevation of the vitreous membrane, named here the pars patelliformis membranae vitrealis. A strong adhesion exists between the rim of the bursa premacularis and the vitreous membrane around the pars patelliformis. This is identical to the "zirkumpapillo-makulare Adhaerenz" of Gartner. 7 This space posterior to the pars patelliformis is called here the spatium subbursale premaculare. Physiologically the convex shape of the subbursal space is maintained by a fluid pressure, which is higher than the intravitreal pressure. The premacular bursa is formed by a narrow canal (Fig. 1) which branches off from Cloquet's canal slightly below the equatorial plane. The top of the sack is supported by its connection with Cloquet's's canal (Fig. 1) around which it may "twine" with an incomplete spiral. Distant support is given to this double canal system by the insertion of the walls of cloquet's canal on the posterior surface canal on the posterior surface of the lens Legamentum Hyaloideo Capsulare of Weiger (Fig. 1). An intravitreal membrane, probably the tractus coronarius (Eisner!) surrounds the double canal system and supports and reinforces it. The entrance to the bursa is situated eccentrically and below the anatomical axis. The canal widens to form the funnellike top of the actual premacular bursa, the cupula bursae vitrealis (Fig. 2). The funnellike shape of the sack is evident in preparations, but under more 7
physiological intravitreal pressures, the sack assumes a more ballonlike sbape. The widest part of the bursa; the fundus .bursae maculmis, is situated a few tenths of a millimeter in front of the retina (Fig. 2). This part of the sack is suspended and extended by a vitreous "membrane" which is apparently continuous with the tractus preretinalis (Eisner2). (Fig. 2) The suspended part of the sack, the fornix, has an oval shape, with a vertical diameter of about 4 mm. and a horizontal diameter of about 6 mm. Below the suspended peripheral ring of the fornix of the. sack the bursa narrows sharply. It's very short inwards sloping wall inserts on the edge of the macula, in a wide "bonding ring," which is identical to the "zirkumpapillo-makulare Adhaerenz" of Gartner (Fig. 2).
Fig. 2 . (Worst, J.G.F.) Enlarged schematic. (1) Canal of doquet. (2) Superior branching channel. (3) Capula of bursa premacularis. (4) Fornix of bursa. (5) Area of Martegiam. (6) Vitreoretinallimiting membrane (Gartner). (7) Tractus preretinalis (Eisner). (8) Pars patelliform is membranae vitrealis. (9) Spatium subbursale premaculare. (10) Corona petaliformis. (11) Perimacular bonding ring. (12) Lower branching channel. (13) Ocellus prefovealis.
The wall of the sack shows a strong adherence with the posterior vitreous membrane and the internal limiting membrane (vitreous-retinale Grenzschicht of Gartner') . The oval bonding ring ("zirkumpapillo-makulare Adhaerenz" of Gartner) very readily traps ink particles. In fact the bonding ring is composed of a double layer of an intravitreal "membrane" structure, between which ink particles are trapped. 8
The strong attachment of the wall of the premacular bursa to the perimacular area suggests that traction phenomena can occur. However, it is in the nature of the hydrodynamics of the premacular bursa that such traction phenomena are minimal, on condition that the anterior segment is intact. It is the anterior vitreous membrane which plays an important rble in the damping of the vitreous movement and in the prevention of direct traction on the perimacular bonding ring. In the case of incomplete datachment of the posterior vitreous membrane, in which elements of the bottom of the premacular bursa remain attached to the rim of the macula, shrinkage of such remaining elements may result in a macular pucker. The loose-meshed bonding ring around the macula, as mentioned, strongly binds white ink particles. The very center of the premacular bursa however adheres strongly to the convex central part of the vitreous membrane (the patelliform part of the vitreous membrane Fig. 2) . This central adherent part does not retain white Indian ink particles. In this manner a very peculiar viewing window or porthole is produced in front of the fovea. (Fig. 2). This porthole provides an excellent view of the fovea through the bottom of the premacular bursa. We propose the name ocellus prefovealis for this window in the bottom of the premacular bursa. Shrinkage of the posterior vitreous membrane with contraction of the elements of the bottom of the premacular sack which remain attached to the vitreous membrane forms part of the general process of fibrous contraction of all of the collagenous elements of the vitreous body, which is presumably under the influence of ABC factors (Worse). The sub bursal premacular space. (Fig. 2) The central part of the bottom of the bursa premacularis lies in close opposition with the convex part of the posterior vitreous membrane (the pars patelliformis), but will separate from it when the posterior vitreous detaches. The lenticular space between the thin internal limiting membrane of the macula and the convex posterior vitreous membrane (the pars patelliform is) is called the sub bursal premacular space. This peculiar lenticular space seems to have received little attention in anatomical descriptions. It is, however, a universally present and most essential part of the vitreous membrane in front of the macula. When viewed from the direction of the premacular bursa the oval elevation of the pars patelliformis membrane vitrealis is very conspicuous, particularly when the ocellus premacularis is present. One may then observe the subbursal premacular space through this miniature viewing-window. The subbursal space appears to be
kept distended by internal fluid pressure. Puncture of the pars patelliformis leads to a collapse of the sub bursal space. If the macula is opened from behind the subbursal space can be filled with ink. This ink never enters the premacular bursa. One may conclude therefore that the premacular bursa and the sub bursal space are anatomically and functionally two completely separate structures. The interpretation of the separation of the bursal space from the subbursal space, in terms of membrane anatomy, is easy with Gartner's concept of the "vitreoretinale Grenzschicht," the vitreoretinal limiting layer. This author has shown the posterior vitreous membrane to consist distinctly of two layers. In our specimens where beginning posterior vitreous detachment was noted it was evident that the posterior vitreous detachment, as pointed out by Gartner, occurs as an intralamellar splitting of the vitreoretinal limiting layers. The separation between the vitreal part and the retinal part of the vitreoretinal limiting layer usually occurs in the bottom of the premacular bursa in such a manner that the premacular bursa detaches intact from the patelliform part of the vitreous membrane. The subbursal space over the macula remains intact in case of "normal" posterior vitreous detachment. However, a number of lesions of the internal limiting membrane around the macula may occur, when the "bonding ring" breaks apart. These lesions are of great significance in the pathogenesis of cystoid macular edema. Another very evident lesion is produced when the area of Martegiani detaches. It is assumed here, that the subbursal space is a physiological schisis in the vitreoretinallimiting layer. The subbursal premacular space therefore is formed by an intralamellar splitting. By far the strongest part is split off towards the vitreous and only an extremely thin layer adheres to the macula proper. The thick part is the pars patelliformis of the vitreous membrane. (Fig. 2). The tearing off of the premacular bursa at the bonding ring in vitreous detachment leads to a number of micro-lesions in the vitreoretinal limiting layer which may result in temporary or permanent local damage to the internal limiting membrane. Clinically this is sometimes manifested by perimacular haemorrhages or fluorescent spots. A bonding ring very much similar to the perimacular ring is formed by the edge of the area of Martegiani around the optic nerve. Structurally the area of Martegiani and the bottom of the premacular bursa are also very similar.
Vitreous Detachment In vitreous detachment peripapillary haemorrhages occur of the same type and clinical significance as the perimacular haemorrhages. In case of posterior vitreous detachment the splitting in the lamellae of the posterior vitreous membrane leaves the covering of the subbursal space intact. In fact, the lesions caused by the detachment are situated around this space. However, manifest rents may also be observed, which lead to a collapse of the lenticular covering. In carefully dissected eyes such rents are rare, but perimacular defects in the internal limiting membrane might occur more frequently. In case of posterior vitreous detachment several variations in the mode of detachment of the bottom of the premacular bursa are possible. The bursa may: 1. Remain adherent in its original state, with the posterior vitreous detaching around it. (Fig. 3). ~
Fig. 3. (Worst, J .G.F. ) Perimacular detachment.
2. Become completely detached without rupture of its bottom. This is a very common type of detachment. (Fig. 4). 3. Detach at the bonding ring, while the bottom of the premacular bursa remains attached. This causes the wellknown posterior vitreous pre~ macular hole (Eisner8 ). The walls of the bursa will now evaginate. (Fig. 5). If the bottom {)f the pre macular bursa remains attached to the rim of the macula, it may contract 9
at the edge of the premacular bursa. It seems that leakage of the intrabursal fluid takes place during the progressive splitting of the posterior vitreous membrane into the newly formed intralamellar retrovitreal space. This leakage would initiate the posterior vitreous detachment. The main entrance to the premacular bursa is a branch channel of Cloquet's canal. A smaller channel however connects the bottom of the bursa with Martegiani's prepapillary bursa. The wall of the prepapillary bursa has the same structure as the wall of the premacular bursa.
Fig. 4. (Worst, J.G.F.) Intact bursa premacularis.
Fig. 6. (Worst, J.G.F.) Peripheral vitreous detachment.
The Physiological Significance of the Premacular Bursa and the Subbursal Premacular Space.
Fig. 5. (Worst, J .G.F.) Premacular hole.
and cause macular pucker. 4. The more peripheral vitreous may detach, with the bursa remaining attached. Martegiani's area may detach separately. (Fig. 6). The posterior vitreous detachment usually starts 10
The hydrodynamic protection. When examining vitreous specimens with an intact and well visible premacular bursa, one may notice that movements imparted to the vitreous (vitreodonesis due to inertia of the vitreous gel) are only partially transmitted to the contents of the premacular bursa. The subbursal space is even more protected from such movements, as the convex covering of the macula and the fluid pressure in the subbursal space give effective mechanical protection to the macula. A remarkable hydrodynamic silence reigns in the bottom of the premacular bursa as the violent frictional movements of the cortical vitreous gel bypass the macula itself. Ink particles in the vitreous around the
macula show rapid movements while the ink in the bursa remains stagnant. The center of the bursa premacularis therefore is, so to say, the "eye" in the hurricane of stormy vitreous movements around the macula. At the limit of the excursions of the eye, a characteristic braking and damping effect may be noticed, which effectively prevents full traction on the base of the premacular bursa. This additional mechanical protective mechanism of the bursa premacularis is illustrated in Fij!. 7. The braking mechanism functions as follows: On rotation of the eye the inertia of the vitreous gel . causes a lag which stretches the intravitreal fiber system. The fibers of the wall of the premacular bursa have the longest "slack" and will not become fully stretthed. On counter rotation elastic forces exert a backwards pull on the vitreous which forces it in the opposite direction. The moving vitreous gel compresses the physiologically "inflated" anterior vitreous membrane.
Fig. 7. (Worst, J.G.F.) Hydrodynamies of the bursa premacularis.
Some aqueous is pressed into the posterior chamber through the zonules. This further contributes to the damping effect, because of the resistance in the zonular system. The aqueous "shockwave" is transmitted to the vitreous membrane on the opposite side. The fact that the vitreous membrane is physiologically distended, is difficult to show in the living eye. In aphakic eyes the membrane has lost it's
physiological insertions and become slack or contracted and cannot function as a fluid damping system. Only in phakic eyes with a sector iridectomy can one visualize the membrane in its distended state. If indentation is used the natural inflated position of the membrane is distorted. After return of the eye to its original position, the inertial vitreous movements and the accompanying braking and damping effects of the anterior vitreous membrane and the internal fiber systems of the vitreous are repeated in an inversed way when the eye looks in the opposite direction. It is important to note that the damping effects on the vitreous excursions around the macula are such that under physiological conditions the premacular bursa insertions do not reach the end of their tether. Furthermore the "slack" in the peribursal membrane system is greater than the total excursions permitted to the peripheral vitreous body. However, this system only works optimally in the phakic eye. In intracapsular aphakia this vitreous damping effect is lost and, in the case of an intact premacular bursa, considerably more traction will be exerted on the perimacular region and on the optic nerve head. These increased movements may precipitate a posterior vitreous detachment, and may contribute to a "disorderly" course, leading to perimacular lesions of the internal limiting membrane. When a slowly and "carefully" produced posterior vitreous detachment exists, this senile pathological condition can be highly protective for the macula in cases of intracapsular aphakia. However, if the bursa premacularis is still attached to the macula preoperatively, but detaches rapidly postoperatively, several lesions of the optic nerve head and the perimacular area can occur. Such lesions are through and through defects in the internal limiting membrane exactly at the site of the strongest attachments. Clinically such detachments are detected as local haemorrhages. I propose that cystoid macular edema is pathophysiologically predetermined by the anatomical changes around the premacular bursa, due to "defective" posterior vitreous detachment (Fig. 8). The extreme excursions and rapid changes of position may test the premacular hydrodynamic and mechanical system to its limits. One may show this by means of an entoptic test: One should look in total darkness to the extreme right and left, alternatively. The typical yellow phosphene, due to the pull exerted on the optic nerve, may now be visible. Occasionally however, a less conspicuous deep purple oval structure will appear in the projection of the macula. .This is the moment when the insertions of the premacular bursa temporarily reach the end of their tether. The configuration and orientation of the bursa macularis phosphene is illustrated in Fig. 7. 11
Fig. 8. (Worst, J .G.F.) Cystoid macular edema anatomy with posterior vitreous detachment.
Biochemical protection of the macula by the premacular bursa. The premacular bursa contains a clear liquid which is assumed to have been derived from the aqueous, which has percolated through the vitreous or may have entered Cloquet's canal, by way of defects in Wieger's ligament, in phakic eyes. The latter more direct route is very evident in intracapsularly aphakic eyes. In phakic eyes the anterior vitreous membrane severely restricts the entry of the aqueous from the posterior chamber into the vitreous, at least in as far as its biotoxic components are concerned. A postulated filling of the premacular bursa with aqueous permits one to define this reservoir as a "second posterior chamber." In view of the remarkable biochemical capacities of the aqueous to destroy exudative products, blood, fibrin, collagen, etc., in the anterior chamber, the presence of aqueous or a biochemically related fluid in the "second posterior chamber" would be very beneficial for continued optimal optical function of the media directly in front of the macula. In fact, blood and exudative products, which are poorly removed from the vitreous itself, are clinically rapidly removed when situated directly in front of the macula. One may explain this clinical observation by assuming a circulation of biochemical active fluid through the premacular bursa. Clinical observations on premacular and vitreal haemorrhages support this hypothesis of a specific circulation and biochemical activity in the premacular bursa. One only needs to bring to mind the remarkably different behaviour of diabetic retinopathy haemorrhages. If in the premacular area it will disappear rapidly; if located in the cortical vitreous, reabsorbtion may take weeks or months, if it occurs 12
at all. The subbursal premacular space, being completely walled off from the intravitreal premacular bursa, is protected from aqueous influences, also in aphakia, on condition that the thick premacular vitreous membrane (pars patellaris) is intact. The mechanism of detachment of the premacular bursa around the macula however, may lead to a number of perimacular lesions, involving also the internal limiting membrane. In this type of premacular bursa detachment, as part of the posterior vitreous membrane syndrome, the macula becomes highly vulnerable to cystoid macular edema in the case of intracapsular. lens extraction. Cystoid macular edema (Irvine-Gass) may be predetermined by perimacular vitreous detachment anomalies, of the internal limiting membrane, which permit ABC factors to damage perimacular capillaries. In the case of extracapsular lens extraction however, the failure of aqueous to enter Cloquet's canal is the basic mechanism for protection of the macula against cystoid macular edema. In the case of extracapsular lens extraction the posterior route of the aqueous to the posterior vitreous detachment remains blocked. The anatomically predetermined cystoid macular edema is not materialized now, as the ABC trigger mechanism remains inactive. Some Pathophysiological Speculations. 1. The anatomical size and shape of the premacular bursa and in particular of its bottom, strongly resemble the "bull's eye" of chloroquine retinopathy. The edge of the bursa corresponds to the outer rim of the lesion, while the center has the same size as the inner rim of the "bonding ring." If one assumes, that the corneal chloroquine deposits have passed into the cornea from the aqueous, one may then assume, that the posterior route through Cloquet's canal has transported the chloroquine into the premacular bursa. As the premacular bursa is a "bywater" of Cloquet's canal, this "bywater" may become polluted with chloroquine. Chloroquine retinopathy could be an example of a pharmaceutical premacular bursa pollution syndrome, and the imprint of the bottom of the sack on the retina a visible expression of it. 2. Some premacular haemorrhages duplicate the contour and the content of the premacular sack. 3. Some macular diseases, including certain types of senile macular degeneration, assume the shape of the premacular sack, as if toxic products had
settled in it. 4. Premacular membranes are often associated with posterior vitreous detachment. Depending upon the type of detachment one may encounter various membranous anomalies, which can be interpreted in terms of disrupted premacular bursa anatomy. Contraction of these membranes leads to macular pucker. 5. Macular edema in serous central retinopathy. The edge of the edematous disk is exactly confined to the insertion of the inner edge of the bonding ring. In the case of traumatic retinal edema, the expansion permitted to the swelling retina is limited by the concave premacular vitreous membrane. An en clavation of the retina may follow in the ocellus prefovealis. This phenomenon is comparable to cerebral en clavation in the foramen magnum. The ensuing necrosis of edematous retina in the ocellus leads to a round macular hole, the size of which is exactly equal to the prefoveal ocellus. Some serous central retinopathies might be due to the presence of toxic substances in the bursa. The failure of its passage through the reabsorbtion in Martegiani's area might be the cause of some still enigmatic central retinopathies associated with biochemical disturbances. 6. Retinitis proliferan~ configuration and premacular bursa wall anatomy. All typical diabetic retinopathies conform to the walls of Martegiani's area and the walls of the premacular bursa. The typical lobster glaw like configuration of advanced diabetic retinopathy is simply an expression of vessels growing into the wall of the premacular bursa. 7. Optic pit and central retinopathy. The optic pit is located at the point where the communicating channel enters the area of Martegiani. Anomalies in the area of the communicating channel may therefore interfere with normal physiology of the premacular bursa. For instance, if a stagnation occurs in the assumed flow of aqueous through the bursa towards the optic nerve, this fluid may accumulate submacularly. 8. Cystoid macular edema (Irvine-Gass Syndrome). In a previous paper I advanced a new pathogenic explanation for this postoperative complication of cataract surgery, the Aqueous Biotoxic Complex theory (ABC complex). The opening of Cloquet's canal by the intracapsular extraction leads to an inflow of aqueous and its biotoxic factors into the premacular bursa. If intact, the natural protection of the macula by the pars patelliformis prevails. The presence of the convex premacular vitreous membrane effec-
tively walls off the macula from aqueous influences. In the case of certain types of posterior vitreous detachment however, ABC factors can act directly on the macula, damaging the perimacular capillary bed, where the detachment of the bursa has caused lesions to the internal limiting membrane; the anatomical predetermination of C.M.D. The perimacular haemorrhages and perimacular fluorescence leaking points, are the clinical signs of such premacular bursa detachment. The usual way of vitreous detachment, however, is one of complete separation of the vitreous membrane without local perimacular damage. Though these cases will also have inflow of aqueous in the posterior vitreous detachment area in case of intracapsular surgery, they will not end up with cystoid macular edema. In this context, the explanation for cystoid macular edema therefore is twofold: 1. There is a preset anatomical condition of the macula, in which the premacular bursa has been detached in a relatively unphysiological manner. 2. The aqueous humour entering the posterior vitreous reservoir attacks the retinal capillaries through lesions caused by this unphysiological detachment mechanism. 9. The massive inflow of aqueous in the vitreous cavity in intra capsular aphakia leads to an extensive destruction of the fibrillar elements of the vitreous and to a further increase of the posterior vitreous detachment. This is the ABC effect on the vitreous itself. Normal vitreous detachment starts on the edge of the premacular bursa, in phakic and aphakic eyes. The aphakic condition however, vastly increases the speed and extent of the detachment. Summary Extracapsular surgery is an ideal type of cataract surgery in combination with lens implantation in that stability and fixation of the lens is greatly enhanced. However, a number of complications can be expected. The main problem of extracapsular surgery is posterior capsule opacification. This is due to regeneration of germinal lens fibres. To prevent this a complete removal of cortical lens matter is advisable, even in lens implantation. This however requires special lenses which have additional iris fixation. The author's technique for extracapsular surgery is described. The clinically protective effect of extracapsular surgery for the macula has led to the discovery of a new anatomical structure in front of the macula, the bursa premacularis. The bursa premacularis is a 13
well-defined fluid-filled space inside the vitreous body in front of the macula. It is postulated to have a protective function for the macula in a hydrodynamic and biochemical sense. A number of pathological conditions could be explained as primarily determined by toxic substances in the premacular bursa or defective detachment of the premacular bursa in the course of posterior vitreous detachment. If this latter condition exists, intracapsular surgery will cause cystoid macular edema, as aqueous can enter the perimacular retina. Cystoid macular edema therefore is postulated to be anatomicaIly predetermined. Acknowledgements I am much indebted to Dr. c.c. Kok-van Alphen, Dr. J. Otto, the Lions Eye Bank of Miami, Florida (Mrs. Pearl Goldberg) and Miss Inge Borgers for providing the pathology eyes. Acknowledgement is due to Prof. J.A. Oosterhuis for his suggestion in nomenclature. Mr. K. Otter's help is greatly appreciated. Without the help of Mrs. H. Bloemendaal-Stob, who did the secretarial work, Mrs. D.P. Vos-van Vliet, who did the anatomical dissections and of Mrs. A.M. Worst-van Dam, who gave her invaluable managerial advice. This paper in its entirety has been published as follows: I. II. III. IV.
AIOIS AIOIS AIOIS AIOIS
Jour. Jour. Jour. Jour.
VoL 2 #1 VoL 3 #2 VoL 3 #3 & 4 VoL 4 #1
References 1. Binkhorst, C.D.: Intra-oculaire lens prothese volgens Ridley, Ned. Tijdschr. v. Geneesk. Jaargang 100, No. 48, Dec. 1956. Binkhorst, C.D.: Iris supported artificial pseudophakos. Trans Ophthal. Soc. UK 79:569,1959. Binkhorst, C.D., Leonard, P.A.M.: Results in 208 Iris-Clip Pseudophakos Implantations. Am. J. Ophthal. VoL 64, No. 5,947-956,1967. 2. Binkhorst, C.D., Kats, A., Leonard, P.A.M.: Extracapsular Pseudophakia. Am. J. OphthaL Vol. 73, No.5, 625-636, May 1972. 3. Worst, J .G.F.: Biotoxizitat des Kammerwassers. Klin. MonatsbL Augenheilk. 167 Band, 3 Heft, 1975. 4. Worst, J.G.F., v.d. Heyden, R.: A Simplified Echographic Procedure for Clinical Oculography, BibL ophthaL, No. 83, pp. 269-272, 1975 (Karger-Basel). 5. Alpar J.J.: A new technique to suture the Binkhorst two-loop & four-loop & Fyodorov lenses. Manuscript. 6. Ridley, H.: Intraocular acrylic lenses. Trans OphthaL Soc. UK 71: 617-621, 1951. 7. Gartner, J.: Histologische Beobachtungen tiber das Verhalten der vitreoretinalen Grenzschicht bei Glaskorperabhebung, K1, MonatsbL Augenheilk, 142 (1963) 769-792. 8. Eisner, G.: Biomicroscopy of the peripheral fundus, Springer Verlag, Berlin-Heidelberg - New York, 1973.
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Fig. 1. (Worst, J .G.F.) Schematic drawing to demonstrate the bursa premacularis. (1) bursa canal (2) Cloquet's canal (3) Ligamentum hyaloidea capsulare of Wieger.
The bottom of the bursa rests on an oval convex elevation of the vitreous membrane, named here the pars patelliformis membranae vitrealis. A strong adhesion exists between the rim of the bursa premacularis and the vitreous membrane around the pars patelliformis. This is identical to the "zirkumpapillo-makulare Adhaerenz" of Gartner. 7 This space posterior to the pars patelliformis is called here the spatium subbursale premaculare. Physiologically the convex shape of the subbursal space is maintained by a fluid pressure, which is higher than the intravitreal pressure. The premacular bursa is formed by a narrow canal (Fig. 1) which branches off from Cloquet's canal slightly below the equatorial plane. The top of the sack is supported by its connection with Cloquet's's canal (Fig. 1) around which it may "twine" with an incomplete spiral. Distant support is given to this double canal system by the insertion of the walls of cloquet's canal on the posterior surface canal on the posterior surface of the lens Legamentum Hyaloideo Capsulare of Weiger (Fig. 1). An intravitreal membrane, probably the tractus coronarius (Eisner!) surrounds the double canal system and supports and reinforces it. The entrance to the bursa is situated eccentrically and below the anatomical axis. The canal widens to form the funnellike top of the actual premacular bursa, the cupula bursae vitrealis (Fig. 2). The funnellike shape of the sack is evident in preparations, but under more 7
physiological intravitreal pressures, the sack assumes a more ballonlike sbape. The widest part of the bursa; the fundus .bursae maculmis, is situated a few tenths of a millimeter in front of the retina (Fig. 2). This part of the sack is suspended and extended by a vitreous "membrane" which is apparently continuous with the tractus preretinalis (Eisner2). (Fig. 2) The suspended part of the sack, the fornix, has an oval shape, with a vertical diameter of about 4 mm. and a horizontal diameter of about 6 mm. Below the suspended peripheral ring of the fornix of the. sack the bursa narrows sharply. It's very short inwards sloping wall inserts on the edge of the macula, in a wide "bonding ring," which is identical to the "zirkumpapillo-makulare Adhaerenz" of Gartner (Fig. 2).
Fig. 2 . (Worst, J.G.F.) Enlarged schematic. (1) Canal of doquet. (2) Superior branching channel. (3) Capula of bursa premacularis. (4) Fornix of bursa. (5) Area of Martegiam. (6) Vitreoretinallimiting membrane (Gartner). (7) Tractus preretinalis (Eisner). (8) Pars patelliform is membranae vitrealis. (9) Spatium subbursale premaculare. (10) Corona petaliformis. (11) Perimacular bonding ring. (12) Lower branching channel. (13) Ocellus prefovealis.
The wall of the sack shows a strong adherence with the posterior vitreous membrane and the internal limiting membrane (vitreous-retinale Grenzschicht of Gartner') . The oval bonding ring ("zirkumpapillo-makulare Adhaerenz" of Gartner) very readily traps ink particles. In fact the bonding ring is composed of a double layer of an intravitreal "membrane" structure, between which ink particles are trapped. 8
The strong attachment of the wall of the premacular bursa to the perimacular area suggests that traction phenomena can occur. However, it is in the nature of the hydrodynamics of the premacular bursa that such traction phenomena are minimal, on condition that the anterior segment is intact. It is the anterior vitreous membrane which plays an important rble in the damping of the vitreous movement and in the prevention of direct traction on the perimacular bonding ring. In the case of incomplete datachment of the posterior vitreous membrane, in which elements of the bottom of the premacular bursa remain attached to the rim of the macula, shrinkage of such remaining elements may result in a macular pucker. The loose-meshed bonding ring around the macula, as mentioned, strongly binds white ink particles. The very center of the premacular bursa however adheres strongly to the convex central part of the vitreous membrane (the patelliform part of the vitreous membrane Fig. 2) . This central adherent part does not retain white Indian ink particles. In this manner a very peculiar viewing window or porthole is produced in front of the fovea. (Fig. 2). This porthole provides an excellent view of the fovea through the bottom of the premacular bursa. We propose the name ocellus prefovealis for this window in the bottom of the premacular bursa. Shrinkage of the posterior vitreous membrane with contraction of the elements of the bottom of the premacular sack which remain attached to the vitreous membrane forms part of the general process of fibrous contraction of all of the collagenous elements of the vitreous body, which is presumably under the influence of ABC factors (Worse). The sub bursal premacular space. (Fig. 2) The central part of the bottom of the bursa premacularis lies in close opposition with the convex part of the posterior vitreous membrane (the pars patelliformis), but will separate from it when the posterior vitreous detaches. The lenticular space between the thin internal limiting membrane of the macula and the convex posterior vitreous membrane (the pars patelliform is) is called the sub bursal premacular space. This peculiar lenticular space seems to have received little attention in anatomical descriptions. It is, however, a universally present and most essential part of the vitreous membrane in front of the macula. When viewed from the direction of the premacular bursa the oval elevation of the pars patelliformis membrane vitrealis is very conspicuous, particularly when the ocellus premacularis is present. One may then observe the subbursal premacular space through this miniature viewing-window. The subbursal space appears to be
kept distended by internal fluid pressure. Puncture of the pars patelliformis leads to a collapse of the sub bursal space. If the macula is opened from behind the subbursal space can be filled with ink. This ink never enters the premacular bursa. One may conclude therefore that the premacular bursa and the sub bursal space are anatomically and functionally two completely separate structures. The interpretation of the separation of the bursal space from the subbursal space, in terms of membrane anatomy, is easy with Gartner's concept of the "vitreoretinale Grenzschicht," the vitreoretinal limiting layer. This author has shown the posterior vitreous membrane to consist distinctly of two layers. In our specimens where beginning posterior vitreous detachment was noted it was evident that the posterior vitreous detachment, as pointed out by Gartner, occurs as an intralamellar splitting of the vitreoretinal limiting layers. The separation between the vitreal part and the retinal part of the vitreoretinal limiting layer usually occurs in the bottom of the premacular bursa in such a manner that the premacular bursa detaches intact from the patelliform part of the vitreous membrane. The subbursal space over the macula remains intact in case of "normal" posterior vitreous detachment. However, a number of lesions of the internal limiting membrane around the macula may occur, when the "bonding ring" breaks apart. These lesions are of great significance in the pathogenesis of cystoid macular edema. Another very evident lesion is produced when the area of Martegiani detaches. It is assumed here, that the subbursal space is a physiological schisis in the vitreoretinallimiting layer. The subbursal premacular space therefore is formed by an intralamellar splitting. By far the strongest part is split off towards the vitreous and only an extremely thin layer adheres to the macula proper. The thick part is the pars patelliformis of the vitreous membrane. (Fig. 2). The tearing off of the premacular bursa at the bonding ring in vitreous detachment leads to a number of micro-lesions in the vitreoretinal limiting layer which may result in temporary or permanent local damage to the internal limiting membrane. Clinically this is sometimes manifested by perimacular haemorrhages or fluorescent spots. A bonding ring very much similar to the perimacular ring is formed by the edge of the area of Martegiani around the optic nerve. Structurally the area of Martegiani and the bottom of the premacular bursa are also very similar.
Vitreous Detachment In vitreous detachment peripapillary haemorrhages occur of the same type and clinical significance as the perimacular haemorrhages. In case of posterior vitreous detachment the splitting in the lamellae of the posterior vitreous membrane leaves the covering of the subbursal space intact. In fact, the lesions caused by the detachment are situated around this space. However, manifest rents may also be observed, which lead to a collapse of the lenticular covering. In carefully dissected eyes such rents are rare, but perimacular defects in the internal limiting membrane might occur more frequently. In case of posterior vitreous detachment several variations in the mode of detachment of the bottom of the premacular bursa are possible. The bursa may: 1. Remain adherent in its original state, with the posterior vitreous detaching around it. (Fig. 3). ~
Fig. 3. (Worst, J .G.F. ) Perimacular detachment.
2. Become completely detached without rupture of its bottom. This is a very common type of detachment. (Fig. 4). 3. Detach at the bonding ring, while the bottom of the premacular bursa remains attached. This causes the wellknown posterior vitreous pre~ macular hole (Eisner8 ). The walls of the bursa will now evaginate. (Fig. 5). If the bottom {)f the pre macular bursa remains attached to the rim of the macula, it may contract 9
at the edge of the premacular bursa. It seems that leakage of the intrabursal fluid takes place during the progressive splitting of the posterior vitreous membrane into the newly formed intralamellar retrovitreal space. This leakage would initiate the posterior vitreous detachment. The main entrance to the premacular bursa is a branch channel of Cloquet's canal. A smaller channel however connects the bottom of the bursa with Martegiani's prepapillary bursa. The wall of the prepapillary bursa has the same structure as the wall of the premacular bursa.
Fig. 4. (Worst, J.G.F.) Intact bursa premacularis.
Fig. 6. (Worst, J.G.F.) Peripheral vitreous detachment.
The Physiological Significance of the Premacular Bursa and the Subbursal Premacular Space.
Fig. 5. (Worst, J .G.F.) Premacular hole.
and cause macular pucker. 4. The more peripheral vitreous may detach, with the bursa remaining attached. Martegiani's area may detach separately. (Fig. 6). The posterior vitreous detachment usually starts 10
The hydrodynamic protection. When examining vitreous specimens with an intact and well visible premacular bursa, one may notice that movements imparted to the vitreous (vitreodonesis due to inertia of the vitreous gel) are only partially transmitted to the contents of the premacular bursa. The subbursal space is even more protected from such movements, as the convex covering of the macula and the fluid pressure in the subbursal space give effective mechanical protection to the macula. A remarkable hydrodynamic silence reigns in the bottom of the premacular bursa as the violent frictional movements of the cortical vitreous gel bypass the macula itself. Ink particles in the vitreous around the
macula show rapid movements while the ink in the bursa remains stagnant. The center of the bursa premacularis therefore is, so to say, the "eye" in the hurricane of stormy vitreous movements around the macula. At the limit of the excursions of the eye, a characteristic braking and damping effect may be noticed, which effectively prevents full traction on the base of the premacular bursa. This additional mechanical protective mechanism of the bursa premacularis is illustrated in Fij!. 7. The braking mechanism functions as follows: On rotation of the eye the inertia of the vitreous gel . causes a lag which stretches the intravitreal fiber system. The fibers of the wall of the premacular bursa have the longest "slack" and will not become fully stretthed. On counter rotation elastic forces exert a backwards pull on the vitreous which forces it in the opposite direction. The moving vitreous gel compresses the physiologically "inflated" anterior vitreous membrane.
Fig. 7. (Worst, J.G.F.) Hydrodynamies of the bursa premacularis.
Some aqueous is pressed into the posterior chamber through the zonules. This further contributes to the damping effect, because of the resistance in the zonular system. The aqueous "shockwave" is transmitted to the vitreous membrane on the opposite side. The fact that the vitreous membrane is physiologically distended, is difficult to show in the living eye. In aphakic eyes the membrane has lost it's
physiological insertions and become slack or contracted and cannot function as a fluid damping system. Only in phakic eyes with a sector iridectomy can one visualize the membrane in its distended state. If indentation is used the natural inflated position of the membrane is distorted. After return of the eye to its original position, the inertial vitreous movements and the accompanying braking and damping effects of the anterior vitreous membrane and the internal fiber systems of the vitreous are repeated in an inversed way when the eye looks in the opposite direction. It is important to note that the damping effects on the vitreous excursions around the macula are such that under physiological conditions the premacular bursa insertions do not reach the end of their tether. Furthermore the "slack" in the peribursal membrane system is greater than the total excursions permitted to the peripheral vitreous body. However, this system only works optimally in the phakic eye. In intracapsular aphakia this vitreous damping effect is lost and, in the case of an intact premacular bursa, considerably more traction will be exerted on the perimacular region and on the optic nerve head. These increased movements may precipitate a posterior vitreous detachment, and may contribute to a "disorderly" course, leading to perimacular lesions of the internal limiting membrane. When a slowly and "carefully" produced posterior vitreous detachment exists, this senile pathological condition can be highly protective for the macula in cases of intracapsular aphakia. However, if the bursa premacularis is still attached to the macula preoperatively, but detaches rapidly postoperatively, several lesions of the optic nerve head and the perimacular area can occur. Such lesions are through and through defects in the internal limiting membrane exactly at the site of the strongest attachments. Clinically such detachments are detected as local haemorrhages. I propose that cystoid macular edema is pathophysiologically predetermined by the anatomical changes around the premacular bursa, due to "defective" posterior vitreous detachment (Fig. 8). The extreme excursions and rapid changes of position may test the premacular hydrodynamic and mechanical system to its limits. One may show this by means of an entoptic test: One should look in total darkness to the extreme right and left, alternatively. The typical yellow phosphene, due to the pull exerted on the optic nerve, may now be visible. Occasionally however, a less conspicuous deep purple oval structure will appear in the projection of the macula. .This is the moment when the insertions of the premacular bursa temporarily reach the end of their tether. The configuration and orientation of the bursa macularis phosphene is illustrated in Fig. 7. 11
Fig. 8. (Worst, J .G.F.) Cystoid macular edema anatomy with posterior vitreous detachment.
Biochemical protection of the macula by the premacular bursa. The premacular bursa contains a clear liquid which is assumed to have been derived from the aqueous, which has percolated through the vitreous or may have entered Cloquet's canal, by way of defects in Wieger's ligament, in phakic eyes. The latter more direct route is very evident in intracapsularly aphakic eyes. In phakic eyes the anterior vitreous membrane severely restricts the entry of the aqueous from the posterior chamber into the vitreous, at least in as far as its biotoxic components are concerned. A postulated filling of the premacular bursa with aqueous permits one to define this reservoir as a "second posterior chamber." In view of the remarkable biochemical capacities of the aqueous to destroy exudative products, blood, fibrin, collagen, etc., in the anterior chamber, the presence of aqueous or a biochemically related fluid in the "second posterior chamber" would be very beneficial for continued optimal optical function of the media directly in front of the macula. In fact, blood and exudative products, which are poorly removed from the vitreous itself, are clinically rapidly removed when situated directly in front of the macula. One may explain this clinical observation by assuming a circulation of biochemical active fluid through the premacular bursa. Clinical observations on premacular and vitreal haemorrhages support this hypothesis of a specific circulation and biochemical activity in the premacular bursa. One only needs to bring to mind the remarkably different behaviour of diabetic retinopathy haemorrhages. If in the premacular area it will disappear rapidly; if located in the cortical vitreous, reabsorbtion may take weeks or months, if it occurs 12
at all. The subbursal premacular space, being completely walled off from the intravitreal premacular bursa, is protected from aqueous influences, also in aphakia, on condition that the thick premacular vitreous membrane (pars patellaris) is intact. The mechanism of detachment of the premacular bursa around the macula however, may lead to a number of perimacular lesions, involving also the internal limiting membrane. In this type of premacular bursa detachment, as part of the posterior vitreous membrane syndrome, the macula becomes highly vulnerable to cystoid macular edema in the case of intracapsular. lens extraction. Cystoid macular edema (Irvine-Gass) may be predetermined by perimacular vitreous detachment anomalies, of the internal limiting membrane, which permit ABC factors to damage perimacular capillaries. In the case of extracapsular lens extraction however, the failure of aqueous to enter Cloquet's canal is the basic mechanism for protection of the macula against cystoid macular edema. In the case of extracapsular lens extraction the posterior route of the aqueous to the posterior vitreous detachment remains blocked. The anatomically predetermined cystoid macular edema is not materialized now, as the ABC trigger mechanism remains inactive. Some Pathophysiological Speculations. 1. The anatomical size and shape of the premacular bursa and in particular of its bottom, strongly resemble the "bull's eye" of chloroquine retinopathy. The edge of the bursa corresponds to the outer rim of the lesion, while the center has the same size as the inner rim of the "bonding ring." If one assumes, that the corneal chloroquine deposits have passed into the cornea from the aqueous, one may then assume, that the posterior route through Cloquet's canal has transported the chloroquine into the premacular bursa. As the premacular bursa is a "bywater" of Cloquet's canal, this "bywater" may become polluted with chloroquine. Chloroquine retinopathy could be an example of a pharmaceutical premacular bursa pollution syndrome, and the imprint of the bottom of the sack on the retina a visible expression of it. 2. Some premacular haemorrhages duplicate the contour and the content of the premacular sack. 3. Some macular diseases, including certain types of senile macular degeneration, assume the shape of the premacular sack, as if toxic products had
settled in it. 4. Premacular membranes are often associated with posterior vitreous detachment. Depending upon the type of detachment one may encounter various membranous anomalies, which can be interpreted in terms of disrupted premacular bursa anatomy. Contraction of these membranes leads to macular pucker. 5. Macular edema in serous central retinopathy. The edge of the edematous disk is exactly confined to the insertion of the inner edge of the bonding ring. In the case of traumatic retinal edema, the expansion permitted to the swelling retina is limited by the concave premacular vitreous membrane. An en clavation of the retina may follow in the ocellus prefovealis. This phenomenon is comparable to cerebral en clavation in the foramen magnum. The ensuing necrosis of edematous retina in the ocellus leads to a round macular hole, the size of which is exactly equal to the prefoveal ocellus. Some serous central retinopathies might be due to the presence of toxic substances in the bursa. The failure of its passage through the reabsorbtion in Martegiani's area might be the cause of some still enigmatic central retinopathies associated with biochemical disturbances. 6. Retinitis proliferan~ configuration and premacular bursa wall anatomy. All typical diabetic retinopathies conform to the walls of Martegiani's area and the walls of the premacular bursa. The typical lobster glaw like configuration of advanced diabetic retinopathy is simply an expression of vessels growing into the wall of the premacular bursa. 7. Optic pit and central retinopathy. The optic pit is located at the point where the communicating channel enters the area of Martegiani. Anomalies in the area of the communicating channel may therefore interfere with normal physiology of the premacular bursa. For instance, if a stagnation occurs in the assumed flow of aqueous through the bursa towards the optic nerve, this fluid may accumulate submacularly. 8. Cystoid macular edema (Irvine-Gass Syndrome). In a previous paper I advanced a new pathogenic explanation for this postoperative complication of cataract surgery, the Aqueous Biotoxic Complex theory (ABC complex). The opening of Cloquet's canal by the intracapsular extraction leads to an inflow of aqueous and its biotoxic factors into the premacular bursa. If intact, the natural protection of the macula by the pars patelliformis prevails. The presence of the convex premacular vitreous membrane effec-
tively walls off the macula from aqueous influences. In the case of certain types of posterior vitreous detachment however, ABC factors can act directly on the macula, damaging the perimacular capillary bed, where the detachment of the bursa has caused lesions to the internal limiting membrane; the anatomical predetermination of C.M.D. The perimacular haemorrhages and perimacular fluorescence leaking points, are the clinical signs of such premacular bursa detachment. The usual way of vitreous detachment, however, is one of complete separation of the vitreous membrane without local perimacular damage. Though these cases will also have inflow of aqueous in the posterior vitreous detachment area in case of intracapsular surgery, they will not end up with cystoid macular edema. In this context, the explanation for cystoid macular edema therefore is twofold: 1. There is a preset anatomical condition of the macula, in which the premacular bursa has been detached in a relatively unphysiological manner. 2. The aqueous humour entering the posterior vitreous reservoir attacks the retinal capillaries through lesions caused by this unphysiological detachment mechanism. 9. The massive inflow of aqueous in the vitreous cavity in intra capsular aphakia leads to an extensive destruction of the fibrillar elements of the vitreous and to a further increase of the posterior vitreous detachment. This is the ABC effect on the vitreous itself. Normal vitreous detachment starts on the edge of the premacular bursa, in phakic and aphakic eyes. The aphakic condition however, vastly increases the speed and extent of the detachment. Summary Extracapsular surgery is an ideal type of cataract surgery in combination with lens implantation in that stability and fixation of the lens is greatly enhanced. However, a number of complications can be expected. The main problem of extracapsular surgery is posterior capsule opacification. This is due to regeneration of germinal lens fibres. To prevent this a complete removal of cortical lens matter is advisable, even in lens implantation. This however requires special lenses which have additional iris fixation. The author's technique for extracapsular surgery is described. The clinically protective effect of extracapsular surgery for the macula has led to the discovery of a new anatomical structure in front of the macula, the bursa premacularis. The bursa premacularis is a 13
well-defined fluid-filled space inside the vitreous body in front of the macula. It is postulated to have a protective function for the macula in a hydrodynamic and biochemical sense. A number of pathological conditions could be explained as primarily determined by toxic substances in the premacular bursa or defective detachment of the premacular bursa in the course of posterior vitreous detachment. If this latter condition exists, intracapsular surgery will cause cystoid macular edema, as aqueous can enter the perimacular retina. Cystoid macular edema therefore is postulated to be anatomicaIly predetermined. Acknowledgements I am much indebted to Dr. c.c. Kok-van Alphen, Dr. J. Otto, the Lions Eye Bank of Miami, Florida (Mrs. Pearl Goldberg) and Miss Inge Borgers for providing the pathology eyes. Acknowledgement is due to Prof. J.A. Oosterhuis for his suggestion in nomenclature. Mr. K. Otter's help is greatly appreciated. Without the help of Mrs. H. Bloemendaal-Stob, who did the secretarial work, Mrs. D.P. Vos-van Vliet, who did the anatomical dissections and of Mrs. A.M. Worst-van Dam, who gave her invaluable managerial advice. This paper in its entirety has been published as follows: I. II. III. IV.
AIOIS AIOIS AIOIS AIOIS
Jour. Jour. Jour. Jour.
VoL 2 #1 VoL 3 #2 VoL 3 #3 & 4 VoL 4 #1
References 1. Binkhorst, C.D.: Intra-oculaire lens prothese volgens Ridley, Ned. Tijdschr. v. Geneesk. Jaargang 100, No. 48, Dec. 1956. Binkhorst, C.D.: Iris supported artificial pseudophakos. Trans Ophthal. Soc. UK 79:569,1959. Binkhorst, C.D., Leonard, P.A.M.: Results in 208 Iris-Clip Pseudophakos Implantations. Am. J. Ophthal. VoL 64, No. 5,947-956,1967. 2. Binkhorst, C.D., Kats, A., Leonard, P.A.M.: Extracapsular Pseudophakia. Am. J. OphthaL Vol. 73, No.5, 625-636, May 1972. 3. Worst, J .G.F.: Biotoxizitat des Kammerwassers. Klin. MonatsbL Augenheilk. 167 Band, 3 Heft, 1975. 4. Worst, J.G.F., v.d. Heyden, R.: A Simplified Echographic Procedure for Clinical Oculography, BibL ophthaL, No. 83, pp. 269-272, 1975 (Karger-Basel). 5. Alpar J.J.: A new technique to suture the Binkhorst two-loop & four-loop & Fyodorov lenses. Manuscript. 6. Ridley, H.: Intraocular acrylic lenses. Trans OphthaL Soc. UK 71: 617-621, 1951. 7. Gartner, J.: Histologische Beobachtungen tiber das Verhalten der vitreoretinalen Grenzschicht bei Glaskorperabhebung, K1, MonatsbL Augenheilk, 142 (1963) 769-792. 8. Eisner, G.: Biomicroscopy of the peripheral fundus, Springer Verlag, Berlin-Heidelberg - New York, 1973.
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