Symposium: Tumors of the Lids and Orbit f
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ORBITAL SEPTA: ANATOMY AND FUNCTION LEO KOORNNEEF, MD, PHD BY INVITATION
AMSTERDAM, THE NETHERLANDS
As a consequence of some puzzling motility disturbances in patients with blow-out fractures, a new anatomic approach to the human orbit was developed. This new approach revealed unknown connective tissue septa inside the orbit. These connective tissue septa were highly organized and formed an accessory locomotor system. This system is involved in pathologic circumstances like blow-out fractures and can account for the motility disturbances in these cases; additionally, it plays an important, yet to be unravelled, role when normal eye movements are performed.
THis investigation was started after the Orbital Centre in Amsterdam had met with some puzzling motility disturbances in patients with blow-out fractures. According to today' s generally accepted conception, extraocular muscles are trapped in the fracture hole after a blow-out fracture, resulting in diplopia. But are the extraocular muscles indeed trapped in the fracture? If so, the motility Submitted for publication Oct 25, 1978. From the Reconstructive Morphology Team, Department of Anatomy and Embryology, University of Amsterdam, and the Orbital Centre, University Eye Clinic, Wilhelmina Gasthuis, Amsterdam. Presented in combination with the American Society of Ophthalmic Plastic and Reconstructive Surgery at the 1978 Annual Meeting of the American Academy of Ophthalmology, Kansas City, Mo, Oct 22-26. Reprint requests to University Eye Clinic, Wilhelmina Gasthuis, Eerste Helmersstraat 104, 1054 EG Amsterdam, The Netherlands.
disturbances in blow-out fractures of the orbital floor are unexpected. Since the inferior oblique muscle passes between the inferior rectus muscle and the orbital floor, one would expect that if a muscle gets trapped in the fracture, it would be the inferior oblique muscle. In the experience of the Orbital Centre, this has never occurred. On the other hand, one would expect that fractures in the orbital floor situated near the apex would exclusively be the site of incarceration of the inferior rectus muscle. This does occur and is reflected in vertical motility impairment in the upward as well as in the downward gaze and, in particular, in the lateral upward and lateral downward gaze. In the nasal upward and nasal downward gaze, which is mainly governed by the oblique muscles, this vertical motility impairment could be expected to be less pronounced. As stated before, this asymmetric vertical motility disturbance, being characteristic of an incarcerated inferior rectus muscle, was encountered by our orbital center, but very infrequently. The great majority of orbital floor fractures with a prolapsus of orbital contents into the maxillary antrum do show a limitation of the upward gaze and downward gaze in all directions as if the entire complex of inferior rectus and inferior oblique muscles are uniformly trapped.
876
VOLUME 86 MAY 1979
SYMPOSIUM ON ORBITAL DISEASES
The problems we faced were (1) how this phenomenon could be explained, and (2) if an additional anatomic structure could be found that would account for these unexpected and severe motility disturbances as if the inferior rectus and the inferior oblique muscles were trapped together. A search through anatomic literature did not provide an answer, but nevertheless we were struck by the fact that in many anatomic illustrations the bony boundaries of the orbit had been chiseled away or entirely removed.
It should be clear that this procedure precluded an answer to our problem, because our point of interest was precisely the relationship between the orbital contents and the orbital walls. Thus, instead of removing the orbital contents for examination, a technique derived from surgery was used, which approached the orbital contents via the orbital aperture, leaving the bony boundaries and their relationships with the orbital contents intact. This proved to be an extremely good idea. Dissection was performed under a Zeiss operation microscope. With a blepharostat, the eyelids were spread and an incision was made in the conjunctival sack. Connective tissue septa were found between the orbital periorbit and Tenon's capsule, enveloping the eyeball. Some of these septa contained vessels or nerves, or both. These connective tissue septa sprang into view directly after incision of the conjunctiva. Medially below, in the orbit, was a rigid connective tissue mass between the inferior oblique and the inferior rectus muscle. This mass had a striated aspect and it appeared to resist
877
pressure of the forceps even better than other connective tissue septa. A small part was taken out and subjected to histologic processing. It contained smooth muscle cells. Since in the further · process of dissection of the orbital connective tissue the continuities observed had to be broken, the need for a histologic technique grew with deeper penetration. For several technical reasons we decided to make 140w thick histologic serial sections instead of the usual thin 10M serial sections. An advantage of the thick histologic section was accentuation of structures that extend in space in one particular direction, by superposition and overprojection when subjected to light, as a result of their location. Thus, the connective tissue boundaries, which can be easily overlooked in the thin sections, will be readily recognizable walls in the thick section, in which the massivity of the connective tissue septa is emphasized. By this circumstance the connective tissue septa were probably recognized as such histologically for the first time. Histologic processing of complete orbits together with bony boundaries is difficult and requires much time and endurance. Twenty-six human orbits were processed. After perfusion fixation via arterial passing through, followed by an additional fixation for a period of two months, the orbits were separated from the rest of the head. To permit sectioning of the orbital bones together with the orbital contents, EDTA was chosen as decalcification agent. The decalcification process was checked weekly with stereo roentgenographic photography. Dehydration occurred in ethanol. Celloidin (Ceducol) was chosen as an
878
LEO KOORNNEEF
embedding substance. The hardened celloidin blocks were sectioned one at a time on a sledge microtome into 140J.L sections. They were stained in diluted hematoxylin azophloxine (Mayer) solutions and diluted acidic fushsin-picric acid solutions (van Gieson). About six months is required to process one complete orbit. On the one hand were structures identified as septa during dissection, that is, identified by their resistance, and on the other hand, structures identified as septa in the thick sections, that is, identified by histologic criteria. The histologic criteria were condensations of collagenic fibers and fibroblasts running in the same direction with a thickness of at least 0.5 mm. To verify whether these connective tissue septa at various levels in the orbit were uniform and reproducible in different specimens, another less time-consuming and even thicker-section technique was developed. These new series affirmed the existence of bilateral symmetry and interindividual uniformity in human orbital connective tissue. Having proved the uniformity of orbital connective tissue, we wished to gain more spatial information about the course and location of this tissue, and an accurate representation in space was indispensable. Following the reconstruction technique developed by Los, 1 the sections were photographically recorded and enlarged five times. The connective tissue septa were colored in on the photographs with transparent paints. All parts which were not pertinent to the reconstruction were cut
OPHTH
AAO
out. The necessary thickness of the photographic paper was calculated by multiplying the original thickness of the sections by the photographic enlarging factor. The appropriate thickness was reached by affixing polystyrene and pieces of board to the back of the prints. The prints were piled up to form a threedimensional model. These threedimensional models (a reconstruction) enabled us to follow the exact course and location of orbita connective tissue in space. The reconstructions showed that the connective tissue systems of the different eye muscles vary according to which region in the orbit is approached. 2 These differences per region are illustrated in four schematic drawings (Figure). The original question of why, in cases of blow-out fractures of the orbital floor, the vertical motility disturbances nearly always imply incarceration of the inferior rectus and the inferior oblique muscles together can be answered in the following way: The herniation of the orbital contents into the maxillary sinus obviously does not only contain the muscles, but consists of the entire motility apparatus near the orbital floor, that is, the connective tissue septa of the muscles in the fracture region. This does not affect the connective tissue systems of the eye muscles near the orbital floor only, but has additional tractional effects on, for instance, the connective tissue septa of the medial and lateral recti muscles. Preliminary results of a retrospective study show that blow-out fractures of the orbital floor cause different groups of motility disturbances and that these different disturbances can be correlated to and appear to be dependent on the size and the anatomic site of the fracture.
VOLUME 86 MAY 1979
SYMPOSIUM ON ORBITAL DISEASES
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879
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Course of connective tissue septa of eye muscles at different levels in orbit. Top left, Area near orbital apex. Top right, Area halfway between apex and rear surface of eye. Bottom left, Area near rear surface of eyeball. Bottom right, Area near eyeball equator. Key: slp/sr: superior levator palpebrae/superior rectus muscle complex; lrm: lateral rectus muscle; iom: inferior oblique muscle; irm: inferior rectus muscle; mm: Muller's rectus muscle; mrm: medial rectus muscle; som: superior oblique muscle; on: optic nerve.
Thus, orbital connective tissue can be considered an important accessory locomotor mechanism in close cooperation with the eye muscles, the optic nerve, the CNS, the eyeball, the eyelids, the lacrimal gland, and the intraorbital fat, all forming a functional anatomic entity. Literature data support this view. In 1960 Lang, 3 working on the Achilles tendon, described a con-
nective tissue system around this tendon and showed that connective tissue septa rub against each other and against fat cushions during movements. Between these septa. capillary loops run parallel to the septa. We injected low viscosity compounds into orbital vessels and found comparable capillary loops near the connective tissue septa in the human orbit. Furthermore, Lang found large quantities of hyaluronic acid around the Achilles tendon
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LEO KOORNNEEF
septa. Hyaluronic acid is always present where friction and movements occur. Recently, histochemical investigations by Singh 4 have shown large quantities of hyaluronic acid in the human orbit as well. These facts cannot be coincidental and support our view that human orbital connective tissue is involved in pathologic circumstances like blow-out fractures and can account for the motility disturbances in these cases, but additionally plays an important, yet to be unravelled, role when normal eye movements are performed.
OPrlTH
AAO
REFERENCES 1. Los JA: A new method of three-dimensional reconstruction of microscopical structures based on photographic techniques. Acta Morpho! Neerl Scand 8:273-279, 19701971. 2. Koornneef L: Spatial Aspects of Orbital Musculo-fibrous Tissue in Man. Amsterdam, Swets & Zeitlinger, 1977, pp 1-168. 3. Lang V: Ueber das G!itgewebe der Sehnen, Muskeln, Fascien und Gefasse. Anat Entw 122:197-231, 1960. 4. Singh SP, Nikifosak M: The biochemical composition of human retrobulbar connective tissue. Separatum Experientia 32: 395-396, 1976.
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ORBITAL SEPTA: ANATOMY AND FUNCTION LEO KOORNNEEF, MD, PHD BY INVITATION
AMSTERDAM, THE NETHERLANDS
As a consequence of some puzzling motility disturbances in patients with blow-out fractures, a new anatomic approach to the human orbit was developed. This new approach revealed unknown connective tissue septa inside the orbit. These connective tissue septa were highly organized and formed an accessory locomotor system. This system is involved in pathologic circumstances like blow-out fractures and can account for the motility disturbances in these cases; additionally, it plays an important, yet to be unravelled, role when normal eye movements are performed.
THis investigation was started after the Orbital Centre in Amsterdam had met with some puzzling motility disturbances in patients with blow-out fractures. According to today' s generally accepted conception, extraocular muscles are trapped in the fracture hole after a blow-out fracture, resulting in diplopia. But are the extraocular muscles indeed trapped in the fracture? If so, the motility Submitted for publication Oct 25, 1978. From the Reconstructive Morphology Team, Department of Anatomy and Embryology, University of Amsterdam, and the Orbital Centre, University Eye Clinic, Wilhelmina Gasthuis, Amsterdam. Presented in combination with the American Society of Ophthalmic Plastic and Reconstructive Surgery at the 1978 Annual Meeting of the American Academy of Ophthalmology, Kansas City, Mo, Oct 22-26. Reprint requests to University Eye Clinic, Wilhelmina Gasthuis, Eerste Helmersstraat 104, 1054 EG Amsterdam, The Netherlands.
disturbances in blow-out fractures of the orbital floor are unexpected. Since the inferior oblique muscle passes between the inferior rectus muscle and the orbital floor, one would expect that if a muscle gets trapped in the fracture, it would be the inferior oblique muscle. In the experience of the Orbital Centre, this has never occurred. On the other hand, one would expect that fractures in the orbital floor situated near the apex would exclusively be the site of incarceration of the inferior rectus muscle. This does occur and is reflected in vertical motility impairment in the upward as well as in the downward gaze and, in particular, in the lateral upward and lateral downward gaze. In the nasal upward and nasal downward gaze, which is mainly governed by the oblique muscles, this vertical motility impairment could be expected to be less pronounced. As stated before, this asymmetric vertical motility disturbance, being characteristic of an incarcerated inferior rectus muscle, was encountered by our orbital center, but very infrequently. The great majority of orbital floor fractures with a prolapsus of orbital contents into the maxillary antrum do show a limitation of the upward gaze and downward gaze in all directions as if the entire complex of inferior rectus and inferior oblique muscles are uniformly trapped.
876
VOLUME 86 MAY 1979
SYMPOSIUM ON ORBITAL DISEASES
The problems we faced were (1) how this phenomenon could be explained, and (2) if an additional anatomic structure could be found that would account for these unexpected and severe motility disturbances as if the inferior rectus and the inferior oblique muscles were trapped together. A search through anatomic literature did not provide an answer, but nevertheless we were struck by the fact that in many anatomic illustrations the bony boundaries of the orbit had been chiseled away or entirely removed.
It should be clear that this procedure precluded an answer to our problem, because our point of interest was precisely the relationship between the orbital contents and the orbital walls. Thus, instead of removing the orbital contents for examination, a technique derived from surgery was used, which approached the orbital contents via the orbital aperture, leaving the bony boundaries and their relationships with the orbital contents intact. This proved to be an extremely good idea. Dissection was performed under a Zeiss operation microscope. With a blepharostat, the eyelids were spread and an incision was made in the conjunctival sack. Connective tissue septa were found between the orbital periorbit and Tenon's capsule, enveloping the eyeball. Some of these septa contained vessels or nerves, or both. These connective tissue septa sprang into view directly after incision of the conjunctiva. Medially below, in the orbit, was a rigid connective tissue mass between the inferior oblique and the inferior rectus muscle. This mass had a striated aspect and it appeared to resist
877
pressure of the forceps even better than other connective tissue septa. A small part was taken out and subjected to histologic processing. It contained smooth muscle cells. Since in the further · process of dissection of the orbital connective tissue the continuities observed had to be broken, the need for a histologic technique grew with deeper penetration. For several technical reasons we decided to make 140w thick histologic serial sections instead of the usual thin 10M serial sections. An advantage of the thick histologic section was accentuation of structures that extend in space in one particular direction, by superposition and overprojection when subjected to light, as a result of their location. Thus, the connective tissue boundaries, which can be easily overlooked in the thin sections, will be readily recognizable walls in the thick section, in which the massivity of the connective tissue septa is emphasized. By this circumstance the connective tissue septa were probably recognized as such histologically for the first time. Histologic processing of complete orbits together with bony boundaries is difficult and requires much time and endurance. Twenty-six human orbits were processed. After perfusion fixation via arterial passing through, followed by an additional fixation for a period of two months, the orbits were separated from the rest of the head. To permit sectioning of the orbital bones together with the orbital contents, EDTA was chosen as decalcification agent. The decalcification process was checked weekly with stereo roentgenographic photography. Dehydration occurred in ethanol. Celloidin (Ceducol) was chosen as an
878
LEO KOORNNEEF
embedding substance. The hardened celloidin blocks were sectioned one at a time on a sledge microtome into 140J.L sections. They were stained in diluted hematoxylin azophloxine (Mayer) solutions and diluted acidic fushsin-picric acid solutions (van Gieson). About six months is required to process one complete orbit. On the one hand were structures identified as septa during dissection, that is, identified by their resistance, and on the other hand, structures identified as septa in the thick sections, that is, identified by histologic criteria. The histologic criteria were condensations of collagenic fibers and fibroblasts running in the same direction with a thickness of at least 0.5 mm. To verify whether these connective tissue septa at various levels in the orbit were uniform and reproducible in different specimens, another less time-consuming and even thicker-section technique was developed. These new series affirmed the existence of bilateral symmetry and interindividual uniformity in human orbital connective tissue. Having proved the uniformity of orbital connective tissue, we wished to gain more spatial information about the course and location of this tissue, and an accurate representation in space was indispensable. Following the reconstruction technique developed by Los, 1 the sections were photographically recorded and enlarged five times. The connective tissue septa were colored in on the photographs with transparent paints. All parts which were not pertinent to the reconstruction were cut
OPHTH
AAO
out. The necessary thickness of the photographic paper was calculated by multiplying the original thickness of the sections by the photographic enlarging factor. The appropriate thickness was reached by affixing polystyrene and pieces of board to the back of the prints. The prints were piled up to form a threedimensional model. These threedimensional models (a reconstruction) enabled us to follow the exact course and location of orbita connective tissue in space. The reconstructions showed that the connective tissue systems of the different eye muscles vary according to which region in the orbit is approached. 2 These differences per region are illustrated in four schematic drawings (Figure). The original question of why, in cases of blow-out fractures of the orbital floor, the vertical motility disturbances nearly always imply incarceration of the inferior rectus and the inferior oblique muscles together can be answered in the following way: The herniation of the orbital contents into the maxillary sinus obviously does not only contain the muscles, but consists of the entire motility apparatus near the orbital floor, that is, the connective tissue septa of the muscles in the fracture region. This does not affect the connective tissue systems of the eye muscles near the orbital floor only, but has additional tractional effects on, for instance, the connective tissue septa of the medial and lateral recti muscles. Preliminary results of a retrospective study show that blow-out fractures of the orbital floor cause different groups of motility disturbances and that these different disturbances can be correlated to and appear to be dependent on the size and the anatomic site of the fracture.
VOLUME 86 MAY 1979
SYMPOSIUM ON ORBITAL DISEASES
A
879
B
Course of connective tissue septa of eye muscles at different levels in orbit. Top left, Area near orbital apex. Top right, Area halfway between apex and rear surface of eye. Bottom left, Area near rear surface of eyeball. Bottom right, Area near eyeball equator. Key: slp/sr: superior levator palpebrae/superior rectus muscle complex; lrm: lateral rectus muscle; iom: inferior oblique muscle; irm: inferior rectus muscle; mm: Muller's rectus muscle; mrm: medial rectus muscle; som: superior oblique muscle; on: optic nerve.
Thus, orbital connective tissue can be considered an important accessory locomotor mechanism in close cooperation with the eye muscles, the optic nerve, the CNS, the eyeball, the eyelids, the lacrimal gland, and the intraorbital fat, all forming a functional anatomic entity. Literature data support this view. In 1960 Lang, 3 working on the Achilles tendon, described a con-
nective tissue system around this tendon and showed that connective tissue septa rub against each other and against fat cushions during movements. Between these septa. capillary loops run parallel to the septa. We injected low viscosity compounds into orbital vessels and found comparable capillary loops near the connective tissue septa in the human orbit. Furthermore, Lang found large quantities of hyaluronic acid around the Achilles tendon
880
LEO KOORNNEEF
septa. Hyaluronic acid is always present where friction and movements occur. Recently, histochemical investigations by Singh 4 have shown large quantities of hyaluronic acid in the human orbit as well. These facts cannot be coincidental and support our view that human orbital connective tissue is involved in pathologic circumstances like blow-out fractures and can account for the motility disturbances in these cases, but additionally plays an important, yet to be unravelled, role when normal eye movements are performed.
OPrlTH
AAO
REFERENCES 1. Los JA: A new method of three-dimensional reconstruction of microscopical structures based on photographic techniques. Acta Morpho! Neerl Scand 8:273-279, 19701971. 2. Koornneef L: Spatial Aspects of Orbital Musculo-fibrous Tissue in Man. Amsterdam, Swets & Zeitlinger, 1977, pp 1-168. 3. Lang V: Ueber das G!itgewebe der Sehnen, Muskeln, Fascien und Gefasse. Anat Entw 122:197-231, 1960. 4. Singh SP, Nikifosak M: The biochemical composition of human retrobulbar connective tissue. Separatum Experientia 32: 395-396, 1976.
