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Oculomotor Palsy Due to Supraclinoid Internal Carotid Artery Berry Aneurysm*
609
MACULAR PROJECTION IN LATERAL GENICULATE
2. Polyak, S.: T h e Vertebrate V i s u a l S y s t e m . Chicago, U n i v . C h i c a g o P r e s s , 1957, pp. 334-353. 3. R0nne, H . : Pathologish-anatomishe U n t e r s u c h u n g e n über alkoholishe intoxikationamblyopie. A r c h , f. Ophth., 7 7 : 1 - 9 5 , 1 9 1 0 . 4. —: Z u r pathologishen A n a t o m i e d e r diabetishen intoxikationamblyopie. A r c h . f. O p h t h , 8 5 : 4 8 9 537, 1913. 5. : D i e anatomishe P r o j e k t i o n der M a c u l a im Corpus Geniculatum ext., Ztschr. NeuroL & Psychia't, 2 2 : 4 6 9 - 4 8 5 , 1914. 6. Juba, A , and S z a t m â r i , Α . : U e b e r seltene hirnanatomishe B e f u n d e in Fällen v o n einseitiger peripherer Blindheit. Klin. Monatsbl. f. A u g e n h , 9 9 : 1 7 3 - 1 8 8 , 1 9 3 7 . 7. Rjfane, H . : D i e Architektur der menschlichen Sehbahn. A c t e o p h t h , 2 1 : 1 3 7 - 1 8 9 , 1943. 8. P o l y a k , S . : T h e Vertebrate V i s u a l S y s t e m . Chicago, U n i v . C h i c a g o P r e s s , 1957, pp. 695-759. 9. Victor, M , Mancall, E . L , and D r e y f u s , P . M . : Deficiency amblyopia in the alcoholic patient: A clinicopathologic study. Α Μ Α . A r c h . O p h t h , 6 4 : 1 - 3 3 , 1960. 10. Ballantyne, A . J.: T h e nerve fiber pattern o f the h u m a n retina. T r . Ophth. Soc. U . Kingdom, 6 6 : 179-191, 1946.
OCULOMOTOR
PALSY
CAROTID A
DUE
TO
ARTERY
SUPRACLINOID
BERRY
LONG-TERM STUDY OF T H E RESULTS OF SURGICAL TREATMENTS ON T H E RECOVERY OF THIRD-NERVE
Ε. H.
INTERNAL
ANEURYSM*
BOTTERELL, M . D . ,
L. A.
LLOYD, M . D . ,
FUNCTION
AND H .
J. HOFFMAN,
M.D.
Toronto, Ontario During the years 1938 to 1961, 40 patients with oculomotor palsy due to angiographically verified berry aneurysms, supraclinoid in situation, on the internal carotid artery were admitted to the Toronto General Hospital. These patients were treated by common carotid ligation in the neck, by direct intracranial clipping of the aneurysm or by conservative management. It is our purpose to evaluate the effect of these forms of management on the recovery of third-nerve function. A N A L Y S I S OF T H E MATERIAL
Four cases of oculomotor palsy due to subclinoid internal carotid artery aneurysms have been excluded from this series because these aneurysms produced total ophthalmoplegia. The one case of oculomotor palsy due to a posterior cerebral artery aneurysm was omitted as was one case due to an aneu* F r o m the Departments of O p h t h a l m o l o g y and S u r g e r y of the U n i v e r s i t y of T o r o n t o , and the Neurosurgical U n i t and Department of Ophthalm o l o g y of the T o r o n t o General Hospital.
rysm arising at the bifurcation of the internal carotid artery. The cases under consideration consist entirely of supraclinoid internal carotid artery aneurysms, angiographically verified, arising at the level of the origin of the posterior communicating artery. Those cases which were not adequately,followed after treatment are excluded together with those with third-nerve signs so slight as to be considered insignificant. The period of follow-up on the 40 patients ranged between three months and 10 years after treatment. Because of the recent advances in surgery of intracranial berry aneurysms, most of pur cases were seen in later years. Only ,fpur cases were seen between 1938 and 1949 ; seven cases between 1950 and 1954 and 29 cases between 1955 and 1961. Four patients were treated conservatively because of their age, their general condition or because local conditions made surgery ill advisable. Eight patients were treated by carotid ligation in the neck, this form of treatment being resorted to infrequently in
610
Ε . Η . B O T T E R E L L , L. Α . L L O Y D A N D Η . J. H O F F M A N TABLE 1
DURATION 40
OF
FOLLOW-UP
PATIENTS
WITH
Interval between Treatment & F o l l o w - u p 3 mo. to 6 mo. 6 mo. to 2 yr. 2 yr. to 6 yr. 6 yr. to 10 yr. Postoperative deaths
AFTER
PATHOLOGY TREATMENT
OCULOMOTOR
IN
PALSY
N o . of Patients 13 8 8 5 6
recent years. Twenty-eight patients were treated by intracranial clipping of the aneurysmal neck. Thirty-five of the patients were women and five were men. This striking female sex predominance was most surprising for in our total series of aneurysms females comprised 55 percent of the total.
Forty cases had supraclinoid berry aneurysms arising from the internal carotid artery at the level of the posterior communicating artery branch. Five patients had other berry aneurysms besides the. one responsible for the oculomotor palsy and of these, three had contralateral supraclinoid internal carotid artery aneurysms (one of these three cases as well had subclinoid internal carotid and anterior communicating artery aneurysms) ; one patient had an additional single middle cerebral artery aneurysm and one patient had bilateral middle cerebral artery aneurysms. These supraclinoid aneurysms conformed to Jefferson's classic description. They lay 1
F i g . 1 (Botterell, Lloyd and H o f f m a n ) . Carotid arteriograms of patients with supraclinoid internal carotid artery aneurysms s h o w i n g the postero-inferior direction that these aneurysms take and the variability in their size and shape.
O C U L O M O T O R
P A L S Y
either above or below the posterior communicating artery and were directed posteriorly, inferiorly and laterally (fig. 1 ) . The aneurysms were usually small, the fundus of the aneurysm dipping under the free edge of
D U E
T O
611
A N E U R Y S M
T A B L E ACE
INCIDENCE
PALSY
OF 40
2
PATIENTS
DUE TO SUPRACUNOID
WITH BERRY
OCULOMOTOR ANEURYSM
Age (Yr.)
N o . of Patients
20^29 30-39 40-49 50-59 60-69
5 ~ 13 7 13 2
the tentorium. The third nerve was usually flattened along the wall of the aneurysmal sac, lying above, medial to or below the aneurysm (fig. 2 ) . The third nerve was never seen at operation in the usual supratentorial approach to the aneurysm. When large enough, supraclinoid aneurysms could compress the optic tract above or the fourth, fifth and sixth cranial nerves in the cavernous sinus below. Hyland and Barnett stated that these berry aneurysms usually produced oculomotor palsy by hemorrhage locally in the third nerve. Twenty-five patients had subarachnoid hemorrhage, showing blood in their spinal fluid. Although the remaining 15 cases had clear cerebrospinal fluid, some had local subarachnoid hemorrhage in the region of the third nerve, as judged by the presence of old blood staining of pia and arachnoid seen at operation. Confirmation of hemorrhage into the fibers of the third nerve was possible in some of the cases coming to autopsy but was impossible at operation because the fundus of the aneurysm and the third nerve were both out of sight under the tentorial edge. 2
F i g . 2 (Botterell, L l o y d and H o f f m a n ) . S p e c i men illustrating the relationship between supraclinoid internal carotid artery a n e u r y s m and the surrounding I I , I I I and V cranial nerves, ( a ) Optic chiasma. ( b ) Supraclinoid internal carotid artery aneurysm, ( c ) V* cranial nerve, ( d ) I I I cranial nerve. T h e third nerve is seen t o be flattened along the superior surface o f the aneurysm and actually incorporated in the a n e u r y s m wall. V is seen t o be flattened along the inferior surface o f the aneurysm. T h e aneurysm, w h i c h has t w o silver clips across its neck, is seen t o b e elevating the optic chiasm.
Acute dilatation of the aneurysmal sac causing pressure on the third nerve appeared to be responsible for some cases of oculomotor palsy in which no evidence of bleeding was found in the cerebrospinal fluid or at operation. Several of the cases showed, at autopsy, evidence of stretching and flattening of the oculomotor nerve with changes of a rather chronic nature in spite of a rela-
612
Ε.
Η.
BOTTERELL,
T A B L E
L. Α .
L L O Y D
3
INVOLVEMENT OF OTHER CRANIAL NERVES Cranial N e r v e Involved
N o . of Patients
I I ( h o m o n y m o u s hemianopia due to compression of ipsilateral optic tract) 1 IV 1 V (numbness) S V ' - V (numbness) 2 V ' - V (numbness) 1 V'-V - V VI ! 1 TOTAL 11 1
2
3
2
s
1
tively short history of disturbed third nerve function. SIGNS
AND
SYMPTOMS
Oculomotor palsy. Complete third-nerve palsy existed in 25 patients. Fifteen had a partial third-nerve palsy. Partial palsies were termed slight when the pupil was slightly enlarged, ptosis was minimal and there was more than 15 degrees of muscle movement. Moderate third-nerve palsy included those cases with less than 15 degrees of muscle movement, a fully dilated pupil or severe ptosis and yet without a complete palsy. The patients with both slight and moderate deficits were disabled by diplopia. Frequently in those with slight deficits the diplopia was more troublesome because there was less tendency to suppress the second image. Three of the partial third nerve palsies were slight and 12 were moderate. The onset of impaired oculomotor function was sudden in 24 cases ; in seven cases the palsy developed over a period of hours ; in nine over one to several days. In half the cases of gradual onset, ptosis was the presenting sign and in the rest diplopia was noted first by the patient. Visual blurring for near vision (one m.) was a common complaint and this was due to the loss of accommodation, for vision was usually normal at six m. Some of the patients noticed intermittent visual blurring for a few days before the palsy was established. Photophobia was a common complaint.
A N D
Η.
J.
H O F F M A N
Headache was a prominent symptom in all our patients. Thirty-four patients had local pain in the distribution of the first division of the fifth cranial nerve. The pain was characteristically in and about the ipsilateral eye. In a few patients who were well enough to localize accurately their headache, pain was also felt in the ipsilateral frontal region, along the inner canthus of the ipsilateral eye and along the ipsilateral side of the nose. Jefferson stated that this local headache was characteristic of aneurysmal compression of the third nerve and was probably due to stimulation of the upper border of the cavernous sinus to which the aneurysmal sac frequently became adherent. 1
In 25 patients the headaches were associated with subarachnoid hemorrhage. Six of this group had their pain in the occipital region presumably due to blood in the basal cisterns. Nineteen patients with subarachnoid hemorrhage had localized retro-orbital headaches and two of these were of special interest since their headache preceded their subarachnoid hemorrhage, being present intermittently for three years in one case, and for five days in the other. The remaining 15 patients had local retro-orbital pain without subarachnoid hemorrhage. Involvement of other cranial nerves beside the oculomtor nerve was relatively common, occurring in 11 cases. Neurologic deficits aside from the cranial nerve involvement were relatively uncommon. Twenty-three of the patients had no other focal neurologic signs; 10 had minor signs, such as an extensor plantar response or some minimal limb weakness; and seven had major signs such as hemiplegia or mental deterioration. Eight of the patients were transiently comatose at the time of subarachnoid hemorrhage and eight patients had transient periods of disturbance of mental function. RESULTS
OF
TREATMENT
The effect of treatment on the third-nerve palsy was analyzed from the point of view
OCULOMOTOR PALSY DUE TO
ANEURYSM
613
HL NERVE PALSY
^
Carotid ligation.in neck
finit ial C s complete Ipalsy. (initial M < moderate Ideficit. finit ial S
ο «
complete palsy. moderate deficit.
ο
ο
3 C
M
6-9
S
slight deficit.
•
full recovery.
months Interval: onset oculomotor palsy and treatment F i g . 3 (Botterell, Lloyd and H o f f m a n ) . T h i s chart s h o w s the effect of the interval between onset of the third-nerve palsy and time of treatment on the results of treatment analyzed f r o m the point of v i e w of type of oculomotor palsy—initially and after treatment. T y p e s of oculomotor palsies: C o m p l e t e ; moderate—less than IS degrees muscle movement, a fully dilated pupil o r severe p t o s i s ; slight—more than 15 degrees muscle movement, slight enlargement of pupil and minimal ptosis. T h e top graph illustrates the results in the group treated by carotid ligation in the neck. T h e bottom graph illustrates the results in those treated by intracranial clipping of the aneurysm.
of the type of treatment used, the interval between the onset of third nerve palsy and the time of treatment, and the type of oculomotor paresis, that is, whether it was complete, moderate or slight ; moderate meaning less than 15 degrees ocular movement, a fully dilated pupil or severe ptosis; slight meaning more than 15 degrees muscle movement, slight enlargement of pupil and minimal ptosis. Our control group of untreated cases is necessarily small (four cases) because the
majority of conservatively treated cases did not have angiographic verification of their aneurysm and so were not included in our series. INTRACRANIAL CLIPPING (fig.
3)
Twenty-eight patients were treated by intracranial clipping of their aneurysm. Seven patients with a complete third-nerve palsy were so treated during the first 10 days of the onset of their third-nerve palsy. Three made a complete recovery of third-nerve
614
Ε. Η . B O T T E R E L L , L. Α . L L O Y D A N D Η . J. H O F F M A N
function, one was left with a slight deficit of third-nerve function, two were left with a moderate deficit and one patient died. Five patients with a moderate deficit of third-nerve function were operated on during the first 10 days ; three made a full recovery, one being left with only a slight deficit and one patient dying. W e are including a case report of one of the patients in this group who made a rapid and complete recovery. Mrs. M. G. T h i s 32-year-old h o u s e w i f e w a s admitted to the T o r o n t o General Hospital on D e c e m ber 1, 1956, w i t h a three-week history of severe left retro-orbital pain. D u r i n g the t w o days prior to admission, she noted photophobia, diplopia and increasing left ptosis. O n examination she w a s bright and alert with n o neck stiffness. S h e had an incomplete left third-nerve palsy, moderate in nature, with less than 15 degrees of elevation, depression and adduction, almost complete ptosis and a dilated left pupil w h i c h reacted sluggishly to light. S h e w a s otherwise neurologically normal. Bilateral carotid arteriograms w e r e done and revealed a left supraclinoid internal carotid artery aneurysm arising at the origin of the posterior communicating artery. F o r t y - e i g h t hours after admission a left frontotemporal bone flap w a s turned under hypothermia and the neck of the aneurysm clipped. Immediately postoperatively the third-nerve palsy began to improve s o that at the time of her discharge 10 days later she had only some residual left ptosis and superior rectus weakness. H e r remaining third-nerve paresis completely recovered in the n e x t four w e e k s and she has been perfectly well since then.
Two patients with slight deficits of thirdnerve function were operated on during the first 10 days. One died and one remained with a slight third-nerve deficit. Nine patients with complete third-nerve palsies were operated on between 10 days and one month ; none made a complete recovery, seven were left with moderate deficits of third-nerve function and two died. Two patients with a moderate deficit were operated on between 10 days and one month. One fully recovered, the other died. One patient with a slight deficit of third-nerve function was operated on between 10 days and one month and made a full recovery. Two patients with complete third-nerve palsies were operated on between one and
six months following onset of their palsy, both of these patients were left with moderate deficits of third-nerve function. Of the 28 patients treated by direct intracranial clipping of their aneurysmal neck, six died, eight showed complete recovery of third-nerve function and, in 14 cases, a partial deficit of third-nerve function persisted. CAROTID LIGATION
(fig.
3)
Eight patients were treated by common carotid ligation in the neck. One patient with a moderate deficit was operated on within the first 24 hours of onset and recovered to the point of having only a slight deficit. One patient with a moderate deficit of third-nerve function was operated on between 10 days and one month and was left with a slight deficit. Three patients with a complete third-nerve palsy were operated on between one and six months ; two were left with a moderate deficit and one with a slight deficit of thirdnerve function. One patient with a moderate deficit was operated on between one and six months and was left with a slight deficit. One patient with a complete third-nerve palsy was operated on between six and nine months and was left unchanged. One patient with a moderate deficit operated on between six and nine months was left with a slight deficit. Recovery of third-nerve function was incomplete in the eight patients treated by cervical ligation of the carotid. The period of follow-up after treatment in this group ranged between six months and six years, the mean interval being three years. Jefferson reported failure of full recovery in 23 cases that he treated by cervical carotid ligation and this is confirmed by our experience. Furthermore, diplopia is most troublesome in the cases left with a slight deficit. 1
CONSERVATIVE
TREATMENT
Four patients were left untreated surgically because of their age, their general con-
OCULOMOTOR PALSY D U E TO A N E U R Y S M
dition or because local conditions contraindicated operation. Three of these patients had a complete third-nerve palsy, two remained unchanged and one improved to the state of being left with a moderate deficit. One patient had a moderate deficit initially and this remained unchanged. None of these patients died and all were free of neurologic deficits aside from their third-nerve lesions. Recovery of third-nerve function showed a fairly constant course. The superior rectus muscle was the slowest to recover and the patients who did not achieve full recovery were usually left with a deficit in elevation of the globe. The medial rectus muscle usually showed good recovery, the inferior rectus muscle recovering to a lesser extent. Most of the patients recovered fairly good function in their levator palpebrae as well as some pupillary reaction to light. Recovery of thirdnerve function started frequently within days of treatment and in some cases was complete within weeks of treatment. In most cases it took months for full recovery to take place ; the patients who achieved full recovery usually did so within three months of treatment. However, some patients took as long as a year before achieving maximum recovery. The phenomenon of aberrant regeneration as described by Walsh in the recovering third nerve was observed in only two cases. Headache was completely relieved in patients treated by carotid ligation and by direct attack on the aneurysm. Patients left untreated usually had improvement in their headache of a more gradual nature. 3
DISCUSSION
Complete recovery of oculomotor function was not seen in our group of eight patients treated by carotid ligation in the neck and was not seen by Jefferson in his 23 cases treated by carotid ligation in the neck. By contrast, eight of the 28 patients treated by intracranial clipping of their aneurysm showed a complete recovery of third-nerve function. The interval between the onset of third1
615
nerve dysfunction and the time of treatment was a very significant factor in the recovery of third-nerve function. Six of the 14 patients treated by intracranial clipping of the aneurysm within the first 10 days of onset of the third-nerve dysfunction made a complete recovery. Only two of the 14 cases treated beyond 10 days made a complete recovery of third-nerve function and neither of these two had a complete third-nerve palsy initially. Thus, complete third-nerve palsy in our series recovered fully only if treated by direct intracranial attack on the aneurysms within the first 10 days of the onset of their third-nerve paralysis. Partial recovery of third-nerve function was seen in patients treated months after the onset of third-nerve dysfunction and was seen as well in one of the four patients who received no treatment at all. In our particular series, it is difficult to compare the group treated by intracranial clipping with the group treated by carotid ligation because the latter group is small and most of the cases were treated beyond one month after onset of the third-nerve palsy. The apparently high mortality rate of those treated by direct attack on the aneurysm is explained by the fact that several of these patients were very ill at the time of operation. SUMMARY
1. Forty cases of oculomotor palsy due to angiographically verified supraclinoid internal carotid artery berry aneurysms are reviewed. 2. Twenty-five of these patients had subarachnoid hemorrhage associated with the onset of the third-nerve palsy. 3. There were 35 females and five males in this group. 4. Twenty-eight of the patients were treated by intracranial clipping of the aneurysm and eight of these made a complete recovery of third-nerve function. Eight patients were treated by carotid ligation in the
616
Ε.
Η.
B O T T E R E L L ,
L.
Α.
L L O Y D
A N D
Η.
J.
H O F F M A N
ping of the aneurysm is undertaken soon after the onset of oculmotor palsy. Other forms of treatment are much less effective in restoring third-nerve function. Toronto General Hospital.
neck and none of these recovered full function of their third nerve. Four patients were treated conservatively because of age or general state and none of these fully recovered function of their third nerve. CONCLUSION
ACKNOWLEDGMENTS
W e w i s h to e x p r e s s our gratitude to D r s . W . M. Lougheed and T. P . M o r l e y for permission t o include the records of their patients, and to Prof. T. O l s z e w s k i of the Department of Neuropathology, U n i v e r s i t y of T o r o n t o , for making available his autopsy studies.
Full recovery of third-nerve function following oculomotor palsy due to supraclinoid internal carotid berry aneurysms is likely to occur only if treatment by intracranial clip-
REFERENCES 1. Jefferson, G.: Isolated oculomotor palsy caused by intracranial aneurysm. Proc. Roy. Soc. M e d , 4 0 : 419, 1946. 2. H y l a n d , Η . H , and H . J. M . Barnett: T h e pathogenesis of cranial nerve palsies associated with intracranial aneurysms. P r o c . Roy. Soc. M e d , 4 7 : 1 4 1 , 1954. 3. W a l s h , F . B . : Clinical N e u r o - O p h t h a l m o l o g y . Baltimore, W i l l i a m s & W i l k i n s , 1957, ed. 2, p. 833.
HOMONYMOUS A
HEMIANOPIA*
REVIEW OF ONE HUNDRED J.
LAWTON Durham,
SMITH,
North
Quantitative perimetry is a clinical examination essential to proper evaluation of the neurologic patient. To emphasize the fundamental role of quantitative study of the visual fields in topical neurologic diagnosis, the following review of 100 cases of homonymous hemianopia is presented. MATERIAL
One hundred cases with homonymous visual field defects were selected for review from records of patients seen in neuroophthalmologic consultation over two and one-half years. Criteria for selection were: ( 1 ) visual field examination must have been done by me in each instance, ( 2 ) the defect must have been present at the time of examination, and ( 3 ) the patient had to be ex* F r o m the D i v i s i o n of Ophthalmology, D u k e U n i v e r s i t y School of Medicine. T h i s study w a s supported in part by U . S . Public H e a l t h Service Grant 81-1656.
CASES
M.D.
Carolina
amined at both the perimeter and tangent screen (confrontation fields alone were insufficient). Conventional tangent screen techniques were used and an Aimark projection perimeter was employed for peripheral field examinations. It should be noted that a common cause of homonyous field defects, ophthalmic migraine, was thus eliminated from consideration for, although many migraine patients give vivid histories of hemianopias, it is infrequent for these defects to be present at the time of the perimetric examination. The cases here considered are primarily those which would be seen in consultation by an ophthalmologist. The records were analyzed for the following data: age, sex, race, chief complaint, duration of complaint, visual acuity, visual field findings, measurements of palpebral fissures and pupils, optokinetic responses, ophthalmoscopic findings, ophthalmodynamometry, neurologic findings, results of arteriog-
MACULAR PROJECTION IN LATERAL GENICULATE
2. Polyak, S.: T h e Vertebrate V i s u a l S y s t e m . Chicago, U n i v . C h i c a g o P r e s s , 1957, pp. 334-353. 3. R0nne, H . : Pathologish-anatomishe U n t e r s u c h u n g e n über alkoholishe intoxikationamblyopie. A r c h , f. Ophth., 7 7 : 1 - 9 5 , 1 9 1 0 . 4. —: Z u r pathologishen A n a t o m i e d e r diabetishen intoxikationamblyopie. A r c h . f. O p h t h , 8 5 : 4 8 9 537, 1913. 5. : D i e anatomishe P r o j e k t i o n der M a c u l a im Corpus Geniculatum ext., Ztschr. NeuroL & Psychia't, 2 2 : 4 6 9 - 4 8 5 , 1914. 6. Juba, A , and S z a t m â r i , Α . : U e b e r seltene hirnanatomishe B e f u n d e in Fällen v o n einseitiger peripherer Blindheit. Klin. Monatsbl. f. A u g e n h , 9 9 : 1 7 3 - 1 8 8 , 1 9 3 7 . 7. Rjfane, H . : D i e Architektur der menschlichen Sehbahn. A c t e o p h t h , 2 1 : 1 3 7 - 1 8 9 , 1943. 8. P o l y a k , S . : T h e Vertebrate V i s u a l S y s t e m . Chicago, U n i v . C h i c a g o P r e s s , 1957, pp. 695-759. 9. Victor, M , Mancall, E . L , and D r e y f u s , P . M . : Deficiency amblyopia in the alcoholic patient: A clinicopathologic study. Α Μ Α . A r c h . O p h t h , 6 4 : 1 - 3 3 , 1960. 10. Ballantyne, A . J.: T h e nerve fiber pattern o f the h u m a n retina. T r . Ophth. Soc. U . Kingdom, 6 6 : 179-191, 1946.
OCULOMOTOR
PALSY
CAROTID A
DUE
TO
ARTERY
SUPRACLINOID
BERRY
LONG-TERM STUDY OF T H E RESULTS OF SURGICAL TREATMENTS ON T H E RECOVERY OF THIRD-NERVE
Ε. H.
INTERNAL
ANEURYSM*
BOTTERELL, M . D . ,
L. A.
LLOYD, M . D . ,
FUNCTION
AND H .
J. HOFFMAN,
M.D.
Toronto, Ontario During the years 1938 to 1961, 40 patients with oculomotor palsy due to angiographically verified berry aneurysms, supraclinoid in situation, on the internal carotid artery were admitted to the Toronto General Hospital. These patients were treated by common carotid ligation in the neck, by direct intracranial clipping of the aneurysm or by conservative management. It is our purpose to evaluate the effect of these forms of management on the recovery of third-nerve function. A N A L Y S I S OF T H E MATERIAL
Four cases of oculomotor palsy due to subclinoid internal carotid artery aneurysms have been excluded from this series because these aneurysms produced total ophthalmoplegia. The one case of oculomotor palsy due to a posterior cerebral artery aneurysm was omitted as was one case due to an aneu* F r o m the Departments of O p h t h a l m o l o g y and S u r g e r y of the U n i v e r s i t y of T o r o n t o , and the Neurosurgical U n i t and Department of Ophthalm o l o g y of the T o r o n t o General Hospital.
rysm arising at the bifurcation of the internal carotid artery. The cases under consideration consist entirely of supraclinoid internal carotid artery aneurysms, angiographically verified, arising at the level of the origin of the posterior communicating artery. Those cases which were not adequately,followed after treatment are excluded together with those with third-nerve signs so slight as to be considered insignificant. The period of follow-up on the 40 patients ranged between three months and 10 years after treatment. Because of the recent advances in surgery of intracranial berry aneurysms, most of pur cases were seen in later years. Only ,fpur cases were seen between 1938 and 1949 ; seven cases between 1950 and 1954 and 29 cases between 1955 and 1961. Four patients were treated conservatively because of their age, their general condition or because local conditions made surgery ill advisable. Eight patients were treated by carotid ligation in the neck, this form of treatment being resorted to infrequently in
610
Ε . Η . B O T T E R E L L , L. Α . L L O Y D A N D Η . J. H O F F M A N TABLE 1
DURATION 40
OF
FOLLOW-UP
PATIENTS
WITH
Interval between Treatment & F o l l o w - u p 3 mo. to 6 mo. 6 mo. to 2 yr. 2 yr. to 6 yr. 6 yr. to 10 yr. Postoperative deaths
AFTER
PATHOLOGY TREATMENT
OCULOMOTOR
IN
PALSY
N o . of Patients 13 8 8 5 6
recent years. Twenty-eight patients were treated by intracranial clipping of the aneurysmal neck. Thirty-five of the patients were women and five were men. This striking female sex predominance was most surprising for in our total series of aneurysms females comprised 55 percent of the total.
Forty cases had supraclinoid berry aneurysms arising from the internal carotid artery at the level of the posterior communicating artery branch. Five patients had other berry aneurysms besides the. one responsible for the oculomotor palsy and of these, three had contralateral supraclinoid internal carotid artery aneurysms (one of these three cases as well had subclinoid internal carotid and anterior communicating artery aneurysms) ; one patient had an additional single middle cerebral artery aneurysm and one patient had bilateral middle cerebral artery aneurysms. These supraclinoid aneurysms conformed to Jefferson's classic description. They lay 1
F i g . 1 (Botterell, Lloyd and H o f f m a n ) . Carotid arteriograms of patients with supraclinoid internal carotid artery aneurysms s h o w i n g the postero-inferior direction that these aneurysms take and the variability in their size and shape.
O C U L O M O T O R
P A L S Y
either above or below the posterior communicating artery and were directed posteriorly, inferiorly and laterally (fig. 1 ) . The aneurysms were usually small, the fundus of the aneurysm dipping under the free edge of
D U E
T O
611
A N E U R Y S M
T A B L E ACE
INCIDENCE
PALSY
OF 40
2
PATIENTS
DUE TO SUPRACUNOID
WITH BERRY
OCULOMOTOR ANEURYSM
Age (Yr.)
N o . of Patients
20^29 30-39 40-49 50-59 60-69
5 ~ 13 7 13 2
the tentorium. The third nerve was usually flattened along the wall of the aneurysmal sac, lying above, medial to or below the aneurysm (fig. 2 ) . The third nerve was never seen at operation in the usual supratentorial approach to the aneurysm. When large enough, supraclinoid aneurysms could compress the optic tract above or the fourth, fifth and sixth cranial nerves in the cavernous sinus below. Hyland and Barnett stated that these berry aneurysms usually produced oculomotor palsy by hemorrhage locally in the third nerve. Twenty-five patients had subarachnoid hemorrhage, showing blood in their spinal fluid. Although the remaining 15 cases had clear cerebrospinal fluid, some had local subarachnoid hemorrhage in the region of the third nerve, as judged by the presence of old blood staining of pia and arachnoid seen at operation. Confirmation of hemorrhage into the fibers of the third nerve was possible in some of the cases coming to autopsy but was impossible at operation because the fundus of the aneurysm and the third nerve were both out of sight under the tentorial edge. 2
F i g . 2 (Botterell, L l o y d and H o f f m a n ) . S p e c i men illustrating the relationship between supraclinoid internal carotid artery a n e u r y s m and the surrounding I I , I I I and V cranial nerves, ( a ) Optic chiasma. ( b ) Supraclinoid internal carotid artery aneurysm, ( c ) V* cranial nerve, ( d ) I I I cranial nerve. T h e third nerve is seen t o be flattened along the superior surface o f the aneurysm and actually incorporated in the a n e u r y s m wall. V is seen t o be flattened along the inferior surface o f the aneurysm. T h e aneurysm, w h i c h has t w o silver clips across its neck, is seen t o b e elevating the optic chiasm.
Acute dilatation of the aneurysmal sac causing pressure on the third nerve appeared to be responsible for some cases of oculomotor palsy in which no evidence of bleeding was found in the cerebrospinal fluid or at operation. Several of the cases showed, at autopsy, evidence of stretching and flattening of the oculomotor nerve with changes of a rather chronic nature in spite of a rela-
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Η.
BOTTERELL,
T A B L E
L. Α .
L L O Y D
3
INVOLVEMENT OF OTHER CRANIAL NERVES Cranial N e r v e Involved
N o . of Patients
I I ( h o m o n y m o u s hemianopia due to compression of ipsilateral optic tract) 1 IV 1 V (numbness) S V ' - V (numbness) 2 V ' - V (numbness) 1 V'-V - V VI ! 1 TOTAL 11 1
2
3
2
s
1
tively short history of disturbed third nerve function. SIGNS
AND
SYMPTOMS
Oculomotor palsy. Complete third-nerve palsy existed in 25 patients. Fifteen had a partial third-nerve palsy. Partial palsies were termed slight when the pupil was slightly enlarged, ptosis was minimal and there was more than 15 degrees of muscle movement. Moderate third-nerve palsy included those cases with less than 15 degrees of muscle movement, a fully dilated pupil or severe ptosis and yet without a complete palsy. The patients with both slight and moderate deficits were disabled by diplopia. Frequently in those with slight deficits the diplopia was more troublesome because there was less tendency to suppress the second image. Three of the partial third nerve palsies were slight and 12 were moderate. The onset of impaired oculomotor function was sudden in 24 cases ; in seven cases the palsy developed over a period of hours ; in nine over one to several days. In half the cases of gradual onset, ptosis was the presenting sign and in the rest diplopia was noted first by the patient. Visual blurring for near vision (one m.) was a common complaint and this was due to the loss of accommodation, for vision was usually normal at six m. Some of the patients noticed intermittent visual blurring for a few days before the palsy was established. Photophobia was a common complaint.
A N D
Η.
J.
H O F F M A N
Headache was a prominent symptom in all our patients. Thirty-four patients had local pain in the distribution of the first division of the fifth cranial nerve. The pain was characteristically in and about the ipsilateral eye. In a few patients who were well enough to localize accurately their headache, pain was also felt in the ipsilateral frontal region, along the inner canthus of the ipsilateral eye and along the ipsilateral side of the nose. Jefferson stated that this local headache was characteristic of aneurysmal compression of the third nerve and was probably due to stimulation of the upper border of the cavernous sinus to which the aneurysmal sac frequently became adherent. 1
In 25 patients the headaches were associated with subarachnoid hemorrhage. Six of this group had their pain in the occipital region presumably due to blood in the basal cisterns. Nineteen patients with subarachnoid hemorrhage had localized retro-orbital headaches and two of these were of special interest since their headache preceded their subarachnoid hemorrhage, being present intermittently for three years in one case, and for five days in the other. The remaining 15 patients had local retro-orbital pain without subarachnoid hemorrhage. Involvement of other cranial nerves beside the oculomtor nerve was relatively common, occurring in 11 cases. Neurologic deficits aside from the cranial nerve involvement were relatively uncommon. Twenty-three of the patients had no other focal neurologic signs; 10 had minor signs, such as an extensor plantar response or some minimal limb weakness; and seven had major signs such as hemiplegia or mental deterioration. Eight of the patients were transiently comatose at the time of subarachnoid hemorrhage and eight patients had transient periods of disturbance of mental function. RESULTS
OF
TREATMENT
The effect of treatment on the third-nerve palsy was analyzed from the point of view
OCULOMOTOR PALSY DUE TO
ANEURYSM
613
HL NERVE PALSY
^
Carotid ligation.in neck
finit ial C s complete Ipalsy. (initial M < moderate Ideficit. finit ial S
ο «
complete palsy. moderate deficit.
ο
ο
3 C
M
6-9
S
slight deficit.
•
full recovery.
months Interval: onset oculomotor palsy and treatment F i g . 3 (Botterell, Lloyd and H o f f m a n ) . T h i s chart s h o w s the effect of the interval between onset of the third-nerve palsy and time of treatment on the results of treatment analyzed f r o m the point of v i e w of type of oculomotor palsy—initially and after treatment. T y p e s of oculomotor palsies: C o m p l e t e ; moderate—less than IS degrees muscle movement, a fully dilated pupil o r severe p t o s i s ; slight—more than 15 degrees muscle movement, slight enlargement of pupil and minimal ptosis. T h e top graph illustrates the results in the group treated by carotid ligation in the neck. T h e bottom graph illustrates the results in those treated by intracranial clipping of the aneurysm.
of the type of treatment used, the interval between the onset of third nerve palsy and the time of treatment, and the type of oculomotor paresis, that is, whether it was complete, moderate or slight ; moderate meaning less than 15 degrees ocular movement, a fully dilated pupil or severe ptosis; slight meaning more than 15 degrees muscle movement, slight enlargement of pupil and minimal ptosis. Our control group of untreated cases is necessarily small (four cases) because the
majority of conservatively treated cases did not have angiographic verification of their aneurysm and so were not included in our series. INTRACRANIAL CLIPPING (fig.
3)
Twenty-eight patients were treated by intracranial clipping of their aneurysm. Seven patients with a complete third-nerve palsy were so treated during the first 10 days of the onset of their third-nerve palsy. Three made a complete recovery of third-nerve
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function, one was left with a slight deficit of third-nerve function, two were left with a moderate deficit and one patient died. Five patients with a moderate deficit of third-nerve function were operated on during the first 10 days ; three made a full recovery, one being left with only a slight deficit and one patient dying. W e are including a case report of one of the patients in this group who made a rapid and complete recovery. Mrs. M. G. T h i s 32-year-old h o u s e w i f e w a s admitted to the T o r o n t o General Hospital on D e c e m ber 1, 1956, w i t h a three-week history of severe left retro-orbital pain. D u r i n g the t w o days prior to admission, she noted photophobia, diplopia and increasing left ptosis. O n examination she w a s bright and alert with n o neck stiffness. S h e had an incomplete left third-nerve palsy, moderate in nature, with less than 15 degrees of elevation, depression and adduction, almost complete ptosis and a dilated left pupil w h i c h reacted sluggishly to light. S h e w a s otherwise neurologically normal. Bilateral carotid arteriograms w e r e done and revealed a left supraclinoid internal carotid artery aneurysm arising at the origin of the posterior communicating artery. F o r t y - e i g h t hours after admission a left frontotemporal bone flap w a s turned under hypothermia and the neck of the aneurysm clipped. Immediately postoperatively the third-nerve palsy began to improve s o that at the time of her discharge 10 days later she had only some residual left ptosis and superior rectus weakness. H e r remaining third-nerve paresis completely recovered in the n e x t four w e e k s and she has been perfectly well since then.
Two patients with slight deficits of thirdnerve function were operated on during the first 10 days. One died and one remained with a slight third-nerve deficit. Nine patients with complete third-nerve palsies were operated on between 10 days and one month ; none made a complete recovery, seven were left with moderate deficits of third-nerve function and two died. Two patients with a moderate deficit were operated on between 10 days and one month. One fully recovered, the other died. One patient with a slight deficit of third-nerve function was operated on between 10 days and one month and made a full recovery. Two patients with complete third-nerve palsies were operated on between one and
six months following onset of their palsy, both of these patients were left with moderate deficits of third-nerve function. Of the 28 patients treated by direct intracranial clipping of their aneurysmal neck, six died, eight showed complete recovery of third-nerve function and, in 14 cases, a partial deficit of third-nerve function persisted. CAROTID LIGATION
(fig.
3)
Eight patients were treated by common carotid ligation in the neck. One patient with a moderate deficit was operated on within the first 24 hours of onset and recovered to the point of having only a slight deficit. One patient with a moderate deficit of third-nerve function was operated on between 10 days and one month and was left with a slight deficit. Three patients with a complete third-nerve palsy were operated on between one and six months ; two were left with a moderate deficit and one with a slight deficit of thirdnerve function. One patient with a moderate deficit was operated on between one and six months and was left with a slight deficit. One patient with a complete third-nerve palsy was operated on between six and nine months and was left unchanged. One patient with a moderate deficit operated on between six and nine months was left with a slight deficit. Recovery of third-nerve function was incomplete in the eight patients treated by cervical ligation of the carotid. The period of follow-up after treatment in this group ranged between six months and six years, the mean interval being three years. Jefferson reported failure of full recovery in 23 cases that he treated by cervical carotid ligation and this is confirmed by our experience. Furthermore, diplopia is most troublesome in the cases left with a slight deficit. 1
CONSERVATIVE
TREATMENT
Four patients were left untreated surgically because of their age, their general con-
OCULOMOTOR PALSY D U E TO A N E U R Y S M
dition or because local conditions contraindicated operation. Three of these patients had a complete third-nerve palsy, two remained unchanged and one improved to the state of being left with a moderate deficit. One patient had a moderate deficit initially and this remained unchanged. None of these patients died and all were free of neurologic deficits aside from their third-nerve lesions. Recovery of third-nerve function showed a fairly constant course. The superior rectus muscle was the slowest to recover and the patients who did not achieve full recovery were usually left with a deficit in elevation of the globe. The medial rectus muscle usually showed good recovery, the inferior rectus muscle recovering to a lesser extent. Most of the patients recovered fairly good function in their levator palpebrae as well as some pupillary reaction to light. Recovery of thirdnerve function started frequently within days of treatment and in some cases was complete within weeks of treatment. In most cases it took months for full recovery to take place ; the patients who achieved full recovery usually did so within three months of treatment. However, some patients took as long as a year before achieving maximum recovery. The phenomenon of aberrant regeneration as described by Walsh in the recovering third nerve was observed in only two cases. Headache was completely relieved in patients treated by carotid ligation and by direct attack on the aneurysm. Patients left untreated usually had improvement in their headache of a more gradual nature. 3
DISCUSSION
Complete recovery of oculomotor function was not seen in our group of eight patients treated by carotid ligation in the neck and was not seen by Jefferson in his 23 cases treated by carotid ligation in the neck. By contrast, eight of the 28 patients treated by intracranial clipping of their aneurysm showed a complete recovery of third-nerve function. The interval between the onset of third1
615
nerve dysfunction and the time of treatment was a very significant factor in the recovery of third-nerve function. Six of the 14 patients treated by intracranial clipping of the aneurysm within the first 10 days of onset of the third-nerve dysfunction made a complete recovery. Only two of the 14 cases treated beyond 10 days made a complete recovery of third-nerve function and neither of these two had a complete third-nerve palsy initially. Thus, complete third-nerve palsy in our series recovered fully only if treated by direct intracranial attack on the aneurysms within the first 10 days of the onset of their third-nerve paralysis. Partial recovery of third-nerve function was seen in patients treated months after the onset of third-nerve dysfunction and was seen as well in one of the four patients who received no treatment at all. In our particular series, it is difficult to compare the group treated by intracranial clipping with the group treated by carotid ligation because the latter group is small and most of the cases were treated beyond one month after onset of the third-nerve palsy. The apparently high mortality rate of those treated by direct attack on the aneurysm is explained by the fact that several of these patients were very ill at the time of operation. SUMMARY
1. Forty cases of oculomotor palsy due to angiographically verified supraclinoid internal carotid artery berry aneurysms are reviewed. 2. Twenty-five of these patients had subarachnoid hemorrhage associated with the onset of the third-nerve palsy. 3. There were 35 females and five males in this group. 4. Twenty-eight of the patients were treated by intracranial clipping of the aneurysm and eight of these made a complete recovery of third-nerve function. Eight patients were treated by carotid ligation in the
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ping of the aneurysm is undertaken soon after the onset of oculmotor palsy. Other forms of treatment are much less effective in restoring third-nerve function. Toronto General Hospital.
neck and none of these recovered full function of their third nerve. Four patients were treated conservatively because of age or general state and none of these fully recovered function of their third nerve. CONCLUSION
ACKNOWLEDGMENTS
W e w i s h to e x p r e s s our gratitude to D r s . W . M. Lougheed and T. P . M o r l e y for permission t o include the records of their patients, and to Prof. T. O l s z e w s k i of the Department of Neuropathology, U n i v e r s i t y of T o r o n t o , for making available his autopsy studies.
Full recovery of third-nerve function following oculomotor palsy due to supraclinoid internal carotid berry aneurysms is likely to occur only if treatment by intracranial clip-
REFERENCES 1. Jefferson, G.: Isolated oculomotor palsy caused by intracranial aneurysm. Proc. Roy. Soc. M e d , 4 0 : 419, 1946. 2. H y l a n d , Η . H , and H . J. M . Barnett: T h e pathogenesis of cranial nerve palsies associated with intracranial aneurysms. P r o c . Roy. Soc. M e d , 4 7 : 1 4 1 , 1954. 3. W a l s h , F . B . : Clinical N e u r o - O p h t h a l m o l o g y . Baltimore, W i l l i a m s & W i l k i n s , 1957, ed. 2, p. 833.
HOMONYMOUS A
HEMIANOPIA*
REVIEW OF ONE HUNDRED J.
LAWTON Durham,
SMITH,
North
Quantitative perimetry is a clinical examination essential to proper evaluation of the neurologic patient. To emphasize the fundamental role of quantitative study of the visual fields in topical neurologic diagnosis, the following review of 100 cases of homonymous hemianopia is presented. MATERIAL
One hundred cases with homonymous visual field defects were selected for review from records of patients seen in neuroophthalmologic consultation over two and one-half years. Criteria for selection were: ( 1 ) visual field examination must have been done by me in each instance, ( 2 ) the defect must have been present at the time of examination, and ( 3 ) the patient had to be ex* F r o m the D i v i s i o n of Ophthalmology, D u k e U n i v e r s i t y School of Medicine. T h i s study w a s supported in part by U . S . Public H e a l t h Service Grant 81-1656.
CASES
M.D.
Carolina
amined at both the perimeter and tangent screen (confrontation fields alone were insufficient). Conventional tangent screen techniques were used and an Aimark projection perimeter was employed for peripheral field examinations. It should be noted that a common cause of homonyous field defects, ophthalmic migraine, was thus eliminated from consideration for, although many migraine patients give vivid histories of hemianopias, it is infrequent for these defects to be present at the time of the perimetric examination. The cases here considered are primarily those which would be seen in consultation by an ophthalmologist. The records were analyzed for the following data: age, sex, race, chief complaint, duration of complaint, visual acuity, visual field findings, measurements of palpebral fissures and pupils, optokinetic responses, ophthalmoscopic findings, ophthalmodynamometry, neurologic findings, results of arteriog-