Central trochlear palsy

SURVEY OF OPHTHALMOLOGY

VOLUME 30.

NUMBER 5

l

MARCH-APRIL

1986

REVIEW

Central Trochlear Palsy AHMAD

M. MANSOUR,

M.D.,’

AND ROBERT

D. REINECKE,

M.D.’

‘Department of Ophthalmology, American University of Beirut, Lebanon, and Albert Einstein College qf Medicine, Bronx, hiew York, and ‘Wills &ye Hospital, Philadelphia. Pennglvania

Abstract. Historically, the trochlear (IV) nerve has been “neglected” by neurologists and ophthalmologists. However, the reported incidence of trochlear palsy in two large series has more than doubled in the past two decades, indicating increasing awareness of this nerve. Trauma is the most common cause oftrochlear palsy, as the trochlear nerve is anatomically more vulnerable to trauma than the other ocular motor nerves. Trochlear palsy can also be caused by vascular and inflammatory diseases, congenital factors, toxic substances and tumors. Diplopia secondary to vertical and horizontal deviation is the most common presentation. The trochlear nerve has a relatively high recovery rate after the underlying cause of injury has been corrected. In this article, the anatomy and physiology of the trochlear nerve are described, and the various etiologies, methods of diagnosis and differential diagnosis of trochler palsy are reviewed. (Surv Ophthalmol 30:279-297, 1986)

Key words. congenital disorder trochlear nerve trochlear palsy l

l

l

lesions vascular

Of the cranial nerves, the trochlear nerve has received the least attention in routine neurological and ophthalmogical examinations and in the literature. Trochlear palsy affects both sexes with mild male predominance, and all ages with an average age of 20 years at presentation. Recent increasing awareness of this cranial nerve is reflected by the increase in the reported incidence of isolated trochlear palsy from 7.2% in 19661T6 to 17.2% in 1981’28 based on two series of 1000 patients with ocular motor palsies. Based on literature reports and a series of 82 patients with isolated trochlear palsy followed by one of us (RDR) at Albany Medical Center between 1972 and 1981, we will discuss the anatomy and physiolopy of the trochlear nerve from its nucleus to its exit from the brain, the various causes of trochlear palsy, and the presently available’ diagnostic modalities.

l

ocular disorder

motor

palsy

I. Anatomy

l

trauma

l

of the Trochlear

Nerve

The trochlear nuclei are located at the level of the superior part of the inferior colliculus ventrolateral to the cerebral aqueduct (Fig. 1). They indent the dorsal surface of the medial longitudinal fasciculus. They are the direct continuation of the oculomotor nuclei and are in series with the abducens nuclei. The nuclei are the smallest cranial nerve nuclei, both in area (0.6 mm square)“’ and in number of monerve cells (3400). ‘6gThe fairly large multipolar tor neurons (40-50pm) stain heavily with basophilic dyes, and make up the spherical trochlear nuclei (Fig. 2) .41The fibers run first dorsolaterally around the aqueduct of Sylvius, reach the lower border of the inferior colliculus and pass medially to decusin the superior medullary velum sate completely”5 and emerge from its dorsal surface in the form of

280

Sun, Ophthalmol

30(5) March-April

1986

MANSOUR, REINECKE

F&. 1. Section of the midbrain at the level of the inferior colliculus. The trochlear nucleus is above the medial longitudinal fasciculus. Top: X 16, Modified Bielschowsky stain for axon. Bottom X 100, Modified Biel-

schowsky stain for axon.

rootlets. The number of the rootlets of origin varies from one to six on each side, with an average of two.‘03 These join to form the most slender cranial nerve with one millimeter thickness.‘*’ The course of the nerve can vary. In some cases, it courses laterally and upwards to emerge from a relatively rostra1 part of the inferior colliculus. Similarly, the level of decussation in the brainstem may be more rostraL5* It continues ventrally around the lateral aspect of the midbrain and passes between the posterior cerebral and superior cerebellar arteries between the midbrain and the temporal lobe. The nerve courses along the tentorium cerebelli for one or two centimeters and becomes embedded in this membrane to lie central to the third nerve and pierce the dura to face the lateral wall of the cavernous sinus15’j above

and medial to the trigeminal ganglion and lateral to it enters the orbit the pituitary fossa. Finally, through the superior orbital fissure to innervate the superior oblique muscle. A horsetail branching of the trochlear nerve occurs before it penetrates the belly of the superior oblique muscle. Of the cranial nerves, the trochlear nerve has the longest intracranial course (75 mm). ‘6gThe fibers of the trochlear nerve are mostly medullated and large (12 to 19 micra in diameter) (Fig. 3).g The ratio between the large and small fibers has been reported to be 3 : 1 in man and dog’ by light microscopy, and 49: 1 in goats by electron microscopy.“j5 The ratio between the fibers of the trochlear nerve and the cells in the trochlear nucleus is 1: 1 .14’J65 The superior oblique muscle (the “reading” muscle) has the highest den-

CENTRAL

TROCHLEAR

‘81

PALSY

F&J. 2. Top left: Trochlear nerve (TN) from nucleus to exit from brain. Cerebral aqueduct is represented by the middle notch. Cross section I of the superior part of the inferior colliculus shows the trochlear nucleus and the dorsoiateral course ofTN. Cross section II ofmiddle part of inferior colliculus shows the TN running medially and dorsally round the aqueduct. Cross section III ofsuperior medullary velum illustrates the decussation, rootlet formation and dorsal exit. Bottom left: Section I through the nucleus

shows

the

large

multipolar

motor

neurons

640. ModiGed Bielschowsky stain for axon). Bottom right: Section I II shows the decussation of axons i X 100, Modified Bielschowsky stain for axon). (X

sit)- of nerve fiber innervation per muscle spindle. “I No communication between the trochlear nerve and the sympathetic system has been reported.“’ A supernumary orbital structure may originate from the medial border of the levator palpebrae superioris and insert on the trochlear fascia, and this must be dillercntiated from an anomalous superior oblique muscle.“’ This structure, named the levatortrochlear muscle, was present in 7 out of 98 cadavers.‘“” This muscle is to be differentiated from rare fbrms of complete reduplication of the superior oblique muscle’” and retractor bulbi muscle.“”

II. Physiology of the Trochlear Nerve Physiological studies have suggested the presence of interneurons in the ocular motor nuclei in addition to the motor neurons.“’ These interneurons are thought to connect the different ocular motor nerves

with each other or with the \-cstihulo-ccret)ellum in the form ofvestibulo-ocular projections.” Ixsions in the vestibular nuclei of the cat” and in the mt’sencephalic tract of nerve V in the macaque animal”’ resulted in degeneration ofsome fibers in the trochlear nerve. However, autoradiographic studies in the cat reported no cerebellar fibers terminating in the oculomotor n,uclei.“’ The evidence for an afferrnt system in the frochlear nerve remains controversial.’ ”

III. Embryology of the Trochlear Nerve The ocular motor nuclei are derived from the mesodermal condensation of the premandibular cavity.” The oculomotor nuclei first appear at the 8-9 mm stage followed directly by the appearance of the trochlear nuclei at the 9 mm stage. The trochlear nerve nucleus lies lateral to the narrow communica-

282

Surv Ophthalmol

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MANSOUR, REINECKE

1986

TABLE Etiology of Isolated

1

I’ersus Mixed

Involved Etiology

Total

90 78 14 45 3 26

111+1v

(35) (30) (6) (18) (1) (10)

III+Iv+VI

5 (9) 15 (26) 11 (19)

14 (12) 21 (18) 49 (42)

1 (2)

1 (1)

13 (22) 13 (22)

7 (6) 24 (21)

256 (100)

58 (100)

*Data compiled from two series totalling with ocular motor palsies.‘Lb,‘zR

TABLE Etiology qf Isolated

Palsies

122 81 a4 107 90 80

Total

564 (100)

[No. (%)I

IV

(22) (14) (15) (19) (16) (14)

90 78 14 45 3 26

(35) (30) (6) (18) (1) (10)

256 (100)

*Data compiled from two series with ocular motor palsies.““.‘28

3. Top: Light micrograph through the trochlear nerve. Note the predominance of the large myelinated fibers ( X 1020). (Reprinted from Weidman TA, Sohal GS’“” with permission of the authors and publishers of Bruin Research.) Bottom: Intracranial course of TN (ReSurv printed from Kline LB: Tolosa-Hunt syndrome. 1982, with permission of the auOphthalmol 27:79-95, thor.)

2000 patients

2

III

Undetermined Trauma Neoplasm Vascular Aneurysm Other

116 (100)

of the Ocular Motor Nerves*

Nerve Involved Etiology

Palsy*

Nerve [No. (%)]

IV

Undetermined Trauma Neoplasm Vascular Aneurysm Other

Trochlear

totalling

VI 236 125 220 120 30 203

(25) (13) (24) (13) (3) (22)

934 (100) 2000 patients

Fig.

bryo.“’ Depriving the trochlear nucleus from its peripheral innervation, as by extirpation of the optic primordium, leads to variable degrees of hypoplasia that are mostly related to the timing of the extirpation.“‘,“” Thus, trochlear nuclear aplasia may be primary, or secondary to aplasia of a related peripheral structure during embryonic development.

IV. Etiology of Isolated Trochlear Palsy

tion

between

ion.“’ The

the metencephalon abducens

nuclei

rapidly

and

mesencepha-

follow

at the

10

mm stage. By the sixth to seventh week, the trochlear nerve is prominent, and by the end of the eighth week, all the ocular nerves have reached their respective extraocular muscles. From studies in duck embryos, it seems that approximately half of the cells in the trochlear nucleus and 98% of the trochlear nerve fibers are lost between day 11 of incubation and hatching. The cell/ fiber ratio changes from 1: 20 on day 11 of embryonic life to 1 : 1 at hatching and stays constant thereafter.‘+” Similar results were found in the chick cm-

The etiological patterns of isolated trochlear palsies vary considerably from those of mixed trochlear palsies (Table 1) and isolated palsies of the other ocular motor nerves (Table 2). In these groups, space-occupying lesions account for a relatively large proportion of the cases, while trauma is the most common cause of isolated trochlear palsies. This review is primarily concerned with isolated trochlear palsies. It is based on 22 series reporting 895 patients, whose etiological characteristics are summarized in Tables 3 and 4 and discussed below. A. TRAUMA Closed head trauma is the most common cause of trochlear palsy in most series, and trochlear palsy

CENTRAL

TROCHLEAR

283

PALSY TABLE

3

of Isolated

Reported Etiolqgies

Trochlear

Pa&v

Etiology Author

Year

(Ref)

Rucker ( 126) Khawam (76) Crone (27) Burger i 19) Chapman (22) Miller (97) Raskind ( 118) Rougier ( 125) hlittelman (98) Young’ i 173) Wright ( 172) Coppptto (25) Neetens (106) Harley (57 I Fells (37) Nemet (107) Rush (128) Sydnor I 148) \Vise I 168) Reynolds ( 120) Pollard ( I 14) Reinerke (present study]

No. of Patients

1966 1967 1970

1970 1970 1970 1973 1973 1976 1977 1977 1978 1979 1980 1980 1980 1981 1982 1983 1984 1985 1986

Trauma

-

84 40 14 :33 6 7 3 40 100 52 23 43 43 18 31 27 172 33 3 ‘0 21 82

Total -

Bilateral 18% 100% 100% 0 0 8% 8% 9% 0 54% 100% 0 8% 38% 100% 100% 9%

895

Tumor

Vascular

23 27 11 13 6 0 3 26 22 16 9 9 26 5 25

(27) (68) (79) (40) (100) (0) (100) (65) (22) (31) (39) (21) (60) (28) (80)

55 33 2 0 17 28

(32) (100) (67) (0) (82) (34)

356 (40)

[Number

(Percent)]

Undetermined 28 8 0 2 0 7 0 8 78 19 4 15

(33) (20) (0) (6) (0) (1001 (0) (20) (78) (36) (18) (35)

(0) (10) (0) (20) (0) 1 (33) 0 (0) -

12 0 13 62 0 0

(67) (0) (48) (36) (0) (0)

2 (2)

48 (59)

13 2 0 6 0 0 0

1 0 12 8 9

(16) (5) (0) (18) (0) (0) (0) (3) (0) (23) 135) (21)

7 (8) 1 (2) 0 (0) 7 (21) (1 (0) 0 (0) ‘) (0) 2 (5) ‘1 CO) 2 (4) 0 10) ‘3 (7)

0 3 0 34 0

xot Mentioned

Other

20 (ion)

91 (10)

324 (36)

30 13)

35 (,1)

59 (7)

= not mentioned TABLE Etiulqv

of Isolated

Trochlear

Palsy Related

to .?$veAffected and Sex of82

I‘rauma Congenital :\neurysmt Diabetes Tumor: Clndetermined Other$

28 43 1 1 1 5 3

Total

82 (100)

(35) (52) (1) (1) (1) (6) (4)

represents

one-third i2.‘“4Ii4 Head

cases with

oculomotor

of all traumatic trauma

accounts

or abducens

ocular

OS

ou

Male

16 27 0 0 0 2 2

7 14 1 1 1 3 1

5 2 0 0 0 0 0

15 27 0 1 0 2 2

13 16

47

28

47

35

motor

for 16% of the palsy

and

Center Series*

Sex Distribution

OD

*Present series, Reinecke (A large number ofthese patients of rongrnital cases.). t I nfraclinoid. ZSuprrior cerebellar glioma. $Hydrocephalus; dysthyroid myopathy, scleral buckle.

palsies.

Patients in ,416ary Medical

Eye Affected

No. (o/o) of Patients

EtioloE,

,4

32%

of cases with trochlear palsy.“’ This is why the trochlear nerve is called the “trauma nerve.“7” Motor vehicle accidents, falls from a height, and diff+

were children,

cult childbirth responsible scribed

accounting

are some for trochlear

following

electric

Female

I 0

I 3

1

for the larq

of the usual palsy.

number

forms

One

case

of trauma was de-

shock.”

After a sudden speed deceleration or a blow to the forehead, the brain continues to move backward against

a stationary

skull. This leads to “contrecoup

284

Surv Ophthalmol

30(5) March-April

1986

contusion” against the delicate attachment of the fourth nerve at the medullary velum with subsequent avulsion of the fourth nerve rootlets. Direct compression of the lower midbrain can also occur, injuring the nerve directly or the nucleus with focal bleeding.“’ The susceptibility of the trochlear nerve is explained by its relation to the tentorial edge which is a major determining factor in the distribution of contusions.g0 Because of the symmetry of the contusion forces in common trauma, bilateral trochlear palsy is common after closed head injury. 22~27~76~‘06~‘58 A sudden bilateral palsy is almost always due to trauma.** The exact intensity of head trauma needed to induce trochlear palsy is not clear. Most of the patients with traumatic trochlear palsy in our series suffered a moderate to severe degree of head trauma as evidenced by a prolonged episode of loss of consciousness, but many cases of trochlear palsy have been observed following minor or insignificant trauma.76 In the latter category, the trochlear palsy may be attributed erroneously to a congenital cause. We hypothesize that individual differences in nerve susceptibility to trauma could be related to the number of rootlets formed after decussation. Trochlear palsy from minor head trauma could be the first sign of a basal intracranial tumor.‘05 B. VASCULAR

DISORDERS

Branches of the posterior cerebral artery and superior cerebellar artery, namely the paramedian arteries and the quadrigeminai arteries, supply the trochlear nuclei and nerves. Because of the small size of the nucleus and its nerve, trochlear palsy is rarely seen alone and, more frequently, it will be masked by the presence of oculomotor palsy. Ophthalmoplegia as a sign of arterial insufficiency or occlusion is more frequently present in carotid than in basilar artery disease. Vascular causes were involved in about one-tenth of the cases of trochlear palsy we reviewed, including diabetes, atherosclerosis, aneurysm, arteriovenous malformation, and vascular accidents. Rush’s series reported the incidence to be about 20%.“’

MANSOUR, 2. Atherosclerosis

REINECKE

and Hypertension

Like diabetes, atherosclerosis and hypertension are implicated in around l-10% of trochlear palsy cases. Trochlear palsy was the first indication of hypertension in a man who later suffered myocardial infarction.‘72 In another case, it appeared following hypertensive episodes.3” 3. Aneurysms Aneurysms have predilection to the cavernous sinus and the infraclinoid region. They involve the trochlear nerve in 2 1% of cases, generally after affecting the other ocular motor nerves.‘jJ8 Aneurysms are one of the leading causes of isolated oculomotor nerve palsy in adults, while they account for only 1% of isolated trochlear nerve palsy.“8,‘30 Aneurysms in the posterior fossa cause isolated trochlear palsy by involving the posterior cerebral artery3’.lg5 or the posterior cerebellar artery. In three cases, trochlear palsy was the first sign of expanding intracranial aneurysms. 12* 4. Infratentorial Arteriovenous

Malformations

Infratentorial arteriovenous malformations including the oculocephalic vascular anomaly of Bonnet, Wyburn-Mason,‘“” are reported to cause isolated trochlear palsy2” and, more commonly, multiple nerve is incranial nerve palsies. I50 The trochlear volved in 19% of patients with carotid-cavernous fistula.5 5. Migraine Migrainous ophthalmoplegia is a rare finding with an occurrence of 8 out of 5000 migraine admissions.4 The third nerve is most frequently affected, with the abducens nerve involved one-tenth as often, and the trochlear nerve rarely involved.* Strokes, subarachnoid hemorrhage,‘** vascular coronary angiogembolization (e.g., following raphy’28) and hypoxia (secondary to neonatal hypoxia) have been listed with the causes of trochlear palsy. C. INFLAMMATORY

DISORDERS

1. Diabetes Mellitus

1. Acute Meningitis

The blood supply to the cranial nerves and nuclei is affected in diabetic ophthalmoplegia. Axonal reaction in the ocular motor nuclei and atherosclerosis of the vasa nervora have been documented pathologically.3’ Screening for diabetes is mandatory with unexplained trochlear palsy in the old-age group. Diabetic ophthalmoplegia occasionally presents as transient repeated attacks. Four recurrent episodes of isolated unilateral trochlear palsy were observed in a diabetic patient.“”

Ocular palsies are said to be among the most common signs of involvement of cranial nerves in meningeal disease, especially in the acute epidemic meningitides. ” Cases of trochlear palsy have occurred following acute meningitis.lz8 2. Tuberculous Meningitis Tuberculous meningitis affects predominantly the VI and III cranial nerves, respectively, in around 11% and 6% of patients.‘“O In India, tuber-

CENTRAL

TROCHLEAR

285

PALSY

Neurologic sarcoidosis in its subacute course has involved every cranial nerve, including the trochlear ner1.e. The facial nerve is most commonly affected, followed by the optic nerve.“‘.13” In its chronic course, the optic nerve is the main site of inflammation and ocular cranial nerves are usually spared.

culitis. In “cephalic tetanus”, facial palsy and, less commonly, ptosis (10%) were noted.“O Only one patient with tetanus suffered trochlear palsy with evidence of bulbar palsy; recovery occurred after one week.“Z Tetanus toxin is thought to have a direct neurotoxic activity that may not be reversible in all patients, as evidenced by many recent reports of brain stem lesions in patients dying from tetanus.‘” Botulism is known to cause complete external ophthalmoplegia on the basis of interference by the botulinurn toxin at the neuromuscular junction. Yet, multiple ocular motor nuclei lesions have been documented pathologically.i’ Three cases of diphtheric toxin-induced trochlear palsy were mentioned. VI nerve palsy occurred in 9 out of 64 cases of severe diphtheria while I I I nerve palsy is reportedly rare.“”

4. Ocular Motor Syphilis

D. COLLAGEN-VASCULAR

Gumma formation in the superior orbital fissure peripherally or in the meninges centrally affects the various ocular motor nerves.“‘” In incipient tabes dorsalis, transient ocular motor nuclei inflammation may occur with subsequent spontaneous recovery.“’

Collagen vascular disorders accounted for three cases of isolated trochlear palsy in Rucker’s series,“” and three cases in Rush’s series.‘?‘.‘l” One of Rush’s patients had systemic lupus erythematous and two had progressive systemic sclerosis.“’ Progressive systemic sclerosis is known to cause myopathy”’ with secondary diplopia.” Polymyalgia rheumatica (and hence probably temporal arteritis) was involved in one case of mixed ocular motor nerve palsies.“’ Intermittent ophthalmoplegia is seen occasionally in temporal arteritis and is important as a premonitory sign.“” There is no specific mention of trochlear palsy in temporal arteritis.

culous meningitis was the most common cause 01‘ ocular motor palsies.“g Out of an Indian series of 100 patients, 26 had tuberculous meningitis, onethird with isolated oculomotor paralysis, one-third with abducens affection, and one-third associated with other ocular motor nerve palsies. The thick caseous exudate filling the basal cisterns as a result of basal meningeal reaction, along with the presence of inflammation, leads to pressure atrophy of the ocular motor nerves and other cranial nerves. 3. Neurologic Sarcoidosis

5. Miscellaneous In acute poliomyelitis and epidemic encephalitis whooping cough), ocular (mumps, chickenpox, signs are among the most common manifestation of the disease.‘” Isolated trochlear palsy has been observed in these conditions.“’ In postinfectious polyneuritis (Cuillain-Barri syndrome), the cranial nerves are involved in half of the patients. Facial palsy- is most common, followed respectively by affection ofnerves III, IV, VI, V, IX, X, XI, XII.‘“,‘“’ Four cases of isolated trochlear palsy associated with postinlectious polyneuritis have been report,d,‘Wl?’ Ophthalmoplegia was thought to rarely complicate attacks of herpes zoster ophthalmicus,“g but a literature review”” and a prospective study revealed an incidence of ophthalmoplegia of 3 1% .‘I Trochlear palsy occurred in 21 cases in a series of 2250.“’ Some 35 cases of trochlear palsy have been reported in association with herpes zoster. ‘~3.73,86.91.132 The third nerve is most frequently involved, followed by the sixth and fourth nerves. Ophthalmoplegia may occur contralateral or bilateral to the side of the rash.“” Demyrlination and inflammation of the ocular motor nerves and perivascular infiltration of the supplying \fessels within the cavernous sinus have been observed.“” Herpes zoster virus is thought to affect the ocular motor nerves directly inside the cavernous sinus, or indirectly by a virus-induced vas-

DISEASES

E. TOXIC SUBSTANCES Direct lesions of the fourth cranial nerve were noted following exposure to various toxic substances. In kernicterus, the III and IV cranial nerves were among the most vulnerable, being affected in about 60% of pathologic specimens in which the trochlear nucleus had a spongy appearance.” The abducens nucleus was generally spared. In Pamaquinc naphthoate (Plasmochin) or other quinolinc poisoning, considerable nerve cell loss occurred in the III, IV and VI nerve nuclei with focal degeneration in the basis pontis.“’ Strabismus follows the ingestion of methylchloride or sodium fluoride. An abrupt onset of strabismus should make us suspect lead poisoning,‘!’ especially in the presence ofpapilledema in children, in whom the central nervous system involvement can be rapid in onset. The ocular motor nerve palsy in lead poisoning is said to be a result of increased intracranial pressure due to increased permeability of the blood brain barrier. Papilledema and ocular motor nerve palsies have bran reversed after multiple spinal taps.“‘.+’

286

Surv Ophthalmol

30(5) March-April

MANSOUR,

1986 TABLE

Pathology

and Location

Year

No. of Patients

1959

5

Suzuki (147) Rucker ( 126)

1962 1966

4 7

Khawam (76) Burger ( 19)

1967 1970

1 7

Rougier ( 125) Robert ( 122) King (77) Scully ( 136) Younge (173) Wray (171) Coppetto (25) Boggan ( 17) Kay (72) Rush (128) Ho (65) Samii ( 130) Murray ( 102) Reinecke series

1973 1973 1976 1976 1977 1977 1978 1979 1979 1981 1981 1981 1985 -

2 2 1 1 4 2 3 1 1 7 1 1 1 1

Author (reference) Zielinski

(174)

NERVOUS

SYSTEM

5

of Neoplasms

in Trochlear

Pathology

Palsy

and Location

1 parietal/l occipital/l brainstem/l spinal cord/ 1 hemangioma 4 pinealomas 2 midbrain gliomas/l meningioma/3 primary (brain)/ 1 metastatic “brain tumor” 4 cerebellopontine angle tumor/l cerebellum/ 1 nasopharyngeal carcinoma/l metastatic-lung 2 brainstem tumors 2 pituitary tumors 1 schwannoma 1 medulloblastoma at medullary velum 2 gliomas/2 metastatic-breast, ovary 2 pituitary tumors 1 ependymoma/I medulloblastoma/l acoustic neuroma 1 schwannoma 1 metastatic-midline malignant reticulosis 2 meningioma/l brain primary/4 metastatic 1 schwannoma I schwannoma 1 metastatic-lung adenocarcinoma 1 superior cerebellar glioma

Intravenous gold therapy has caused transient mixed ophthalmoplegia in less than 15% of patients. Gold has also induced a vascular spasm with secondary transient palsy.35,‘46 Alcohol caused isolated bilateral trochlear palsy with partial recovery in one case.‘72 Ophthalmoplegia, which can progress to its complete external form, is one of the triad of Wernicke-Korsakoff encephalopathy. The lesions are confined to zones around the aqueduct, III and IV ventricules, and mamillary bodies. The ocular motor nerve palsy could be secondary to multiple vitamin deficiency. For example, pellagra is known to affect the brain stem nuclei.2g F. CENTRAL

REINECKE

DISORDERS

Various central nervous system diseases are expected to affect the trochlear palsy. Primary hydrocephalus34.‘28 and pseudotumor cerebri7s54 are infrequently involved in trochlear palsy. (Five cases of hydrocephalus and two cases of pseudotumor cerebri have been reported). 7,34,54,‘2* The “false localizing sign” of trochlear palsy is rare compared with the abducens palsy that manifests frequently in patients with increased intracranial pressure. Primary convulsive disorders were associated with isolated trochlear palsy in few reports,34,‘73 although the relation was unclear. In migraine, III nerve involvement is ten times more common than VI, and trochlear palsy is rarely seen.“j3

TABLE Incidence of Various Neoblasmr

6 in Ocular Motor Palsies*

Nerve Involved Neoplasm Pituitary adenoma Craniopharyngioma Glioma-Pons Glioma-Midbrain Chordoma Meningioma Other primary Nasopharyngeal Other metastatic

22 1 0 4

Total

84

9 5 44 0 9 6 43 21* 83

1 12 11 1 32 14

*Data compiled from two series totalling with ocular motor palsies.‘26~‘2R

220

2000 patients

A history of diplopia was found in 97 of 295 patients with multiple sclerosis, but no cases of trochlear palsy were documented.” Trochlear palsy was documented in only six cases of mutiple sclerosis 25,27.l26.128,173

G. NEOPLASMS SYSTEM Tumors trochlear

OF THE

account palsy.

Of

CENTRAL

for

approximately

the

ocular

motor

NERVOUS

3-4% nerves,

of the

CENTRAL

TROCHLEAR

‘Hi

PALSY

/;i,q. 4. Ixli: Midline sagittal rrconstruction CT shows a midlinr cystic Irsiotl \\ith a thick rnhancing \r, a11. ‘1.11~Irsion. 2.5 cm in diameter, is wedged between the pineal region, quadri,qrminal platck and thr superior \x,rmis. Note the c.nlitrqrd I IId ventricle above the lesion, and the IVth ventricle below it. Ri,yht: CIros4 srction at the lc\~4 ol‘tht. tcntorial hiatus showinK thr enhancing lesion between the superior vermis and thr dorsum ol‘the midbrain (Rt~printrd Itom Krohrl (;H. Lfansour Ahl. et al: Isolated trochlear nerve palsy secondary to a juvenile pilocytic astroc‘) toma. ,/ (;/in .\~~rc,-o-O~~hlhnl,nf,i _‘:I 1%123. 1982. with permission of’ rhe publishers of,/ourntrl ?f‘ C’lirzic-nl.~~u~o-O)~hfhnl,,lo(o,p~. I

ner\re is least alrected by tumors, as it is well protected by being “hidden” in the thick tentorial bed. Table 5 summarizes the pathology cases of tumor-associated isolated trochlear patsy reported in the literature. Table 6 compares the incidence of various neoplasms in nerves III, IV and VI. In most of the cases cited in Table 5, trochlear patsy fiAtowed other cranial nerve afrection or was due to tumor-induced increased intracranial pressure. :I third of the cases were metastatic spread from Iumors of the nasopharynx,“’ lung, ovary. breast or elsewhere. Trochtear palsy was the first si,gn of metastasis in one case.“’ Diplopia from bilateral crochtear palsy was the presenting symptom 01‘ metastatic pulmonary adenocarcinoma as demonstrated h!. computed tomography of the head and subsequent needle aspiration of the pulmonary tesion.“” Pineatomas commonly involve the trochtear nerve at its point ot‘cmergencc. In one series of24 pineal tumors, trochtear patsy was seen in four cases white, the III nerve was involved in 18 patients (bitatcrat in 16 ) and the \:I nerve was involved in two patients.“’ LAcoustic neuroma and ccrebellopontine angle tumor account for around 15% of tumors with trochtear pats);. Parasellar and tentorial mcningioma account fi)r 10%. Enlarging pituitary adenomas involved the trochtear nerve and the oculomotor nerve in four patients. Ocular motor nerve patsies are noted in 1% to 14% of pituitary tumors (average of 5% in a total of 436 patients from tijur scxries): the third nerve is the most commonly involved. The ocular patsy resolved rapidly

trochlear

offifty

after removal of the adenoma in these c;~ses.‘~’ Ii’ hledutlohlastoma was present in two cases with trochlear patsy.“.’ ‘I’One of these tumors was in tht region of the medultary velum, and was missed on rhe first computed skull tomography only to br apparent after ocutomotor patsy had set in.““’ The most common primary brain tumors in\potved with trochtcar palsy are the gtiomas of the ccret~ettum and midbrain. \Vc recentI\. encountered a case of upper crrrbettar pitoc‘vtic astroc\~torna in a seven-year-old girt with isolated ctircct attkction ot‘ the trochtear nerve (Figs. 4 and 3). Primary brain tumor, particularly gtioma. is a mot-c common cause of ocular motor ncr\*e patsy in children. ” t>ircct troctilcar nerve involvement b): tumors is rar( rnou~~h to make trochlear palsy a “brniq“ palsy, ill contradistinction to the ahducens nerve. In a srrics of303% cases oftumors of the brain. 90”/~ had ocular symptoms. Papittedema was present in 61%. optic alrophy in IS%, visual tietd d&acts in 38%. and ocular motor paralysis in 22% of patients.“’ Intracranial schwannomas originate usually from sensory nerves and seldom arise from motor nerves. There arc ei,ght reports of intracranial schw~annomas involvin,q the ocular motor ncrvcs. follr in\Y~t\,in,? the trochtear nerve ““‘~” “” and t&r involving the oc.utomotor nerve. Schwannoma ot‘ the abdutens nerve has not been encounrrred. The majority; of schwannomas arise from the \‘I 11 ni’rve and a smaller group from the V nerve.’ I.’‘I’ Trorhtcar patsy ti-om minor hcad in-jury ma!’ ht the initial sign of an intracranial (urnor as demonstrattbd in three cases ofbasal intracranial lumors.“”

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REINECKE

Fig. 5. Pathological sections of the lesion seen in Fig. 4 demonstrate large unipolar and bipolar cells and a highly vascular tumor with strong affinity for neurologlial stains. Top: Hematoxylin and eosin, X 210. Bottom: Argentaffin stain, X 200. (Reprinted from Krohel GB, Mansour AM, et al: Isolated trochlear nerve palsy secondary to a juvenile pilocytic astrocytoma. J Clin Neuro-Ophthalmol 2: 119-l 23, 1982, with permission of the publisher of Journal of Clinical NeuroOphthalmology.)

H. CONGENITAL-IDIOPATHIC

CAUSES

1. Congenital Causes Congenital

aplasia

or hypoplasia

of the trochlear

have been described in isolated formP and in gross deformities such as hydrocephalus, and Goldenhar-Gorlin syndrome. Unilateral agenesis of trochlear nerve nucleus and other brain stem nuclei was demonstrated at autopsy in such a syndrome.” It is likely that an impaired growth of facial structures in utero results in hypoplasia of various extraocular muscles. In more severe cases of Goldenhar-Gorlin syndrome, both the extraocular muscle and its respective brain stem nucleus are underdeveloped.’ The association of Goldenhar-Gorlin syndrome with Duane’s syndrome and the findings of hypoplasia of the VI nerve nucleus in Duane’s syndrome add evidence to the autopsy findings of nunucleus

clear aplasia in oculo-auricuIo-vertebral dysplasia. Rafuse et al”’ reported paralysis of the trochlear nerve in a case with the dysmelic syndrome (phacomelia). Moebius syndrome with paralysis of the oculomotor and abducens nerves is a common sequela of the teratogenic effects of early thalidomide intake by pregnant mothers.“7 Aberrant innervation of the trochlear nerve to the levator palpebrae and orbicularis oculi muscles have been described, as well as various communications of the trochlear nerve with the supratrochlear, infratrochlear, and nasal nerves, and with the frontal and lacrimal branches of the opthalmic division of the trigeminal nerve.“‘” Congenital absence of the superior oblique muscle is rare; the most often missing muscle is the inferior rectus.“’ Sixteen cases have been reported with absence of the superior oblique tendon

CENTRAL

TROCHLEAR

PALSY

diagnosed at surgery, confirmed by coronal tomographic views of the orbit, or found at autopTh ere is a high incidence of absy. X.59.b?.10~1.111.11h.131 sence of extraocular muscles and especially the superior oblique in craniofacial dysostosis.““,zg Absence of the superior oblique tendons was noted in one case of anencephaly.R One case of congenital trochlear palsy had a hard mass in the upper nasal orbit. At exploration, the palpable mass proved to be a hard and thickened superior oblique muscle. Biopsy of the muscle belly revealed connective tissue fibers, hyaline cartilage but no muscle fibers.” This is a unique form of choristomatous growth ofa fibrotic superior oblique muscle presenting as trochlear palsy and as an orbital mass. 2. Idiopathic

Causes

The idiopathic variety Ibrms the largest category (50% ) of‘ trochlear palsy in the pediatric population.‘?” Proposed causes include: trochlear nuclear hypoplasia. birth trauma to the trochlear nerve or the superior oblique muscle, hypoplasia or absence of the superior oblique muscle, anomalous insertion of the muscle, muscle fibrosis, fibrous adhesions between various muscles, muscle sheaths, and orbital walls.“” “ 5 years of age. age: 31 years. deviation was 18 (range, tS40) in patients < 19 years ofage and 13 (range, 4-25) in patients age.

>

CENTRAL

TROCHLEAR

PALSY

lear palsy from vascular causes, 55% of cases from undertermined causes, and 44% of cases caused by trauma. Spontaneous resolution occurred in 65% of unilateral traumatic trochlear palsy and in 25% of bilateral traumatic trochlear palsy.‘“” Recovery occurred as early as one week’“” and as late as six months after onset, with an average of 10 weeks.“”

VI. Diagnosis Diplopia is the most common presentation of trochlear palsy. It is secondary to the vertical and horizontal deviation and only occasionally are torsional difficulties a complaint. The patient’s main problem mav be abnormal head posture, torticollis and e\en scoliosis. History-taking should include the time of onset of trochlear palsy as well as looking at old photographs for a head tilt. General principles fbr diagnosis of trochlear palsy are presented below.‘; A. AMBLYOPIA Visual acuity measurement may be important in localizing the side of the muscle palsy. Amblyopia is uncommon in trochlear palsy, but it is seen in patients with congenital onset trochlear palsy with horizontal deviations. In our series, one girl had a visual acuity of 20/200 in one eye with large esotropia secondary to superior oblique palsy. Amblyopia greater than one line was found to be present in 12% of patients.”

Fig. 7. The patterns ofspread of’ concomitance. Type I is the commonest pattern, II and II L arc occasionally noted, and IV, V, and VI are rarely noted (one case of each in our series). (***) refers to the palsied muscle; RH’f ;md LHT = right and left hypertropia; SR = superior rrctis; IR = inferior rrctus; SO = superior ohiique: ( + 1 refers

tn the degree

of hypertropia.

B. HYPERTROPIA The classic form of trochlear palsy is an incomitant hypertropia greatest in the adducted depression position of the involved eye (Fig. 6). This pattrrn is well illustrated in the fresh traumatic cases and is found in 26% of all cases of trochlear palsy (Table 8). However, spread of comitance may occur with time. Commonly, secondary inhibitional palinvolves one of the following muscles: consy,t’.H”.‘r”~“‘i tralatcral superior rectus, contralateral inferior oblique, ipsilateral inferior rectus or a combination of these (Fig. 7). Hypertropia is decreased in cases of bilateral trochlear palsy (Fig. 6). Asymmetry of the vertical invohement is the rule in bilateral cases.7g,“” One case in our series had no hypertropia. Vertical deviation \raries inversely with age in any category of trochlcar palsy. It is greatest in the congenital-onset group and least in the traumatic group. In the former group, it is maximal on upward gaze and in the latter group, it is maximal on downward gaze (Table 8). C. HORIZONTAL A large proportion

of esotropia reaching 65 diopters. Many patients in our series had had multiple operations for a “congenital esotropia.” Trochlear palsy should he suspected in infants with a history of crossed ryes in whom cardinal field measurements are difficult to obtain. Funduscopy becomes a valuable diaanostic test for torsion. “V” pattern is seen in halfof the cases with Unildtera1 palsy and in the majority with bilateral palsy (Table 9). It is due to the loss of the abducting power of the superior oblique muscle. In our series, “V” rxocleviation was as common as “V“ rsodevia-

TXBLE 9 Patterns of‘Hori;ontal

Iler~iation in 40 Patients Pal3 v*

DEVIATION of our cases had a high degree

*:\dapteci

from

Khawam.“’

127th Trochlear

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MANSOUR,

REINECKE

tion. Exodeviation is due to the overaction of the inferior obliques. Absence of “A” or “V” pattern is seen in the other half of unilateral cases and is a consequence of spread ofcomitance. The “A” pattern ofdeviation is rare. “A” esodeviation is expected to be secondary to the innervational palsy of the contralateral inferior oblique muscle while the “A” exodeviation is related to the ipsilateral inferior rectus inhibitional palsy. We observed a single case of “A” esotropia with bilateral trochlear palsy. D. HEAD POSTURE Head posture is described for its tilt, turn, and chin elevation or depression.‘97 Head tilt to the side of the nonparetic eye is found in half of the patients with unilateral palsy, and the tilt is present in twothirds of patients with bilateral palsy (Fig. 8).76 The absence ofspontaneous head tilt in trochlear palsy is attributed to amblyopia or to extremely large amplitudes of vertical fusion. Acute cases do not present with head tilt. Some patients have a tilt to the side of the paretic eye in order to get more suppression,‘7 and one patient in our series alternated the head tilt from the paretic to the nonparetic side. Bielschowsky head tilt is positive in 90% of patients with trochlear palsy,76.‘73 and positive in a higher percentage of cases with an abnormal head posture. 34In bilateral trochlear palsy with “V” pattern esotropia, chin depression is commonly adopted, thereby allowing fusion on upward gaze. Likewise, chin elevation is expected in “V” exotropia to allow fusion on downward gaze. A young boy was placed on 9 months of traction (Glisson’s sling) for a torticollis without success. After the diagnosis and correction of the trochlear palsy, the ocular torticollis disappeared.15’ E. CYCLODEVIATION Patients with trochlear palsy uncommonly complain of the torsional component until after correction of the tropia. Moreover patients can tolerate well large torsional amplitudes. The average and the range of the vertical as well as the horizontal torsional fusional amplitudes in degrees are, respectively: 28.6 (range, 23-44) and 15.2 (range, of excyclotorsion and in12-29). ‘52 Large amounts creased incidence of torsional diplopia characterize bilateral trochlear palsy. ‘4RCommonly used tests for cyclotropia include the Maddox double prism, the Maddox rod single or double,‘4.6”,g8.‘6’.‘62the Maddox wing, the red and green streaks, the major amblyoscope, the Lancaster-Hess-Lees screen tests, and funduscopy. Double Maddox rod testing was positive in 85% of patients for excyclotorsion and negative in the

Fig. face test “V”

8. Bilateral trochlear palsy. Top: Left head tilt and turn with chin down position. Bottom: Lees’ screen reveals bilateral excycloversion of 20 degrees and a pattern esotropia typical of bilateral trochlear palsy.

rest.3+ The absence of cyclotorsion is a consequence of spread of comitance, especially to the ipsilateral inferior rectus, thereby compensating for the extorsion. Lancaster-Hess-Lees screen tests can measure qualitatively as well as quantitatively the amount of torsion. They also provide a rough cardinal field measurement without the use of prisms, and the laterality of the palsy (Fig 8). Funduscopy is the simplest and quickest method for testing cycloversions (Fig. 9). Hypertropia and extorsion of the optic disc are noted in superior oblique palsy. Quantitation of torsion can be done with a fundus camera. a’ Funduscopy is the only objective test and the only available means to measure cyclodeviations in young children. In cases of bilateral trochlear palsy with minimal hypertropia, and negative Bielschowsky’s test, cyclotropia determination may help to localize the side of trochlear palsy. F. SACCADIC

VELOCITY

Vertical saccadic velocity determinations showed marked slowing of down saccade in the adducted position in trochlear palsy patients compared to controls. This finding can be used to differentiate

CENTRAL

TROCHLEAR

293

PALSY

3. Primary Versus Secondary Inferior Oblique Overaction: Transmission Electron Microscopic Studies It was noted that the presence of mitochondrial aggregates favored the diagnosis of primary inferior oblique muscle overaction; these aggregates were less prominent in case of secondary overaction from trochlear palsy (by transmission electron microscopy of biopsy material from inferior oblique muscles) .‘)I’ C. CENTRAL PALSIES I;(?. 9. Funduscopy

in the diagnosis

of trochlear

palsy.

I

and 11 represent left hypertropia. III and IV represent left hypotropin. I and II I represent extorsion of the disc. I I and IV represent intorsion ofthe disc. I corresponds to superior oblique, II to infer-ior rectus, III to superior rectus, and IV to inferior oblique palsies of the left eye.

CAUSES

OF VERTICAL

Central causes of vertical gaze palsy include skeu deviation (supranuclear dysfunction f?om brain stem lesions)” and Parinaud’s syndrome (supranuclear paresis of bilateral vertical movements usually by tumors that affect the periaqueductal area),l’J”XX.l’X D. SIMULATED UNILATERAL OBLIQUE MUSCLE PALSY

oblique

from recti muscle

palsy.“’

VII. Differential Diagnosis A. HEAD POSTURE The ocular causes of abnormal posture were studied in a prospective series of 188 patients.” Out of 70 cases with \.ertical incomitance, 66% had trochlear palsy. 10% inferior oblique palsy, 9% Brown’s syndrome. 7% blow-out fractures of the orbit, 4% double elevator palsy. and 4% superior rectus palsy. B. VERTICAL

PALSIES

1. Statistical Data According to Bielschowsky,” 90% of acquired vertical palsies are secondary to trochlear palsy. The differential diagnosis of vertical muscle palsy was presented in the following sequence”4: superior ohliquc, double elevator, inferior oblique, Brown’s syndrome, orbital floor fracture with inferior rectus thyroid myopathy, myasentrapment or palsy, thrnia gravis, and progressive external ophthalmoplegia. Isolated paresis of the vertical muscles supplied by the third nerve is quite rare.“’ 2. Normal Variants Mild degrees of superior oblique muscle underaction with inferior oblique muscle overaction are normal variants resulting from differences in the orientation and insertion of the superior oblique tendon. The superior oblique tendon undergoes a large change in its orientation relative to the trochlea during fetal development.

GAZE

SUPERIOR

1. The Three-Step Test Bielschowsky head tilt interpretation assumes that the patient has a single cyclovertical muscle palsy. By following the three-step diagnostic technique (described by Parks,“’ modified by Hardesty.” and simplified by Vazquez”‘“), many entities can he seen to mimic unilateral trochlear palsy. KushnerHt found 48 such cases including four cases of hilateral trochlcar palsy, four cases of contralateral inferior rectus restriction, and 32 cases of hypertropia with intermittent exotropia and no oblique muscle dysftmction (as evidenced by resolution ofhypertropia after horizontal muscle surgery).

2. Additional

Diagnostic

Steps

To avoid overdiagnosing trochlear palsy, auxiliary steps can help to differentiate paralytic from restrictive strabismus, single from multiple, and unilateral from hilateral muscle palsies. These tests include: Bielschowsky “missing” test or the “fourth” step (checking hyprrtropia on upward and downward gaze in the primary position);” measurement of saccadic eye movements, forced ductions, and ,generated force testing;;“’ qualitati\:e mrasuremrnt of cyclodeviation (the “fifth” step). This step hecomes essential in cases of mixed palsies. A combined palsy ofthe superior oblique and the contralateral inferior rectus muscles’” would simulate an isolated inferior rectus of the contraiateral eye by the three-step technique. The finding of an extorted right eyr would establish the diagnosis of concomitant superior oblique palsy.

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3. “Masked” Bilateral Trochlear Surgical Failures

Palsy and

Bilateral trochlear palsy should be recognized before strabismus surgery is attempted. “Masked” bilateral superior oblique palsy has been recognized following operation for a seemingly unilateral trochlear palsy. Urist’“” reported the first two cases, and since then 25 cases have been added.63 It is safe to assume trochlear palsy is bilateral until proven otherwise. The following findings suggest bilateral trochlear palsy: a large “V” pattern in excess of 25 prism diopters; angle of cyclotorsion greater than 10 degrees; bilateral excyclotorsion; and minimal hypertropia in the field of the seemingly nonaffected eye. 61.148 Acknowledgments Acknowledgments

MANSOUR, REINECKE

1986 I9

Burger cranial 20 Cantillo fracture. 21 Castren oblique 22.

23. 24. 25. 26.

27. 28.

to Dr S. Goldberger for help in prepar-

ing the manuscript, Dr. T. Yamamoto for providing the pathological material, DrJ.L. Smith for reviewing the manuscript, G. Chrysanthou for supplying clinical material, N. Mansour and B. Mansour for preparing the illustrations.

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1973

3. Astle WF, Rosenbaum AL: Familial congenital fourth cranial nerve palsy. Arch Ophthalmol 103:532-535, 1985 4. Bailev TD. O’Connor PS. Tredici Tl. Shacklett DE: Ouhthalmoplkgic migraine. J Clin Neuro-oph&mol 4:225-228,‘1984 5. Bajandas FJ: The six syndromes of the sixth nerve, in Smith JL (ed): Neuro-Ophthalmology Lipdate. New York, Masson Publishers, 1977, pp 49-67 6. Bajandas FJ: The four causes of fourth nerve palsy, in NeuroOphthalmology Board Revieul Manual. Thorofare, NJ, Charles B Slack, 1980, pp 91-97 7. Baker RS, Buncic JR: Vertical ocular motility disturbance in pseudotumor cerebri. J Clin Nemo-ophthalmol 5:41-44, 1985 8. BarnesJ, Boniuk M: Anencephaly with absence ofthe superior oblique tendons. Sure Ophthalmol 16371-374, 1972 9. Barrat JOW: Observations on the structure of the third, fourth, and sixth cranial nerves. J Anat Phvsiol 35:214-223, 1901 10. Beaty HN: Tetanus, in Petersdorf RG. Adams RD, Braunwald E, et al (eds): Harrison > Principles oflnternal Medicine, V’ol I, Part 4. New York, McGraw Hill, 1983, ed 10, p 1003-1006 dysplasia 11. Berkman MD, Feingold M: Oculoauriculovertebral (Goldenhar’s syndrome). Oral SW 24:408-417, 1968 A: Lectures on Motor Anomalies. Hanover, NH, 12. Bielschowsky Dartmouth College Publications, 1940, pp 73-80 13. Birndorf LA, Levy NS: Isolated sixth nerve palsy following prolonged general anesthesia. JPed Ophthalmol11:5%6l, 1974 14. Bixenman WW: Diagnosis of superior oblique palsy. J Clin Nemo-ophthalmol I; 199208. 1981 Ophthalmo15. Bleeker GM: Parinaud’s vertical ophthalmoplegia. logica 263:44-45, 1971 16. Blumenthal H, Miller C: Motor nuclear involvement in progressivfe supranuclear degeneration. Arch Neurof 20:362, 1’969 17. Boegan IE. Rosenblum ML. Wilson CB: Neurilemmoma of the fourth cranial nervre. J Neurosurg .50:51%521. 1979 18. Brodal A: Neurological .4natom_v in Relation to Clinical Medicine. New York, Oxford University Press, 1981, rd 3, pp 535-571

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