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Neurological Review |

Bilateral Ocular Paralysis Analysis of 31 Inpatients FREE

James R. Keane, MD
[+] Author Affiliations

Author Affiliation: Department of Neurology, University of Southern California, Los Angeles.


Arch Neurol. 2007;64(2):178-180. doi:10.1001/archneur.64.2.178.
Text Size: A A A
Published online

To my knowledge, no general study of complete ophthalmoplegia is available. This study was performed to determine the seats and causes of bilateral ocular paralysis. The personal records of 13 440 neurology and neurosurgery inpatients were reviewed. Eighteen (58%) of 31 patients had Fisher syndrome (13 cases) or Guillain-Barré syndrome (5 cases). Four cases resulted from midbrain infarction, 3 from myasthenia, and 1 each from pituitary apoplexy, skull base metastasis, botulism, mucormycosis, phenytoin toxicity, and trauma. Many conditions produce complete ophthalmoplegia on rare occasions, but Fisher syndrome, which paralyzes the eyes in nearly one third of cases, was by far the commonest cause.

In 1888, W. R. Gowers wrote

Paralysis of all the muscles of both eyes, internal and external, while theoretically conceivable from disease at the neighborhood of the orbital fissure and optic foramen on each side . . . is practically only met with in cases of nuclear disease. . . . Whether acute multiple neuritis ever involves the ocular nerves we do not know; the possibility that such peripheral neuritis may simulate central disease must be borne in mind.1

Complete bilateral ocular paralysis is a rare condition, usually reported as single cases. As no general study is available to my knowledge, I reviewed my experience to determine the causes and locations of conditions immobilizing both eyes.

From personal records of 13 440 inpatients who were personally examined in the wards of the Los Angeles County/University of Southern California Medical Center during a 34-year period, I selected those without perceptible movement in either eye. Comatose patients were excluded. Seven of the patients have been described previously.2 Photographs available for review included 21 slides, 4 video segments, 1 movie clip, and 1 fundus photograph. Diagnoses were established by history, physical examination, and contemporary laboratory and radiological tests. Guillain-Barré syndrome was distinguished from Fisher syndrome by the presence of definite limb weakness. Clinical and radiographic findings provided localization.

Complete ophthalmoplegia occurred in 31 patients (0.2% of my patients). Their ages ranged from 3 to 73 years, with a mean age of 49 years; 22 (71%) were men. The pupils were fixed in 16 cases (>5 mm in 13 cases), partially involved in 8, and spared in 7. Two patients with Fisher syndrome developed oval, reactive pupils. Ptosis was complete in 25 cases, partial in 5, and absent in 1.

Cranial nerve involvement, aside from the ocular motor nerves, occurred in 17 patients and included optic neuropathy in 4 cases bilaterally and 2 unilaterally; unilateral 5th-nerve impairment in 1 case; and bilateral involvement of the 7th nerves in 9 cases, the 10th nerves in 4 cases, the 11th nerves in 3 cases, and the 12th nerves in 2 cases.

Fisher syndrome (13 cases) and Guillain-Barré syndrome (5 cases) were the leading causes of ophthalmoplegia, together composing 18 (58%) of 31 cases. (Ocular paralysis occurred in 31% of my cases with Fisher syndrome and 3% of those with Guillain-Barré syndrome [Table 1].) Midbrain-thalamic infarcts were responsible for 4 cases (3 from atherosclerosis and 1 with cryptococcal meningitis associated with dermatomyositis), 3 cases had myasthenia, and there was 1 case each with orbitosinus mucormycosis, foodborne botulism, pituitary apoplexy, renal carcinoma metastasizing to the skull base (clivus-cavernous sinuses and posterior orbits), acute phenytoin toxicity, and automobile trauma with fractures through the cavernous sinuses and orbits.

Table Graphic Jump LocationTable 1. Etiology of Complete Bilateral Ophthalmoplegia

Sites of involvement included polyneuropathy in 18 cases, the brainstem in 5, the neuromuscular junction in 4, cavernous sinuses and posterior orbits in 3, and the cavernous sinuses in 1 (Table 2).

Table Graphic Jump LocationTable 2. Location of Lesions Causing Complete Ophthalmoplegia
POLYNEUROPATHY

The high proportion of patients with Fisher and Guillain-Barré syndromes in this series reflects the fact that nearly one third of patients with Fisher syndrome develop complete ophthalmoplegia3 (Table 1). Indeed, Fisher syndrome is one of the few conditions—along with neurotoxic snake4 and tick5 bites—that commonly produce complete ocular paralysis. Cephalic tetanus6 is an occasional cause of bilateral ocular paralysis, but diabetic cranial neuropathy, one of the commonest causes of diplopia and an occasional cause of cranial polyneuropathy,7 very rarely causes complete bilateral ophthalmoplegia.8

MUSCLE AND NEUROMUSCULAR JUNCTION

Impairment of neuromuscular transmission would seem to be a parsimonious route to ophthalmoplegia, but only 1% of my patients with myasthenia and 6% of those with botulism (Table 1) had complete ocular paralysis. Neurotoxins are more effective at blocking the neuromuscular junctions of eye muscles, acting presynaptically in tick bite paralysis5 and through presynaptic or postsynaptic effects in snake envenomation.4

Thyroid eye disease, among the commonest causes of diplopia in eye clinics, rarely produces sufficient tethering and weakness of the extraocular muscles to eliminate all eye movements. In contrast, amyloidosis is an uncommon condition that paralyzes the eyes out of proportion to its rarity.9 Many cases of congenital ocular fibrosis and congenital myopathic ophthalmoplegia exhibit minimal or absent eye movement whereas progressive external ophthalmoplegia exhibits slowly progressive ocular limitation that occasionally becomes complete.

CAVERNOUS SINUS AND ORBITS

A 1964 review10 of skull base lesions found 14 cases of complete bilateral ocular paralysis caused by tumors and 5 cases with vascular causes. Tumors included 5 originating in the pituitary or hypophysis, 3 metastases (lung, breast, and ovarian primary tumors), 2 sinus malignancies, 2 of indeterminate nature, 1 lymphoma, and 1 nasopharyngeal malignancy. Vascular causes consisted of 2 cases of carotid-cavernous fistulae, 1 case with combined effects of fistula and repair, 1 supraclinoid carotid aneurysm crossing the midline (with incomplete paralysis), and 1 case of paired cavernous carotid aneurysms.10

More recent reports include malignancies involving the cavernous sinuses (lymphoma,11,12 pituitary carcinoma,13 sphenoid sinus adenocarcinoma,14 and metastases from prostate carcinoma15 and mesenteric liposarcoma16), skull base (parathyroid metastasis17), and meninges (lymphoma18). Exceptionally, benign involvement of the skull base with fibrous dysplasia can result in ocular paralysis.19

Vascular causes include carotid-cavernous fistulae20 and bilateral orbital infarction associated with antiphospholipid antibody syndrome.21 Meningitis is a surprisingly rare cause of complete bilateral ophthalmoplegia,22 as is bacterial cavernous sinus thrombophlebitis,23 but sino-orbital-cavernous fungal diseases (mucormycosis,24,25 or less commonly, aspergillosis26 or actinomycosis27) disproportionately paralyze the eyes through infarction and inflammation.

BRAINSTEM

Coma often obscures ophthalmoplegia in central lesions of the midbrain, but rarely, strokes,28,29 abscess,30,31 viral encephalitis,32,33 and paraneoplastic encephalitis3436 paralyze both eyes. Occasionally, progressive supranuclear palsy, Whipple disease, and even multiple sclerosis render the eyes immobile, largely through supranuclear mechanisms. Wernicke disease produced complete ophthalmoplegia in 3% of cases in a large series,37 and experimental Wernicke disease typically progresses to complete ophthalmoplegia.38 The rare ophthalmoplegic brainstem toxicity of drugs (especially phenytoin and carbamazepine) frequently produces caloric-fast, reversible ocular paralysis with sparing of the pupils and often the eyelids.39 Finally, a few curious cases document the unexplained association of increased intracranial pressure with complete ophthalmoplegia.40

Correspondence: James R. Keane, MD, Department of Neurology, University of Southern California Medical School, Room 5641, 1200 N State St, Los Angeles, CA 90033 (jkeane@usc.edu).

Accepted for Publication: January 15, 2006.

Financial Disclosure: None reported.

Gowers  WR A Manual of Diseases of the Nervous System.  Philadelphia, Pa: P Blakiston, Son & Co; 1888
Keane  JR Acute bilateral ophthalmoplegia: 60 cases. Neurology 1986;36279- 281
PubMed Link to Article
Mori  MKuwabara  SFukatake  TYuki  NHattori  T Clinical features and prognosis of Miller Fisher syndrome. Neurology 2001;561104- 1106
PubMed Link to Article
Phillips  RETheakston  RDWarrell  DA  et al.  Paralysis, rhabdomyolysis and haemolysis causes by bites of Russell's viper (Vipera russelli pulchella) in Sri Lanka: failure of Indian (Haffkine) antivenom. Q J Med 1988;68691- 715
PubMed
Grattan-Smith  PJMorris  JGJohnston  HM  et al.  Clinical and neurophysiological features of tick paralysis. Brain 1997;1201975- 1987
PubMed Link to Article
Jayme-Goyaz  GG Cephalic tetanus following injury to the eyeball. Am J Ophthalmol 1941;241281- 1299
Keane  JR Multiple cranial nerve palsies: analysis of 979 cases. Arch Neurol 2005;621714- 1717
PubMed Link to Article
Cammarata  SSchenone  APasquali  GFTabaton  M Complete bilateral relapsing ophthalmoplegia in a diabetic patient with a sensory-motor distal polyneuropathy. Eur Neurol 1986;25278- 280
PubMed Link to Article
Raflo  GTFarrell  TASioussat  RS Complete ophthalmoplegia secondary to amyloidosis associated with multiple myeloma. Am J Ophthalmol 1981;92221- 224
PubMed
Hermans  GRetif  JPerier  O Acute bilateral ophthalmoplegia caused by median tumor of the base of the skull [in French]. Bull Soc Belge Ophtalmol 1964;138593- 601
PubMed
Jonkhoff  ARHuijgens  PCSchreuder  WOTeule  GJJHeimans  JJ Hypophyseal non-Hodgkins lymphoma presenting with clinical panhypopituitarism successfully treated with chemotherapy. J Neurooncol 1993;17155- 158
PubMed Link to Article
Tsuda  HKashima  YIshikawa  HIkeda  MSawada  U Malignant lymphoma in the cavernous sinus with bilateral total ophthalmoplegia and tonic pupils. Neuroophthalmology 2004;28237- 243
Link to Article
Nudleman  KLChoi  BKusske  JA Primary pituitary carcinoma: a clinical pathological study. Neurosurgery 1985;1690- 95
PubMed Link to Article
Cakmak  OErgin  TNAydin  VM Isolated sphenoid sinus adenocarcinoma: a case report. Eur Arch Otorhinolaryngol 2002;259266- 268
PubMed Link to Article
Anderson  DFAfshar  FToma  N Metastatic prostatic adenocarcinoma presenting as complete ophthalmoplegia from pituitary apoplexy. Br J Ophthalmol 1994;78315- 316
PubMed Link to Article
Bitoh  SHasegawa  HOhtsuki  HObashi  JKobayashi  Y Parasellar metastases: four autopsied cases. Surg Neurol 1985;2341- 48
PubMed Link to Article
Eurelings  MFrijns  CJJeurissen  FJ Painful ophthalmoplegia from metastatic nonproducing parathyroid carcinoma: case study and review of the literature. Neuro-oncol 2002;444- 48
PubMed Link to Article
Lau  JJOkada  CYTrobe  JD Galloping ophthalmoplegia and numb chin in Burkitt lymphoma. J Neuroophthalmol 2004;24130- 134
PubMed Link to Article
Alam  AChander  BN Craniofacial fibrous dysplasia presenting with visual impairment. Med J Armed Forces India 2003;59342- 343
Link to Article
Kamel  HAMChoudhari  KAGillespie  JSJ Bilateral traumatic caroticocavernous fistulae: total resolution following unilateral occlusion. Neuroradiology 2000;42462- 465
PubMed Link to Article
Vaphiades  MSBrock  WBrown  HHPetursson  GWestfall  CT Catastrophic antiphospholipid antibody syndrome manifesting as an orbital ischemic syndrome. J Neuroophthalmol 2001;21260- 263
PubMed Link to Article
Kastenbauer  SPfister  H-W Pneumococcal meningitis in adults. Brain 2003;1261015- 1025
PubMed Link to Article
Visudtibhan  AVisudhiphan  PChiemchanya  S Cavernous sinus thrombophlebitis in children. Pediatr Neurol 2001;24123- 127
PubMed Link to Article
Schwartz  JNDonnelly  EHKlintworth  GK Ocular and orbital phycomycosis. Surv Ophthalmol 1977;223- 28
PubMed Link to Article
Kasper  LHBernat  JLNordgren  REReeves  AG Bilateral rhinocerebral phycomycosis. Ann Neurol 1979;6131- 133
PubMed Link to Article
Mylonakis  EPaliou  MSax  PESkolnik  PRBaron  MJRich  JD Central nervous system aspergillosis in patients with human immunodeficiency virus infection: report of 6 cases and review. Medicine (Baltimore) 2000;79269- 280
PubMed Link to Article
Holland  NRDeibert  E CNS actinomycosis presenting with bilateral cavernous sinus syndrome. J Neurol Neurosurg Psychiatry 1998;644
PubMed Link to Article
Tomecek  FJMorgan  JK Ophthalmoplegia with bilateral ptosis secondary to midbrain hemorrhage: a case with clinical and radiologic correlation. Surg Neurol 1994;41131- 136
PubMed Link to Article
de Mendonca  APimentel  JMorgado  FFerro  JM Mesencephalic haematoma: case report with autopsy study. J Neurol 1990;23755- 58
PubMed Link to Article
Harvey  FHCarlow  TJ Brainstem abscess and the syndrome of acute tegmental encephalitis. Ann Neurol 1980;7371- 376
PubMed Link to Article
Sarma  SSekhar  LN Brain-stem abscess successfully treated by microsurgical drainage: a case report. Neurol Res 2001;23855- 861
PubMed Link to Article
Kalita  JMisra  UK Neurophysiological changes in Japanese encephalitis. Neurol India 2002;50262- 266
PubMed
Centers for Disease Control and Prevention, Outbreak of Powassan encephalitis: Maine and Vermont, 1999-2001. JAMA 2001;2861962- 1963
PubMed Link to Article
Dietl  HWPulst  St-MEngelhardt  PMehraein  P Paraneoplastic brainstem encephalitis with acute dystonia and central hypoventilation. J Neurol 1982;227229- 238
PubMed Link to Article
Rees  JHHain  SFJohnson  MR  et al.  The role of [18F]fluoro-2-deoxyglucose-PET scanning in the diagnosis of paraneoplastic neurological disorders. Brain 2001;1242223- 2231
PubMed Link to Article
Barnett  MProsser  JSutton  I  et al.  Paraneoplastic brain stem encephalitis in a woman with anti-Ma2 antibody. J Neurol Neurosurg Psychiatry 2001;70222- 225
PubMed Link to Article
Victor  MAdams  RDCollins  GH The Wernicke-Korsakoff Syndrome.  Philadelphia, Pa: FA Davis Co; 1971: 27
Cogan  DGWitt  EDGoldman-Rakic  PS Ocular signs in thiamine-deficient monkeys and in Wernicke's disease in humans. Arch Ophthalmol 1985;1031212- 1220
PubMed Link to Article
Puri  VChaudhry  N Total external ophthalmoplegia induced by phenytoin: a case report and review of literature. Neurol India 2004;52386- 387
PubMed
Friedman  DIForman  SLevi  LLavin  PJDonahue  S Unusual ocular motility disturbances with increased intracranial pressure. Neurology 1998;501893- 1896
PubMed Link to Article

Figures

Tables

Table Graphic Jump LocationTable 1. Etiology of Complete Bilateral Ophthalmoplegia
Table Graphic Jump LocationTable 2. Location of Lesions Causing Complete Ophthalmoplegia

References

Gowers  WR A Manual of Diseases of the Nervous System.  Philadelphia, Pa: P Blakiston, Son & Co; 1888
Keane  JR Acute bilateral ophthalmoplegia: 60 cases. Neurology 1986;36279- 281
PubMed Link to Article
Mori  MKuwabara  SFukatake  TYuki  NHattori  T Clinical features and prognosis of Miller Fisher syndrome. Neurology 2001;561104- 1106
PubMed Link to Article
Phillips  RETheakston  RDWarrell  DA  et al.  Paralysis, rhabdomyolysis and haemolysis causes by bites of Russell's viper (Vipera russelli pulchella) in Sri Lanka: failure of Indian (Haffkine) antivenom. Q J Med 1988;68691- 715
PubMed
Grattan-Smith  PJMorris  JGJohnston  HM  et al.  Clinical and neurophysiological features of tick paralysis. Brain 1997;1201975- 1987
PubMed Link to Article
Jayme-Goyaz  GG Cephalic tetanus following injury to the eyeball. Am J Ophthalmol 1941;241281- 1299
Keane  JR Multiple cranial nerve palsies: analysis of 979 cases. Arch Neurol 2005;621714- 1717
PubMed Link to Article
Cammarata  SSchenone  APasquali  GFTabaton  M Complete bilateral relapsing ophthalmoplegia in a diabetic patient with a sensory-motor distal polyneuropathy. Eur Neurol 1986;25278- 280
PubMed Link to Article
Raflo  GTFarrell  TASioussat  RS Complete ophthalmoplegia secondary to amyloidosis associated with multiple myeloma. Am J Ophthalmol 1981;92221- 224
PubMed
Hermans  GRetif  JPerier  O Acute bilateral ophthalmoplegia caused by median tumor of the base of the skull [in French]. Bull Soc Belge Ophtalmol 1964;138593- 601
PubMed
Jonkhoff  ARHuijgens  PCSchreuder  WOTeule  GJJHeimans  JJ Hypophyseal non-Hodgkins lymphoma presenting with clinical panhypopituitarism successfully treated with chemotherapy. J Neurooncol 1993;17155- 158
PubMed Link to Article
Tsuda  HKashima  YIshikawa  HIkeda  MSawada  U Malignant lymphoma in the cavernous sinus with bilateral total ophthalmoplegia and tonic pupils. Neuroophthalmology 2004;28237- 243
Link to Article
Nudleman  KLChoi  BKusske  JA Primary pituitary carcinoma: a clinical pathological study. Neurosurgery 1985;1690- 95
PubMed Link to Article
Cakmak  OErgin  TNAydin  VM Isolated sphenoid sinus adenocarcinoma: a case report. Eur Arch Otorhinolaryngol 2002;259266- 268
PubMed Link to Article
Anderson  DFAfshar  FToma  N Metastatic prostatic adenocarcinoma presenting as complete ophthalmoplegia from pituitary apoplexy. Br J Ophthalmol 1994;78315- 316
PubMed Link to Article
Bitoh  SHasegawa  HOhtsuki  HObashi  JKobayashi  Y Parasellar metastases: four autopsied cases. Surg Neurol 1985;2341- 48
PubMed Link to Article
Eurelings  MFrijns  CJJeurissen  FJ Painful ophthalmoplegia from metastatic nonproducing parathyroid carcinoma: case study and review of the literature. Neuro-oncol 2002;444- 48
PubMed Link to Article
Lau  JJOkada  CYTrobe  JD Galloping ophthalmoplegia and numb chin in Burkitt lymphoma. J Neuroophthalmol 2004;24130- 134
PubMed Link to Article
Alam  AChander  BN Craniofacial fibrous dysplasia presenting with visual impairment. Med J Armed Forces India 2003;59342- 343
Link to Article
Kamel  HAMChoudhari  KAGillespie  JSJ Bilateral traumatic caroticocavernous fistulae: total resolution following unilateral occlusion. Neuroradiology 2000;42462- 465
PubMed Link to Article
Vaphiades  MSBrock  WBrown  HHPetursson  GWestfall  CT Catastrophic antiphospholipid antibody syndrome manifesting as an orbital ischemic syndrome. J Neuroophthalmol 2001;21260- 263
PubMed Link to Article
Kastenbauer  SPfister  H-W Pneumococcal meningitis in adults. Brain 2003;1261015- 1025
PubMed Link to Article
Visudtibhan  AVisudhiphan  PChiemchanya  S Cavernous sinus thrombophlebitis in children. Pediatr Neurol 2001;24123- 127
PubMed Link to Article
Schwartz  JNDonnelly  EHKlintworth  GK Ocular and orbital phycomycosis. Surv Ophthalmol 1977;223- 28
PubMed Link to Article
Kasper  LHBernat  JLNordgren  REReeves  AG Bilateral rhinocerebral phycomycosis. Ann Neurol 1979;6131- 133
PubMed Link to Article
Mylonakis  EPaliou  MSax  PESkolnik  PRBaron  MJRich  JD Central nervous system aspergillosis in patients with human immunodeficiency virus infection: report of 6 cases and review. Medicine (Baltimore) 2000;79269- 280
PubMed Link to Article
Holland  NRDeibert  E CNS actinomycosis presenting with bilateral cavernous sinus syndrome. J Neurol Neurosurg Psychiatry 1998;644
PubMed Link to Article
Tomecek  FJMorgan  JK Ophthalmoplegia with bilateral ptosis secondary to midbrain hemorrhage: a case with clinical and radiologic correlation. Surg Neurol 1994;41131- 136
PubMed Link to Article
de Mendonca  APimentel  JMorgado  FFerro  JM Mesencephalic haematoma: case report with autopsy study. J Neurol 1990;23755- 58
PubMed Link to Article
Harvey  FHCarlow  TJ Brainstem abscess and the syndrome of acute tegmental encephalitis. Ann Neurol 1980;7371- 376
PubMed Link to Article
Sarma  SSekhar  LN Brain-stem abscess successfully treated by microsurgical drainage: a case report. Neurol Res 2001;23855- 861
PubMed Link to Article
Kalita  JMisra  UK Neurophysiological changes in Japanese encephalitis. Neurol India 2002;50262- 266
PubMed
Centers for Disease Control and Prevention, Outbreak of Powassan encephalitis: Maine and Vermont, 1999-2001. JAMA 2001;2861962- 1963
PubMed Link to Article
Dietl  HWPulst  St-MEngelhardt  PMehraein  P Paraneoplastic brainstem encephalitis with acute dystonia and central hypoventilation. J Neurol 1982;227229- 238
PubMed Link to Article
Rees  JHHain  SFJohnson  MR  et al.  The role of [18F]fluoro-2-deoxyglucose-PET scanning in the diagnosis of paraneoplastic neurological disorders. Brain 2001;1242223- 2231
PubMed Link to Article
Barnett  MProsser  JSutton  I  et al.  Paraneoplastic brain stem encephalitis in a woman with anti-Ma2 antibody. J Neurol Neurosurg Psychiatry 2001;70222- 225
PubMed Link to Article
Victor  MAdams  RDCollins  GH The Wernicke-Korsakoff Syndrome.  Philadelphia, Pa: FA Davis Co; 1971: 27
Cogan  DGWitt  EDGoldman-Rakic  PS Ocular signs in thiamine-deficient monkeys and in Wernicke's disease in humans. Arch Ophthalmol 1985;1031212- 1220
PubMed Link to Article
Puri  VChaudhry  N Total external ophthalmoplegia induced by phenytoin: a case report and review of literature. Neurol India 2004;52386- 387
PubMed
Friedman  DIForman  SLevi  LLavin  PJDonahue  S Unusual ocular motility disturbances with increased intracranial pressure. Neurology 1998;501893- 1896
PubMed Link to Article

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