Optometry - Journal of the American Optometric Association
Volume 81, Issue 9 , Pages 454-460, September 2010

On the frontline: What an optometrist needs to know about myasthenia gravis

  • Joseph A. Pruitt, O.D.

      Affiliations

    • Minneapolis Veterans Affairs Medical Center, Minneapolis, Minnesota
    • University of Missouri-Saint Louis College of Optometry, Saint Louis, Missouri
    • Corresponding Author InformationCorresponding author: Joseph A. Pruitt, O.D., Minneapolis Veterans Affairs Medical Center, 1 Veterans Drive (100-77), Minneapolis, Minnesota 55417.
    • ,
  • Pauline F. Ilsen, O.D.

      Affiliations

    • Southern California College of Optometry, Fullerton, California
    • West Los Angeles Veterans Affairs Healthcare Center, Los Angeles, California

published online 23 July 2010.

Article Outline

Abstract 

Background

Myasthenia gravis (MG) is an autoimmune disease that affects the voluntary skeletal muscles. It is characterized by transient weakness of the muscles that improves with rest. Muscle weakness involving the eyes can produce signs or symptoms of diplopia, blurred vision, ptosis, and ophthalmoplegia. Ptosis is defined as an abnormal eyelid “drooping” beyond the normal 1 to 2 mm of the upper limbus of the cornea. Hence, most patients with MG have ophthalmic manifestations. Among all patients with MG, up to half will have exclusively ocular symptoms. In these cases, the condition is referred to as ocular myasthenia.

Case Report

A 60-year-old man was referred from a neurology clinic for management of intermittent diplopia for greater than 1 year and intermittent bilateral ptosis for the prior year. He reported that he first noticed symptoms of MG at the age of 42, but did not receive the diagnosis until 1 year before his aforementioned neurology examination. He was prescribed spectacles with bilateral ptosis crutches. A diagnosis of severe seronegative MG was subsequently confirmed with neurologic examination and antibody testing.

Conclusions

Because patients with undiagnosed myasthenia gravis may present initially with ocular signs or symptoms, it is important for the optometrist to be familiar with the condition and the simple “in-office” tests that can be performed to establish a tentative diagnosis and management plan. The optometrist can also participate in the management of ocular manifestations of myasthenia and should be familiar with the use of a ptosis crutch (in addition to prism spectacles or occlusion therapies if indicated) as a nonsurgical intervention for ptosis.

Keywords: Myasthenia gravis, Ocular myasthenia, Myogenic ptosis, Ptosis crutch

 

Myasthenia gravis (MG) is an incurable antibody-mediated autoimmune disorder characterized by generalized voluntary skeletal muscle weakness. Literally translated from its Latin and Greek etymological roots, myasthenia gravis means “grave muscle weakness.”1, 2

The cause of the weakness is a defect at the level of the neuromuscular junction in which autoimmune antibodies block the receptors responsible for initiating muscular contraction. The neurotransmitter that is subject to this competitive inhibition is acetylcholine (ACh).2, 3 The muscles of the eye, neck, limbs, and the muscles within the chest (especially the muscles within the chest cavity responsible for respiration) are commonly affected.2 The muscles of the eye involved in lid retraction and eye movements are most notably affected.2, 4, 5, 6, 7, 8, 9 Muscle weaknesses involving the eye produce signs or symptoms of blurred vision, variable diplopia, and ptosis.1, 2, 3, 4, 5, 6, 7, 8, 9 Colavito et al.1 noted that accommodative dysfunction and vergence insufficiency can occur. Therefore, the optometrist must be cognizant that patients presenting with complaints of asthenopia, blur, and ophthalmoplegia may have an underlying systemic disease, like MG.1

The process by which the muscular weakness manifests is a result of competitive inhibition; therefore, the initial weakness observed is transient and improves with periods of rest.2 Likewise, muscular weakness increases during periods of increased or prolonged physical activity.5, 7, 9, 10, 11, 12, 13, 14, 15

Although MG is an antibody-mediated autoimmune disease, a reported 15% of patients with systemic or generalized MG have no detectable antibodies to acetylcholine receptors (meaning they are “seronegative” for MG).16 Furthermore, seronegative MG is fairly common in children and usually manifests before adolescence. A reported 40% of cases present before the age of 10 years.17

It is estimated that 85% to 90% of all reported MG cases, both seropositive or seronegative, present with ocular symptoms.5, 6, 7, 8, 9, 11, 12, 15, 16, 17, 18, 19, 20 Additionally, it has been reported that 20% to 50% of all cases of MG are purely ocular (ocular MG). Up to 55% of all cases of ocular MG are seropositive.4 Ocular MG is considered a separate diagnosis from generalized MG. Yet, most cases of generalized MG have ocular manifestations. There is also evidence of ocular MG progression toward generalized MG. However, patients who have had ocular MG for more than 1 to 3 years are not likely to progress on to generalized MG.21, 22, 23

Two theories have been suggested to explain the high proportion of MG cases that present with ophthalmic symptoms. The first is the susceptibility of ocular muscles to the disease process.17, 24 The second reason is that ocular involvement in MG is relatively easy to recognize compared with that of other muscle groups.17

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Case report 

A 60-year-old white man was referred to the Veterans Affairs (VA) neurology clinic from another facility for management of his myasthenia gravis with intravenous immunoglobulin G (IVIG). Seronegative MG had been diagnosed 1 year prior and had been managed unsuccessfully with prednisone (maximum dose, 60 mg 4 times a day alternating with 20 mg 4 times a day). He reported initially experiencing diplopia at age 42, which resolved gradually over a period of 3 years. He had no further symptoms until age 53, at which time he began having difficulty with generalized, full-body fatigue. At age 59, the diplopia recurred, occurring intermittently initially but gradually progressing until it was constant. Three months after the diplopia returned, he also began to have intermittent bilateral ptosis. Prior testing performed by the referring facility included computed tomography scan of the chest (the results of which were negative for thymoma or other pathology), erythrocyte sedimentation rate (ESR) (1 mm/hr), antinuclear antibody test (ANA) screening (negative), acetylcholine-blocking antibodies (<15, negative), acetylcholine-binding antibodies (<0.1, negative), and repetitive nerve stimulation testing (which found a reduced amplitude of response).

The patient's medical history was otherwise remarkable for hypertension and prostate cancer, for which he underwent a radical prostatectomy 3 years prior. Current medications included citalopram, atenolol, losartan, cetirizine, fish oil, and hydrochlorothiazide. The patient's family medical history was unremarkable.

Significant neurologic examination findings included a complete ptosis of the right eye while at rest and limited gaze in all directions secondary to an external ophthalmoparesis involving cranial nerves III, IV, and VI. Pupils were equal, round, and reactive to light. Based on prior laboratory test results and examination findings, the patient's previous diagnosis of presumed seronegative myasthenia gravis had been reaffirmed.

The patient returned to the neurology unit 2 months later and reported that his symptoms of weakness, fatigue, and shortness of breath had actually worsened since the previous visit. There was little to no improvement in clinical examination findings. Therefore, the diagnosis of presumed severe seronegative myasthenia gravis was made, and the patient was to be admitted to undergo 5 days of high-dose intravenous human immunoglobulin (IVIg).

Three weeks later, the patient was admitted to the hospital for a 5-day course of IVIg therapy. During his hospital stay, the patient was sent to the optometry department for an evaluation of diplopia, a refraction, and prescription for glasses fitted with a ptosis crutch. The patient's entering/uncorrected acuities were 20/40 in the right eye (O.D.), in the left eye (O.S.), and both eyes (OU). Confrontation visual fields were full. No movement was observed on cover test at distance, and 4 prism diopters of exophoria was evident at near (40 cm). Pupils were equal, round, and reactive to light. Extraocular muscles (EOMs) showed a full range of motion with no reported pain or diplopia by the patient. Diplopia did not manifest during the entire examination, but a bilateral complete ptosis did, which necessitated taping of the lids for the refraction. (Although different than the observation by the neurology department of a monocular ptosis, the finding was ultimately attributed to the patient's increased fatigue caused by a full day of appointments and activities revolving around his IVIg therapy.) The refraction found a slight mixed astigmatic refractive error, with best-corrected visual acuities of 20/25 O.D., O.S. Tear film instability was noted, and use of over-the-counter artificial tears was recommended. Finally, bilateral ptosis crutch spectacles were ordered to be worn full time.

Table 1. Differential diagnoses for ocular manifestations of MG48
MechanismCauses
Mechanical
Levator aponeurosis dehiscence
Involutional

Iatrogenic/ocular surgery

Trauma


Cicatrization

Eyelid mass
Neoplasia

Large chalazion


Myogenic
Chronic progressive external ophthalmoplegia

Myotonic dystrophy

Oculopharyngeal dystonia

Neurogenic
Multiple sclerosis

Horner's syndrome

CN III palsy

Internuclear ophthalmoplegia

Mass effect
Thyroid orbitopathy

Idiopathic orbital inflammation (or orbital pseudotumor)

Orbital neoplasia

Pseudoptosis
Enophthalmos

Hypotropia

Contralateral lid retraction

Later that day, the patient returned to the neurology department for further evaluation, and laboratory test results were reviewed. The serum acetylcholine receptor binding antibody level measured 0.15 nmol/L (normal, <0.30 nmol/L). Quantitative immunoglobulin (QIG) levels were as follows: QIG-IgA, 144 mg/dL (normal, 82 to 453); QIG-IgM, 64.0mg/dL (normal, 46 to 304); QIG-IgG, 859 mg/dL (normal, 751 to 1560), QIG-Kappa, 668 mg/dL (normal, 629 to1350); and QIG-Lambda, 297mg/dL (normal, 313 to 723). Thyroid-stimulating hormone level was 1.483 uIU/mL (normal, 0.35 to 4.50), free thyroxine level was 1.14 ng/dL (normal, 0.89 to 1.76), and thyroid function test results were consistently within the normal range upon repeated testing; the Westergren erythrocyte sedimentation rate measured 10 mm/h (normal); and the high-sensitivity C-reactive protein level was 0.63 mg/dL (low, <0.744). Because of these results, along with the previous test results performed by the referring facility, the diagnosis of seronegative myasthenia gravis was confirmed. The patient was discharged from the hospital on the following day and was to follow up with the neurology department in 1 month to consider repeat IVIg therapy at that time.

The patient returned to the optometry clinic 10 months later for an ocular examination. At this visit he recalled having had laser treatment for a “retinal degeneration” bilaterally some years previously. He reported success with his glasses with the ptosis crutch, but claimed to have lost them; he had no other visual or ocular complaints. Best-corrected visual acuities were 20/20 O.D., 20/25 O.S. Confrontation visual fields were full to finger counting O.D., O.S. Pupils were equal, round, and reactive to light, and there was no apparent pupillary defect. Extraocular motility was restricted in lateral gazes, a complete ptosis was noted O.D. and a mild ptosis O.S. Biomicroscopy findings showed clear lids and lashes, white and quiet conjunctiva, clear corneas, open angles, deep and quiet anterior chambers, normal irides, 1+ nuclear sclerotic cataracts, and clear vitreous OU. Intraocular pressures were measured by Goldmann applanation tonometry and were 14 mmHg O.D., O.S. Frequency doubling technique C-20 visual field screening (performed without taping the patient's lids) found a complete defect O.D. caused by the ptosis and a full visual field O.S. Dilated fundoscopy found small optic nerve heads with distinct margins, pink and healthy rim tissue, and cup-to-disc ratios of 0.3. The retinal vasculature and maculae were normal OU. Chorioretinal scarring was noted inferior/temporally O.D. and from 1:00 o'clock to 5:30 o'clock O.S., without any breaks, and were consistent with (and confirmed) the patient's vague memory of prior laser retinal treatments. Two new pairs of spectacles, one with and one without the ptosis crutches, were to be ordered. The patient was instructed to return to the clinic in 1 year for an annual comprehensive eye examination.

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Discussion 

The ocular manifestations of MG make it likely that a patient with otherwise undiagnosed disease will seek eye care. Patients may also be referred to eye care professionals by other health care disciplines for management of symptoms. Therefore, optometrists are on the frontline in initiating and implementing the proper care for these individuals.25 To appropriately manage a patient with ocular manifestations of MG one must be familiar with the clinical presentations, possible differential diagnoses, diagnostic tests, and treatments. Clinical presentations are summarized in Table 2.

Table 2. Clinical presentation of myasthenia gravis1, 2, 3, 4, 5, 6, 7, 8, 9, 49, 50, 51, 52, 53, 54
OcularSystemic

Variable symptoms (worsening with fatigue)
Blurred vision

Double vision

Droopy eyelid



Fluctuating symptoms, worsen with repetition
Weakness rather than fatigue is predominant

Facial, neck weakness

Difficulty with articulation (dysarthria)

Difficulty swallowing (dysphagia)

Weak voice (dysphonia)

Difficulty climbing stairs, rising from chair

Respiratory weakness

Generalized fatigue

Normal sensation



Signs
Heterophoria

Accommodative infacility

Worsening ptosis with prolonged upgaze



Signs
Head droop

Dysarthria

Dysphonia

Proximal limb weakness


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In-clinic diagnostic screening for myasthenia gravis 

Recognition of the disease from its ocular manifestations can be achieved easily by utilizing clinical or “in-office” screening tests that primary care practitioners, such as optometrists, can perform easily. Clinical diagnostic screening tests are shown in Table 3.

Table 3. Systemic diagnostic tests and in-clinic screening for myasthenia gravis2, 6, 7, 11, 12, 20, 21, 27, 28
ProcedureProcedure characteristicsResults indicative for MG
Systemic diagnostic tests
Tensilon (edrophonium chloride)Injection of acetylcholine sterase inhibitorImprovement in muscle weakness of the affected muscle groups
Acetylcholine receptor antibodiesBlood titer that specifically identifies this antibodyBlood serum level >0.2 mmol/mL
Anti-MuSK antibodiesBlood titer that specifically identifies the a muscle-specific receptor tyrosine kinaseAny detection of the antibody in blood serum
Thyroid functionBlood test to measure thyroid-stimulating hormone, thyroxine, and Triiodothyronine (T3)Detection of either hypo- or hyperthyroidism
Computed tomography or magnetic resonance imagingRule out thymus gland abnormalityDetection of thymus gland abnormalities
Muscle biopsyAllows for the quantification of acetylcholine receptorsWithin normal limits of receptors found with weakness consistent with MG
Single-fiber electromyogramSelf-explanatory: steadily becoming the gold standard to rule out neuromuscular junction transmission defects in generalized MG, but difficult to perform with regard to ocular MG because it is difficult to isolate ocular musclesNot a specific test for MG
100% sensitivity
False-negatives are not uncommon; ∼15%
requires a highly specialized laboratory
Clinical/”in-office” diagnostic screening procedures
Ice testPatient applies an ice pack on ptotic eye for ∼2 minutesImprovement in ptosis of at least 2 mm
Sleep testPatient rests in a darkened, quiet room, for ∼30 minutesImprovement in ptosis
Fatigue testHave the patient engage in physical activity; most often climbing a flight of stairsA worsening is any signs and/or symptoms; most often a ptosis
Cogan's lid twitch testPatient forcibly closes the eyes for ∼10 to 30 seconds, then opens to look in primary gaze
-or-
patient looks in downgaze for ∼10 to 30 seconds, then immediately saccades back into primary gaze		Short-lived, “twitch” improvement in ptosis when patient returns to primary gaze
Orbicularis weaknessPatient forcibly squeezes eyelids shut, tightly, and the examiner then tries to overcome the blepharospasm with finger pressure onlySuccessfully overcoming blepharospasm
Lid fatiguePatient looks in upgaze for ∼2 minutes
Patient looks in upgaze for 30 seconds then returns to primary gaze		1. Increasing ptosis while patient maintain their gaze upwards
2. An increase in ptosis (Darple's sign) or an appreciable lid lag
Curtains signExaminer raises the eyebrow or upper lid of the more ptotic eyeAn increase in the ptosis of the contralateral eye as a result of Hering's law

The ice test is performed by having the patient apply an ice pack or cold compress to the ptotic eye for approximately 2 minutes. The localized decrease in temperature slows the breakdown of acetylcholine, increasing availability at the synapse. A positive result is an improvement in the ptosis of greater than 2 mm.1, 7, 12

The sleep test is performed by having the patient rest in a quiet, darkened room for approximately 30 minutes. The mechanism of this test is 2-fold. First, having the patient rest, essentially motionless, reduces the demand for acetylcholine. Second, the 30-minute time elapse allows for the replenishing of available acetylcholine.6, 7 A positive result is any improvement in ptosis.1, 7, 12

In comparing the ice versus rest test, 1 study concluded that the ice test is much more effective.20 It is hypothesized that the additional mechanism in the sleep test is also employed in the ice test.20 Therefore, the ice test theoretically embodies both the effective mechanisms of rest and temperature reduction.

Conversely to the ice and sleep test, the fatigue test is performed in an antagonistic fashion in an attempt to worsen the ocular signs or symptoms rather than see an improvement. The test is performed by having the patient engage in any form of physical activity, such as climbing a flight of stairs, followed by re-evaluation of signs and symptoms of ocular MG. The most common sign observed is the worsening of the ptosis.

Another diagnostic test is the Cogan's lid twitch. Cogan's lid twitch test is performed in 1 of 2 ways. One way is to have the patient forcibly close the eyes for 10 to 30 seconds then look back into primary gaze.6 The second way is to have the patient look down for 10 to 30 seconds and then immediately look back to primary gaze.12 A positive result is a temporary improvement of lid opening (i.e., upper lid twitch).6, 12 This short-lived improvement is secondary to the voluntary maximal contraction of the antagonistic orbicularis oculi muscles, which results in a temporary recovery of phasic, more than tonic, motor units in the levator palpebrae muscles.26

The orbicularis weakness test is performed by having the patient tightly squeeze the eyelids shut and then the examiner uses finger pressure to try and overcome the blepharospasm.1, 12 A positive result is a successful attempt in overcoming the blepharospasm.1, 12 Under normal circumstances, the blepharospasm should not be overcome easily by finger pressure alone, but because of the patient's inability to sustain maximal muscle contraction secondary to MG, this can be achieved.1, 12

The lid fatigue test is performed by having the patient look in extreme upgaze for approximately 1 to 2 minutes.1, 12 This action assesses the fatigability of the levator muscle.12 A positive result is an increasing ptosis while eyes are in upgaze.1, 12 In addition, another option is to have the patient sustain an extreme upgaze for 30 seconds and then return to primary gaze. A positive result is when the patient shows a lid lag or an increase in ptosis, known as Darple's Sign.

Curtain sign, also known as enhanced ptosis or paradoxical ptosis, can be elicited by the examiner raising the eyebrow or upper lid of the more ptotic eye.1, 12 A positive result is a significant increase in the ptosis of the contralateral eye. This result is explained by Hering's law, in which paired ocular muscles receive equal innervation.27

In addition to the aforementioned tests, rudimentary accommodative and binocular vergence testing could further assess ocular fatigue, which may be associated with MG.1 Such tests include monocular accommodative amplitudes, accommodative facility, near point convergence with stamina, as well as positive and negative fusional vergences.

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Systemic investigation 

The customary systemic diagnostic tests for MG require an injection, imaging, or extensive laboratory work. The diagnostic procedure that is considered the gold standard is the Tensilon test.12 The Tensilon test is an intramuscular injection of an acetylcholine stearase inhibitor that inhibits the breakdown of acetylcholine, thus making a greater amount of acetylcholine available for synapse in the neuromuscular junction. A positive result for MG is an improvement of the ptosis or ophthalmoplegia after the injection.4, 12 Procedures for systemic investigation are summarized in Table 2.

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Systemic management for myasthenia gravis 

Treatment for systemic or generalized MG includes a variety of options but remains primarily systemic medication.8, 26 First-line therapy typically consists of an acetylcholinesterase inhibitor like pyridostigmine bromide.4, 8, 12 Another option is immunosuppressant therapy such as prednisolone, cyclosporine, azathioprine, methotrexate, and mycophenolate mofetil.4, 8, 12 More extensive measures attempted in the past include plasmapheresis (or plasma exchange) and IVIg injections.27, 28, 29, 30

Thymectomy, the surgical removal of the thymus gland, is also an effective and accepted treatment for generalized MG.22, 31, 32, 33, 34 Thymic pathology is thought to be an important mediator in the development of MG because of the thymus' role in T-lymphocyte education and self-tolerance.35 Recent theories suggest thymectomies could be performed for early presentations of ocular MG to prevent or slow the disease progression as well as the addition of immunosuppressive therapy only if proven necessary.22, 24, 35 Therefore, thymectomies are often performed on young individuals in the early stages of MG regardless of the presence of a tumor.1 Additionally, if there is found to be thyroid involvement, a thyroidectomy is a viable treatment option.4, 12, 18

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Ocular management 

Treatment for ocular MG specifically may include all the systemic investigatory options, because a reported 50% to 60% of purely ocular MG cases will eventually progress to generalized MG.5 Nevertheless, ocular MG treatments consist of both surgical and nonsurgical options. The optometrist may also play an important role in the nonsurgical management of ocular MG. Ocular MG treatments should include refraction, achieving best-corrected visual acuity (BCVA) and accommodation/vergence testing.1 Yet, the main goal is geared toward management of the ptosis and diplopia. With regard to diplopia, the standard treatment is occlusion and prisms.36 However, prism treatment is limited by the disease's variability.18, 37 In addition, diplopia may be minimized only in primary gaze.38 An alternative treatment would be the use of the patient's head turn, turning the head so the eyes are positioned in the field of gaze that permits fusion.37, 38 Occlusion has been another widely recommended means for managing variable diplopia.37, 38, 39 A commonly recommended option for occlusion is an eye patch, but patients may find this objectionable.37, 38, 40 An alternative method for occlusion that may be more acceptable would be “fogging” one eye with a plus or minus lens over the habitual prescription.37 A frosted lens can be fabricated by an optical laboratory; however, a conventional spectacle lens can be “frosted” temporarily with the use of opaque cellophane tape or fingernail polish.37

Surgical and nonsurgical treatment options may be used for the management of the ptosis. Surgical options for myogenic ptosis are ptosis repair surgery, blepharoplasty, frontalis suspension for which a Tutoplast sling (Tutogen Medical, Inc., West Paterson, New Jersey) can be utilized, external levator advancement, and tarsomyectomy.32, 41, 42, 43, 44, 45, 46, 47, 48, 49 A nonsurgical option is botulinum toxin type A injection to temporarily treat myogenic ptosis.8 One simple solution for ptosis is to tape the eyelid using dermatologic tape.37 One drawback to this is corneal exposure and the need for topical lubrication. Outside of surgical intervention, an option that is widely available for management of ptosis is the ptosis crutch. A ptosis crutch is an inexpensive, noninvasive option for those with ptosis from myasthenia.

A ptosis crutch is a pliable Teflon or plastic-coated stainless steel wire mounted or soldered onto a spectacle frame, which is formed to contour to the patient's need.50, 51 The advantages of a ptosis crutch are that it is effective, cost-efficient, noninvasive, and temporary. Disadvantages include possible dry eye complications and mild physical discomfort.

Fitting the ptosis crutch is simple because it is the same as it is for regular spectacles. A frame appropriate for the patient's facial features or structure is selected. Once selected, the manufacturing laboratory of choice needs to be contacted in advance, alerting the laboratory that a ptosis crutch is needed to be mounted in addition to fabricating the lenses. Most laboratories are capable of providing this service “in-house,” but some may require the frame be shipped to a partner facility. Ordering ptosis crutches is a simple process that only requires good communication with the manufacturing laboratory.

Once the finished product is received, patient-specific adjustments can be made to both the frames and crutches. Successful adjustments to the crutches are accomplished by having the patient subjectively inform the adjuster of the position in which the eyelids are most comfortable and clear of the pupil. Then the adjuster manually adjusts the crutches to maintain the position identified by the patient.

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Conclusion 

Because of the increased likelihood of ocular involvement in patients with MG, optometrists are quite likely to be the first to encounter an undiagnosed patient or be involved in the treatment of the patient. Primary care optometrists must be able to recognize the disease and establish a tentative diagnosis by utilizing diagnostic clinical screening tests. Confirmation of the diagnosis must be done, preferably by a neurologist, and should involve laboratory tests as well as a Tensilon test.

The optometrist may also be involved in the management of ocular manifestations of myasthenia. Correction of diplopia, especially with prisms, may be challenging given the variability of the disease. Therefore, it is recommended that occlusive therapy be attempted as an initial treatment for diplopia.52, 53, 54 A ptosis crutch utilized with ocular lubrication may provide a noninvasive solution for ptosis, especially in cases in which the patient refuses surgery or when surgery is contraindicated.50, 51

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References 

  1. Colavito J, Cooper J, Ciuffreda K. Non-ptotic ocular myasthenia gravis: a common presentation of an uncommon disease. Optometry 76(7): 363-75.
  2. National Institute of Neurological Disorders and Stroke Publication 99-768. Available at: http://www.ninds.nih.gov/disorders/myasthenia_gravis/myasthenia_gravis.htm. Last accessed April 15, 2008.
  3. Donati F, Bevan D. Neuromuscular blocking agents. In: Clinical Anesthesia. ed 5. Chapter 16. Lippincott Williams & Wilkins; 2006;
  4. Palace J, Vincnet A, Beeson D. Myasthenia gravis: diagnostic and management dilemmas. Curr Opin Neurol. 2001;14:583–589
  5. Homel P, Kupersmith M. Development of generalized myasthenia gravis in patients with ocular myasthenia gravis. Arch Neurol. 2003;60(10):1491–1492
  6. Toyka K. Ptosis in myasthenia gravis: extended fatigue and recovery bedside test. Neurology. 2006;67(8):1524
  7. Reddy A, Backhouse O. “Ice-on-eyes,” a simple test for myasthenia gravis presenting with ocular symptoms. Practical Neurology. 2007;7(2):109–111
  8. Benatar M, Kaminski H. Evidence report: The medical treatment of ocular myasthenia (an evidence-based review): Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2007;68(24):2144–2149
  9. Rudnicki S. Lamber-Eaton Myasthenic syndrome with pure ocular weakness. Neurology. 2007;68(21):1863–1864
  10. Rowland R, Sparr S. Head-drop and shortness of breath as a presentation of myasthenia gravis. J Am Geriatr Soc. 2007;55(4):S116
  11. Hilton-Jones D, Palace J. The management of myasthenia gravis. Practical Neurology. 2005;5:18–27
  12. Golnik K. How to diagnose and treat myasthenia gravis. Rev Ophthalmol. 2002;9(10):219
  13. Scherer K, Bedlack R, Simel D. Does this patient have myasthenia gravis?. JAMA. 2005;293(15):1906–1914
  14. Morris O, O'day J. Fatiguable ptosis and pseudoretraction caused by myasthenia gravis. Clin Exp Ophthalmol. 2004;32:303–304
  15. Shaw J. When muscles falter: update on myasthenia gravis. Clinical update: neuro-opthalmology. Available at: http://www.aao.org/publications/eyenet/200607/neuro.cfm. 2006. Last accessed November 12, 2009
  16. Golnik K, Pena R, Lee A, et al. An ice test for the diagnosis of myasthenia gravis. Ophthalmology. 1999;106(7):1282–1286
  17. Ubogu E, Kaminski H. The preferential involvement of extraocular muscle by myasthenia gravis. Neuro-ophthalmology. 2001;25(4):219–228
  18. Kennard C. Examine eye movements. Practical Neurology. 2007;7:326–330
  19. Chan J, Orrison W. Ocular myasthenia: a rare presentation with MuSK antibody and bilateral extraocular muscle atrophy. Br J Ophthalmol. 2007;91:842–843
  20. Kubis K, Danesh-Meyer H, Savino P, et al. The ice test versus the rest test in myasthenia gravis. Ophthalmology. 2000;107(11):1995–1998
  21. Gilbert M, De Sousa E, Savino P, et al. Ocular myasthenia gravis treatment: the case against prednisone therapy and thymectomy. Arch Neurol. 2007;64(12):1790–1792
  22. Chavis P, Stickler D, Walker A. Immunosuppressive or surgical treatment for ocular myasthenia gravis. Arch Neurol. 2007;64(12):1792–1794
  23. Kupersmith M, Latkany R, Homel P. Development of generalized disease at 2 years in patients with ocular myasthenia gravis. Arch Neurol. 2003;60(2):243–248
  24. Kaminski H, Daroff R. Treatment of ocular myasthenia: steroids only when compelled. Arch Neurol. 2000;57(5):752–753
  25. Bennett D, Mills K, Riordan-Eva P, et al. Anti-MuSK antibodies in a case of ocular myasthenia gravis. J Neurol Neurosurg Psychiatry. 2006;77(4):564–565
  26. Sommer N, Sigg B, Melms A, et al. Ocular myasthenia gravis: response to long term immunosuppressive treatment. J Neurol Neurosurg Psychiatry. 1997;62(2):156–162
  27. Glaser J. Infranuclear disorders of eye movements. In:  Tasman W,  Jaeger EA editor. Duane's clinical ophthalmology. Philadelphia: Lippincott-Raven; 1995;p. 1–56
  28. Howard J. Intravenous immunoglobulin for the treatment of acquired myasthenia gravis. Neurology. 1998;51(6):Suppl. 5:S30–S36
  29. Hilkevich O, Drory V, Chapman J, et al. The use of intravenous immunoglobulin as maintenance therapy in myasthenia gravis. Clin Neuropharmacol. 2001;24(3):173–176
  30. Meche F, Schmitz P. A randomized trial comparing intravenous immune globulin and plasma exchange in Guillian-Barre syndrome. Dutch Guillian-Barre Study Group. N Engl J Med. 1992;326(17):1123–1129
  31. Roberts P, Venuta F, Rendina E, et al. Thymectomy in the treatment of ocular myasthenia gravis. J Thorac Cardiovasc Surg. 2001;122(3):562–568
  32. Lauriola L, Ranelletti F, Maggiano N, et al. Thymus changes in anti-MuSK-positive and –negative myasthenia gravis. Neurology. 2005;64(3):536–538
  33. Mori T, Nomori H, Ikeda K, et al. The distribution of parenchyma, follicles, and lymphocyte subsets in thymus of patients with myasthenia gravis, with special reference to remission after thymectomy. J Thorac Cardiovasc Surg. 2007;133(2):364–368
  34. Bachmann K, Burkhardt D, Schreiter I, et al. Thymectomy is more effective than conservative treatment for myasthenia gravis regarding outcome and clinical improvement. Surgery. 2009;145:392–398
  35. Agius M. Treatment of ocular myasthenia with corticosteroids: yes. Arch Neurol. 2000;57(4):750–751
  36. Morris O, O'Day J. Strabismus Surgery in the management of diplopia caused by myasthenia gravis. Br J Ophthalmol. 2004;88:832–850
  37. Bienfang DC. Neuroophthalmology. In:  Samuels MA editors. Manual of neurologic therapeutics. Ed 7.. Philadelphia: Lippincott Williams & Wilkins; 2004;
  38. Calvert PC. Disorders of neuromuscular transmission: myasthenia gravis. In:  Miller NR,  Newman NJ editor. Walsh & Hoyt's clinical neuro-ophthalmology. Philadelphia: Lippincott Williams & Wilkins; 2005;p. 1059–1065
  39. Penn AS, Rowland MP. Myasthenia gravis. In:  Rowland MP editors. Merritt's neurology. Ed 11.. Philadelphia: Lippincott Williams & Wilkins; 2005;p. 877–884
  40. Amato MM, Monheit B, Shore JW. Neuro-ophthalmology; examination of the ptosis patient. In:  Tasman W editors. Duane's clinical ophthalmology. vol. 5:Philadelphia: Lippincott, Williams, & Wilkins; 2009;
  41. Periman L, Sires B. Floppy eyelid syndrome: a modified surgical technique. Ophthalm Plast Reconstruct Surg. 2002;18(5):370–372
  42. Sakol P, Mannor G, Massaro B. Congenital and acquired blepharoptosis. Curr Opin Ophthalmol. 1999;10:335–339
  43. Shields M, Putterman A. Blepharoptosis correction. Curr Opin Otolaryngol Head Neck Surg. 2003;11(4):261–266
  44. Eliasoph I. RE: “Surgical correction of blepharoptosis in patients with myasthenia gravis.”. Opththal Plast Reconstr Surg. 2002;18(4):312–313
  45. McCord C, Seify H, Codner M. Transblepharoplasty ptosis repair: three-step technique. Plast Reconstruct Surg. 2007;120(4):1037–1044
  46. Seider N, Beiran I, Kaltreider S. One medial triangular Tutoplast sling as a frontalis suspension for adult myogenic blepharoptosis. Acta Ophthalmologica Scand. 2006;84:121–123
  47. Wong V, Beckingsale P, Olley C, et al. Management of myogenic ptosis. Ophthalmology. 2002;109(5):1023–1031
  48. Bernardini F, Concillis C, Devoto M. Frontalis suspension sling using a silicone rod in patients affected by myogenic blepharoptosis. Orbit. 2002;21(3):195–198
  49. Gausas R, Goldstein S. Ptosis in the elderly patient. Int Ophthalmol Clin. 2002;42(2):61–74
  50. Lapid O. Eyelid crutches for ptosis: a forgotten solution. Plast Reconstruct Surg. 2000;106(5):1213–1214
  51. Takagi S, Hosokawa K, Yano K, et al. Crutches glasses for blepharoptosis. Plast Reconstruct Surg. 2002;109(7):2605
  52. Bamford CR. Myasthenia gravis. In:  Domino FJ editors. The 5-minute clinical consult. Philadelphia: Lippincott, Williams, & Wilkins; 2007;p. 808–809
  53. Mazzoni P, Pearson TS, Rowland, LP, ed. Myasthenia gravis. In: Merritt's neurology handbook, Ed 2. Philadelphia: Lippincott, Williams, & Wilkins, 2006: 507–510.
  54. Loh A. Myasthenia gravis. In:  Schaider J,  Hayden SR,  Wolfe R, et al. editor. Rosen & Barkin's 5-minute emergency medicine consult. Ed 3.. Philadelphia: Lippincott, Williams, & Wilkins; 2007;p. 718–719

PII: S1529-1839(10)00334-9

doi:10.1016/j.optm.2009.09.023

Optometry - Journal of the American Optometric Association
Volume 81, Issue 9 , Pages 454-460, September 2010

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