THE ROLE OF THE ANTI GQ1B ANTIBODY IN DIFFERENTIAL. DIGNOSIS OF ACUTE OPTHALMOPARESIS
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1 THE ROLE OF THE ANTI GQ1B ANTIBODY IN DIFFERENTIAL. DIGNOSIS OF ACUTE OPTHALMOPARESIS Abstract Miller Fisher syndrome has a triad of total external ophthalmoplegia, ataxia and areflexia, Botulism is caused by a bacterial neurotoxin which is against proteins involved in presynaptic vesicle release. The usual clinical presentation is the involvement of cranial muscles and palsies with blurred vision, diplopia, ptosis, dilated pupils and facial paralysis. We aimed to make differantial diagnosis of Miller Ficher Syndrome and botilismus in an ophtalmoparethic patient. Case: A 67-year-old female patient presented with acute opthalmoparesis and a history diarrhea three days before, which was two days after consuming tinned food. Routine blood tests including syphilis serology, radiological and electroneurophysiological examination including cranial CT and MRI scans and electrocardiogram were normal. Cerebrospinal fluid studies including cytology were normal. After consulting with the infectious diseases department, crystallized penicillin treatment plus trivalent botulinum anti-toxin against toxins A, B and E were given. During his follow-up in the neurological intensive care unit, little change in his symptoms occurred other than the opthalmoparesis becoming symmetrical. A clinical diagnosis of Miller-Fisher Syndrome was reached through anti-ganglioside GQ1B and GM1 Ig G and M antibody investigations. The patient was treated with intravenous immunoglobulins two weeks after (in the late period) the symptoms started and he has recovered completely. Conclusion: Systemic autoimmune diseases should be considered in patients with bilateral opthalmoparesis. As in the present patient, the evaluation of specific antibodies helps in the diagnosis and thus early effective treatment is possible. Key words: Anti-ganglioside antibody, Botulism, Miller-Fisher syndrome, Opthalmoparesis Introduction Miller Fisher syndrome (MFS) was described as a triad of total external ophthalmoplegia, ataxia and absent deep tendon reflexes (areflexia) in It usually has a monophasic course and is a less commonly seen subtype of Guillain Barré syndrome (GBS). 1 In 1992 acute phase immu- Correspondence: Dr. Department of Neurology, Cathay General Hospital, Hsinchu Branch; No. 478, Sec. 2, Chunghua Rd., Hsinchu City, Taiwan googlejoseph@yahoo.com.tw 354
2 Antiganglioside antibody in Miller Fisher syndrome noglobulin G (IgG) antibodies to GQ1b ganglioside, found in over 90% of cases, have been reported as a highly specific serum marker for this syndrome. 2,3 Botulism is caused by a bacterial neurotoxin, typically botulinum toxin type A, B or E produced by Clostridium botulinum. This toxin is against proteins involved in presynaptic vesicle release. The usual clinical presentation is cranial muscle, e.g. extraocular muscle, palsies with blurred vision, diplopia, ptosis, dilated pupils and facial paralysis. Speaking and swallowing problems occur. Eventually flaccid limb paralysis and respiratory dysfunction may develop; the disease may be lethal. 4 In this report, a 67-year old female patient with external ophthalmoplegia is presented and the importance of anti GQ1b antibody titers in the differential diagnosis of MFS and Botulism is discussed. Case Report A 67-year-old female patient reported having diarrhea two days after eating tinned beans, followed by a hamburger and a toasted sandwich a few hours later. Two days after the beginning of the diarrhea, she started having fatigue, nausea and vomiting. Acute gastroenteritis therapy was started. One day after this she developed double and blurred vision, dizziness and a loss of balance. On admission, her eye movements were restricted on both sides, more prominent on the right skew deviation with mild left side ptosis, pupils were midriatic and unreactive to light. (Fig.1) Limb power was normal, tendon reflexes decreased and plantar responses were bilaterally flexor. Cerebellar tests, the sensory examination and the examination of other systems were normal. Routine blood tests including syphilis serology, radiological examination including cranial CT and MRI scans and electrocardiogram were normal. Cerebrospinal fluid (CSF) studies including cytology were normal; the CSF was clear, with normal opening pressure. Electroneurophysiological examination, motor nerve conduction studies, F waves, sensory nerve conduction studies and H reflexes were normal. On repetitive stimulation, Fig. 1. Three-step test: right superior oblique muscle palsy and left side oculomotor palsy, semiptosis: Right hypertropia (arrow): left gaze and right-heat tilt. 355
3 no decremental or incremental response was observed. The most likely differential diagnosis was between botulism and MFS. Stool and serum samples were sent for botulism toxin assay, antiganglioside GQ1B and GM1 Ig G and M antibodies. After consulting with the infectious diseases department, crystallized penicillin treatment plus trivalent botulinum anti-toxin against toxins A, B and E were given. During his follow-up in the neurological intensive care unit, little change in his symptoms occurred other than the opthalmoparesis becoming symmetrical. By ELISA method, anti-gq1b tilter was noted to have a remarkable elevation (>1:1200, normal range: 1:200) Intravenous immunoglobulin (IVIG) therapy (0.4 g/kg/day for five days) was started for the treatment of MFS. After the treatment, the eye movements improved, ptosis slowly resolved and diplopia disappeared. (Fig. 2) The tendon reflexes were present but still hypoactive on upper limbs. The patient is still under follow-up by our department. Right now, fourteen months after the beginning of the symptoms, she has no complaint and his neurological examination is normal except for hypoactive tendon reflexes. Discussion Guillain Barre syndrome is usually considered to be the prototype of post infectious neuroimmune disease. Epidemiological studies have indicated previous infection with bacteria like Campylobacter jejuni and viruses e.g. cytomegalovirus and Epstein Barr viruses. 5,6 It has several pathological subtypes, the most common Fig. 2. Eye position returns to normal after treatment. 356
4 Antiganglioside antibody in Miller Fisher syndrome being multifocal demyelinating polyneuropathy. Miller Fisher syndrome is a less commonly seen subtype with a classical triad of total external ophthalmoplegia, ataxia and areflexia. 7 Approximately 75% of the patients have a history of a viral infection within the last ten days. 8 Guillain Barre syndrome is the world s leading cause of acute autoimmune neuromuscular paralysis. Understanding the pathophysiological events of GBS, and improving immunotherapies are fundamental to improving the clinical outcome. 1 Recent research into GBS and MFS variant has focused on the forms mediated by anti-ganglioside antibodies in which correlations have been established between anti-ganglioside antibodies and specific clinical phenotypes, notably between anti-gm1/gd1a antibodies and the acute motor axonal variant and anti-gq1b/gt1a antibodies and MFS. 9,10 Anti-ganglioside antibodies like GM1, GM2, GD1A, GD1B, GT1A, and GQ1B can arise through molecular mimicry with GBSassociated Campylobacter jejuni oligosaccharides. 11 In GBS the frequency of these antibodies varies from as 29-70%, patients with MFS have at a much higher frequency, probably around 95%. 12,13 The main principle in the therapy is careful intensive care and respiratory support when required. More specific treatment is also available. Clinical trials have shown that plasma exchange and IVIG shorten the recovery time if used early. 14,15 Plasma exchange removes the antibodies in the blood mediating the neuropathy, thus fighting against the continuous production of new autoantibodies. In a monophasic-acute disease like MFS, this seems to be effective, although a complete removal of all autoantibodies is impossible. 16 The mechanism of action of IVIG probably includes the blockage of Fc receptors, increased catabolism of autoimmune immunoglobulin, and possible roles in providing anti-idiotypic antibodies and in promoting remyelination. 1,15 In our case, significant improvement of symptoms was observed after the IVIG therapy. The prognosis in MFS, on the other hand, is usually good with a self-limiting course and a full resolution of symptoms in an average of 8-10 weeks. Yet not all cases of MFS are benign and some cases may progress to severe weakness and respiratory distress. The clinical pattern, primarily affecting extraocular muscle and cranial nerves, and the mode of paralysis in MFS are similar to those found with botulism. 17,18 Botulism is a potentially life-threatening condition caused by botulinum neurotoxin that acts against proteins involved in presynaptic vesicle release. The neurotoxin is formed during the growth of the spore-forming bacterium Clostridium botulinum. It can enter the body via the gastrointestinal tract or through mucous membranes i.e. the eyes or the respiratory tract. Toxin production from C. botulinum, C. butyricum, or C baratii spores may also occur in vivo. 19 The most common form is food-borne botulism which follows the ingestion of food containing preformed botulinum neurotoxin. 20 Botulism can also occur as a result from toxin formation from spores in vivo, most commonly in infants. Other forms include wound botulism and infectious botulism to which adults with altered intestinal flora due to abdominal surgery, prolonged antimicrobial treatment or gastrointestinal wounds and abscesses are particularly vulnerable. 20 Inhalation botulism may result from aerosolization of the neurotoxin, that it be absorbed from the airway. Finally, iatrogenic botulism can develop rarely as a consequence of therapeutic or accidental injection of the neurotoxin. 19 The differential diagnosis includes GBS, MFS, chemical intoxication, stroke, and other food poisonings. Being a potentially lethal condition, the need for a rapid diagnosis and therapy to save the patient is obvious. Early diagnosis is important because antitoxin theraphy is most when administered early and recovery time is several weeks to months, depending on the amount of toxin ingested and the toxin type. 20 The symptoms seen in MFS are related to the third, fourth, and sixth cranial nerves. It has been proposed by some biochemical studies and supported by immono-histochemical studies that these cranial nerves contain a considerable amount of GQ1b. The serum of these individuals contains 357
5 a blocking factor in the IgG fraction which acts similar to some biological toxins. The distal nerve terminal lacks the blood-nerve barrier and is accessible for circulating antibodies. So the cranial nerve findings may be the result of the direct action of the antibodies on the neuromuscular junction between the cranial nerves and ocular muscles. 1,18 The concept of anti-gq1b IgG antibody syndrome has been introduced after the description of atypical cases like the ones discussed above, with features of MFS, ataxic GBS and other clinical pictures plus positive anti-ganglioside antibodies. These patients seem to share a common antibody against GQ1b and their illness has a relatively mild course. The case described in this report may be accepted as one with this syndrome as his illness had a mild and benign course. As a conclusion, systemic autoimmune diseases should be considered in patients with bilateral opthalmoparesis. Occasionally botulism is in the differential diagnosis. As in the present patient, the evaluation of specific antibodies helps in the diagnosis and thus early effective treatment is possible. References 01. Winer JB.: Guillain Barré syndrome. J Clin Pathol: Mol Pathol 2001;54: Chiba A, Kusunoki S, Shimizu T, et al. Serum IgG antibody to Ganglioside GQ1b is a possible marker of Miller Fisher syndrome. Ann Neurol 1992;31: Willison HJ, O Hanlon GM. The Immunopathogenesis of Miller Fisher syndrome. Journal of Neuroimmunology 1999;100: Dowling PC, Cook SD. Role of infection in Guillain- Barre syndrome: Laboratory confirmation of herpes viruses in 41 cases. Ann Neurol 1981;9: Chang VH, Robinson LR. Serum positive botulism with neuropathic features.arch Phys Med Rehabil 2000;81: Rees JH, Gregson NA, Hughes RA. Anti-ganglioside GM1 antibodies in Guillain-Barre syndrome and their relationship to Camplybacter jejeuni infection. Ann Neurol 1995;38: Lee SH, Lim GH, Kim JS, et al.hk. Acute ophthalmoplegia (without ataxia) associated with anti- GQ1b antibody. Neurology 2008;5;71: Winer JB, Hughes RA, Anderson MJ, et al. A prospective study ofacute idiopathic neuropathy.ii.antecedent events. J Neurol Neurosurg Psychiatry 1988; 51: Mori M, Kuwabara S, Fukutake T, et al.clinical features and prognosis of Miller Fisher syndrome. Neurology 2001;56: Caudie C, Schandelong A, Rapoport F, et al.anti- GD1b IgG positive case of overlapping Ficher s and Guillain-Barre syndromes. Ann Biol Clin (Paris) 2004; 62: Willison HJ, Plomp JJ. Anti-ganglioside antibodies and the presynaptic motor nerve terminal. Ann N Y Acad Sci 2008;1132: Willison HJ,Veitch J, Paterson G,et al. Miller Fisher syndrome is associated with serum antibodies to GQ1b ganglioside. J Neurol Neurosurg Psychiatry 1993;56: Kusunoki S. Antiganglioside antibodies in the pathogenesis of autoimmune neuropathies. Rinsho Shinkeigaku 1999;39: van der Meche FG, Schmitz PI. Arandomized trialcomparing intravenous immunglobulin and plasma exchange in Guillain-Barre syndrome. Dutch Guillain- Barre study group.n Engl J Med 1992;326: Plasma Exchange/Sandoglobulin Guillain-Barr? Syndrome Trial Group. Randomised trial of plasma exchange, intravenous immunoglobulin, and combined treatments in Guillain-Barré syndrome. Lancet 1997;349: Lehmann HC, Hartung HP, Hetzel GR, et al. Plasma Exchange in Neuroimmunological Disorders Part 1: Rationale and Treatment of Inflammatory Central Nervous System Disorders. Arch Neurol 2006;63: Buchwald B, Bufler J, Carpo M., et al. Combined pre- and postsynaptic action of IgG antibodies in Miller Fisher syndrome. Neurology 2001;56: Yavaşcan Ö, Sütçüoğlu S, Dizdarer G, et al. Miller- Fisher sendromu - Iki vaka takdimi. Çocuk Sağlığı ve Hastalıkları Dergisi 2004;47: Chadderdon SM., Hagg DS, Jacoby DB.Botulism Secondary to Clostridium Baratii Type F Toxin. Chest 2004;126:4: Supplement 947S. 20. Dembek ZF, Smith LA, Rusnak JM. Botilism:cause, effects, diagnosis, clinical and laboratory identification, and treatment modalities. Disaster Med Public Health Prep
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