Ataxia, Ophthalmoplegia, and Areflexia: What Would You Think?

Karsan, N.; Fletcher, P.; Bodi, I.; MacDonald, B. K.

doi:https://doi.org/10.1155/2012/150813

Case Reports in Neurological Medicine

On this page

Abstract Case Discussion Conclusion References Copyright Related Articles

Case Report | Open Access

Volume 2012 | Article ID 150813 | https://doi.org/10.1155/2012/150813

Ataxia, Ophthalmoplegia, and Areflexia: What Would You Think?

N. Karsan,¹P. Fletcher,¹I. Bodi,²and B. K. MacDonald¹

Academic Editor: A. Fasano, A. Atri

Received05 Mar 2012

Accepted28 Apr 2012

Published27 Jun 2012

Abstract

We present here a case of carcinomatous meningitis presenting as Miller Fisher syndrome (MFS). There are four further cases described in the literature with evidence of tumour invasion within the central nervous system (CNS) shown either in cerebrospinal fluid examination or on histology. There are further five cases described in which an association between cancer and a Miller Fisher phenotype has been shown. Some of these have identified antiganglioside antibodies in the serum and, in one case, also showed antibodies deposited within the primary tumour itself. This raises a question as to whether there is a paraneoplastic form. It would be informative when further cases present in this way to histologically examine for malignant CNS invasion, and the presence of antiganglioside antibodies in both the malignant primary and areas of nervous system thought to be affected by MFS.

1. Case

A forty-four-year-old man, who was previously fit and well, presented to Accident and Emergency with a three-day history of fever, abdominal pain, headache, and vomiting nine days after returning from a cycling tour in rural India. There was nothing significant to find on examination, and he was afebrile.

Basic blood tests and cultures showed a mildly raised white cell count and aspartate transaminase (AST) only. An ultrasound scan of the abdomen showed widespread lymphadenopathy in the epigastrium, mesentery, and iliac and para-aortic areas, which was confirmed on CT. Five days after his admission, he developed a complex opthalmoplegia, mild dysphagia, lower limb weakness with areflexia in the upper and lower limbs, and ataxia. There was no sensory involvement, and cognition was normal. Nerve conduction studies showed a motor neuropathy in keeping with the clinical picture of an MFS. Intracranial CT and MRI with contrast were normal, apart from some nonspecific increased signal within the medulla on T2 imaging. Antiganglioside antibodies were negative. A lumbar puncture showed a normal opening pressure and protein, but 35 white cells (90% lymphocytes, 10% polymorphs) and glucose of 2.8 (no matched sample sent) and no organisms on Gram stain. CSF cytology was unremarkable.

Following the ultrasound and CT findings, he was started on antituberculous medication, and following the suspected diagnosis of MFS, he was also started on intravenous immunoglobulin. He went on to have a diverse number of problems which failed to reach a unifying diagnosis. These occurred in quick succession and included(i)subclavian vein thrombus,(ii)sinus tachycardia of 120–140 beats per minute with an ECG showing inferolateral ischaemia. An echo at this time revealed mild inferior wall hypokinesis and a small pericardial effusion,(iii)peripheral oedema,(iv)acure renal failure causing ureteric obstruction requiring a nephrostomy,(v)respiratory arrest leading to High Dependency Unit admission.

A postmortem examination revealed a poorly differentiated signet cell adenocarcinoma within the pancreas and stomach with diffuse infiltration into the adrenal glands. There was extensive spread within the lymphatic and vascular channels with perineural invasion. The lungs showed multiple small thromboemboli, in keeping with pulmonary microembolisation. A few tumour cells were evident within the thromboemboli. The brain slices showed widespread signet ring carcinoma infiltration into the leptomeninges and brain parenchyma, and in the Virchow-Robin spaces and basilar artery, with occasional small branches of the vertebral artery showing thrombotic occlusion (Figure 1). One sample contained part of the hypoglossal nerve, which showed heavy perineural infiltration (Figure 2).

2. Discussion

Secondary invasion of the leptomeninges by systemic cancer was first described by Eberth in 1870 [1], but the term carcinomatous meningitis was not coined until 1912 [2]. Various terms are now used, including neoplastic or metastatic meningitis, to reflect that meningeal invasion can occur secondarily to any form of malignancy. Prior to the advent of CT in the 1970s, myelography was the main imaging modality of choice, and diagnosis was therefore rare. More sophisticated imaging techniques, greater clinical awareness, and the development of better systemically (if not necessarily centrally) acting chemotherapeutic agents, have led to longer life expectancy in systemic malignancies and therefore an increase in the incidence of the condition [3].

Incidence rates vary depending on the case series studied. It is generally accepted that about 5% of patients suffering from metastatic malignancy [4–6] are affected, but estimates are as high as 5–15% for leukaemias and lymphomas, and 1-2% in patients with primary brain tumours [7]. In one postmortem series, patients with known cancer and neurological signs had leptomeningeal involvement in up to 20% of cases [8–10]. The most common type of tumour to metastasise to the leptomeninges is adenocarcinoma or signet ring cell carcinoma as a subtype. In several large series, breast cancer accounted for the majority of cases (11–64%), followed second by lung cancer (14–29%) and third by melanoma (6–18%) [7, 8, 11]. However, these series are dated, and current incidence rates may be different.

Systemic tumour cells have been shown to most commonly enter the CNS via either the arachnoid vessels or choroid plexus following haematological dissemination in both humans [12] and experimental models [13, 14]. Less frequently invasion occurs by infiltration along perineural or perivascular spaces [15–17] or direct spread from parenchymal lesions. The most common sites of deposition are around the skull base, the dorsal surface of the cord, and the cauda EQUINA [7, 18]. It has been postulated that this distribution reflects slower CSF flow around these areas coupled with gravity effects leading to tumour cell deposition. Interestingly, in one study, CSF examination from concomitant ventricular and lumbar sampling showed a discrepancy of positive lumbar, with negative ventricular, cytology in 30% of cases [8].

The clinical presentation can arise from direct cranial or spinal nerve involvement or from complications caused by obstruction of CSF outflow, usually secondary to basal meningitis. In a series of 140 patients [5], the most frequent symptoms were gait problems (46%), headache (38%), altered mental state (25%), and pain and weakness (22%). The most frequent signs were lower motor neuron weakness (78%), absent reflexes (60%), abnormal mental state (50%), extensor plantars (50%), dermatomal sensory loss (50%), ocular paralysis (30%), and facial weakness (25%).

Our patient presented with an ataxia, generalised areflexia, and complex opthalmoplegia mimicking a Miller Fisher syndrome. As can be deducted from the above data, absent reflexes and ocular paresis are fairly common in the cases described, so it may be that his clinical presentation can be fully explained by direct meningeal invasion along the neuroaxis. However, the question arises as to whether this presentation of an exact phenotype of what is thought to be an antibody-mediated syndrome (MFS) suggests a paraneoplastic component to MFS.

Miller Fisher originally described the triad of ataxia, areflexia, and opthalmoplegia in 1956 [19]. The syndrome is thought to be autoimmune in origin, secondary to molecular mimicry between infectious organisms and host gangliosides. For example, with Campylobacter jejuni, a bacterium often implicated, antibodies are found which cross-react with lipopolysaccharides on the bacterial surface and host gangliosides GQ1b/GT1a [20]. Anti-GQ1b gangliosides were first described in Miller Fisher syndrome in 1992 [21], and a strong association was found, with between 83% [22] and 100% (Willison and Veitch, 1994) of cases being positive for GQ1b. However, GQ1b antibodies are not specific to Miller Fisher syndrome, and are found in cases of Bickerstaff’s encephalitis (65%) and Guillian-Barré Syndrome (25%), and anti-GQ1b antibodies cross-react with other gangliosides such as GD1b, GT1a, and GD3 in approximately 50% of cases [23]. An association of a predominant oropharyngeal weakness with anti-GT1a seroreactivity, and ophthalmoplegia with anti-GQ1b within the Miller Fisher phenotype, has been described [24–26].

It is unclear whether the pathology of MFS is centrally or peripherally mediated [27], with central nervous system (CNS) involvement clinically (supranuclear palsy and intranuclear opthalmoplegia [28]) and electrophysiologically (abnormal visual, somatosensory, and auditory-evoked potentials) recorded in some cases [29, 30]. The strong association of GQ1b antibodies in Bickerstaff’s encephalitis [31, 32], which in addition to a Miller Fisher picture also has superimposed CNS dysfunction, may also add to the idea of both a central and peripheral role to the pathology [33]. High levels of GQ1b have been found both in the nodes of Ranvier [34, 35] and in the nerve trunks [36] of the extraocular cranial nerves (III, IV, and VI) relative to the other cranial or spinal nerves, and this was thought to help explain the ophthalmoplegia seen. However, antiganglioside antibodies have been found to bind to nodes of Ranvier of other nerves and in mouse sciatic nerves [37] (although here this fixation had no effect on the conduction velocities, so the pathological implication of this is not clear), and GQ1b has also been shown to be present at high levels in other unaffected sites. The neuromuscular junction (NMJ) may also be a site of target. In mouse hemidiaphragm preparations treated with anti-GQ1b antibody-positive sera, a temporary increase in acetylcholine release at NMJ is observed [38], and anti-GQ1b antibodies cause structural and functional changes in the NMJ [39]. In humans, abnormalities and electrical “jitter”, a sign of instability of the neuromuscular junction, which improved with clinical recovery, have been demonstrated on electromyography [40].

The anatomical basis of the ataxia is unclear. In Fisher’s original paper, he proposed the involvement of 1a afferent fibres, but studies have failed to stain GQ1b in them. Using body sway analysis, Kuwabara et al. [41] have further supported the concept that the ataxia is proprioceptive in origin. Muscle spindle bodies [42] and dorsal roots immunostain for anti-GQ1b antibodies (dorsal roots also stain for GD1b and GD3), but the physiological significance of this is unclear [43]. A study looked at immunostained human cerebellum with anti-GQ1b sera from three Miller Fisher patients [44], and western blot analysis has shown an increase in anticerebellar antibodies in Miller Fisher syndrome patients compared to GBS patients and controls [45]. Therefore, although the site of disease process remains unclear, there is evidence to suggest involvement of peripheral nerve, dorsal root ganglion, neuromuscular junction, and even cerebellum.

In cases such as this where direct evidence of CNS infiltration by malignant cells is seen, it may be that in addition to carcinomatous infiltration of the basal meninges or cauda EQUINA, direct infiltration of areas implicated in the Miller Fisher pathology, such as dorsal root ganglia and/or muscle spindles, leads to the clinical picture of Miller Fisher syndrome. It may well be that a presentation that so distinctly mimicking a syndrome caused by an antibody mediated response is due purely to the chance combination of areas involved. However, as discussed, Miller Fisher syndrome is autoimmune and has also been described in association with autoimmune conditions [46–49], so the exactly same presentation in carcinomatous meningitis raises the question as to whether there is a paraneoplastic component in some cases.

We have found four further cases in the literature where carcinomatous meningitis has presented as Miller Fisher syndrome (Table 1). The first two were described by Guarino et al. in 1995 [50], with the first secondary to a gastric adenocarcinoma and the second to likely myeloma. Both were diagnosed based on positive CSF cytology. Nakatsuji et al. [51] described a case of a woman with a month’s history of progressive ataxia, ophthalmoplegia, and areflexia with sensory involvement and sluggish pupillary reflexes on examination. The CSF was lymphocytic, but repeated cytological examination was negative. The MRI showed leptomeningeal enhancement, and a postmortem confirmed widespread leptomeningeal and cranial nerve infiltration by signet ring cell adenocarcinoma. Unfortunately, the family did not permit a postmortem of the rest of the body, so no primary was found. Csépány et al. [52] described a man who presented with a six day history of a progressive right third nerve palsy, bilateral lower motor neurone seventh nerve palsies, hyporeflexia, and ataxia. The CSF cytology showed “signet ring cells” and a few “large atypical cells.” Following this, a chest CT showed a lung mass which on biopsy was revealed to be adenocarcinoma. The CT of his head showed metastatic disease and some enhancement of the right Sylvian fissure. In all four cases, there was clear evidence of active malignancy within the central nervous system, either by CSF examination or by direct evidence of malignant infiltration. However, none of the studies measured anti-GQ1b antibodies, so it is impossible to know whether the clinical picture was accounted for solely by direct malignant infiltration, or whether there was an additional paraneoplastic component.

A literature search looking for an association between malignancy and Miller Fisher syndrome revealed five cases (Table 2) [53–57]. Apart from a small number of white cells (2–14) in the CSF in three cases, none had any direct evidence of malignancy within the CNS on cytology and none had additional information provided by postmortem examination. Anti-GQ1b antibodies were sent in all five cases and were positive in two. It is unclear from these cases which antiganglioside antibodies were tested for. In the cases by Aki et al. and Rubio-Nazabal et al., both patients improved clinically by treatment with plasmapheresis or intravenous immunoglobulin (IVIg), respectively. This may be suggestive of a paraneoplastic mechanism. The GQ1b antibodies were negative in the first case and strongly positive in the second. This patient then went on to have a relapse of Hodgkin’s lymphoma, and it would have been interesting to know if the antibody titres normalised with clinical improvement and then increased again with relapse of the malignancy. In our case, antiganglioside antibodies were negative, and there was no response to IVIg.

Interestingly, in the other case with positive anti-GQ1b antibodies (De Toni et al.) [54], as well as high circulating antigangliosides (including GD1a and disialo-GS), high levels of antibodies to the ganglioside GD1 were stained in the primary adenocarcinoma of the lung, with an absence of staining in neoplastic controls (i.e., bronchial adenocarcinoma without a Miller Fisher syndrome), which supports a paraneoplastic cross-reactivity concept.

There is some suggestion that there may be a paraneoplastic component, at least in some cases, which obviously potentially influences management. Therefore, in any future cases, it would be interesting and informative to firstly correlate any antiganglioside activity with time and secondly, in cases unfortunate enough to pass away, to obtain histology from other areas which may be affected by Miller Fisher syndrome, such as the dorsal horns and cerebellum, looking for direct malignant invasion to these areas, and whether these areas and the primary tumours (as in De Toni et al.’s case [54]) stain for antiganglioside antibodies.

3. Conclusion

There is therefore some suggestion that there may be a paraneoplastic component, at least in some cases of MFS, which obviously potentially affects management.

References

C. J. Eberth, “Zur Entwickelung des Epithelioms (Cholesteatoms) der Pia und der Lunge,” Virchows Archiv, vol. 49, no. 1, pp. 51–63, 1869.
View at: Publisher Site | Google Scholar
W. F. Beerman, “The absence of brain tumour symptoms in cases of tumours of the brain,” California State Journal of Medicine, vol. 11, no. 6, pp. 234–235, 1913.
View at: Google Scholar
W. R. Wasserstrom, J. P. Glass, and J. B. Posner, “Diagnosis and treatment of leptomeningeal metastases from solid tumors: experience with 90 patients,” Cancer, vol. 49, no. 4, pp. 759–772, 1982.
View at: Google Scholar
J. G. Kaplan, T. G. DeSouza, A. Farkash et al., “Leptomeningeal metastases: comparison of clinical features and laboratory data of solid tumors, lymphomas and leukemias,” Journal of Neuro-Oncology, vol. 9, no. 3, pp. 225–229, 1990.
View at: Publisher Site | Google Scholar
J. B. Posner, Neurologic Complications of Cancer, F. A. Davis, Philadelphia, Pa, USA, 1995.
S. Kesari and T. T. Batchelor, “Leptomeningeal metastases,” Neurologic Clinics, vol. 21, no. 1, pp. 25–66, 2003.
View at: Publisher Site | Google Scholar
M. C. Chamberlain, “Carcinomatous meningitis,” Archives of Neurology, vol. 54, no. 1, pp. 16–17, 1997.
View at: Google Scholar
J. P. Glass, M. Melamed, N. L. Chernik, and J. B. Posner, “Malignant cells in cerebrospinal fluid (CSF): the meaning of a positive CSF cytology,” Neurology, vol. 29, no. 10, pp. 1369–1375, 1979.
View at: Google Scholar
W. R. Shapiro, J. B. Posner, and Y. Ushio, “Treatment of meningeal neoplasms,” Cancer Treatment Reports, vol. 61, no. 4, pp. 733–743, 1977.
View at: Google Scholar
J. B. Posner and N. L. Chernik, “Intracranial metastases from systemic cancer,” Advances in Neurology, vol. 19, pp. 579–592, 1978.
View at: Google Scholar
J. R. Little, A. J. D. Dale, and H. Okazaki, “Meningeal carcinomatosis: clinical manifestations,” Archives of Neurology, vol. 30, no. 2, pp. 138–143, 1974.
View at: Google Scholar
R. A. Price and W. W. Johnson, “The central nervous system in childhood leukemia. I. The arachnoid,” Cancer, vol. 31, no. 3, pp. 520–533, 1973.
View at: Google Scholar
B. Azzarelli, L. D. Mirkin, and M. Goheen, “The leptomeningeal vein. A site of re-entry of leukemic cells into the systemic circulation,” Cancer, vol. 54, no. 7, pp. 1333–1343, 1984.
View at: Google Scholar
G. O. Grain and J. P. Karr, “Diffuse leptomeningeal carcinomatosis; clinical and pathologic characteristics,” Neurology, vol. 5, no. 10, pp. 706–722, 1955.
View at: Google Scholar
B. G. Redman, E. Tapazoglou, and M. Al-Sarraf, “Meningeal carcinomatosis in head and neck cancer. Report of six cases and review of the literature,” Cancer, vol. 58, no. 12, pp. 2656–2661, 1986.
View at: Google Scholar
J. L. Nugent, P. A. Bunn Jr., and M. J. Matthews, “CNS metastases in small cell bronchogenic carcinoma. Increasing frequency and changing pattern with lengthening survival,” Cancer, vol. 44, no. 5, pp. 1885–1893, 1979.
View at: Google Scholar
R. S. Aroney, D. N. Dalley, and W. K. Chan, “Meningeal carcinomatosis in small cell carcinoma of the lung,” American Journal of Medicine, vol. 71, no. 1, pp. 26–32, 1981.
View at: Google Scholar
R. Boyle, M. Thomas, and J. H. Adams, “Diffuse involvement of the leptomeninges by tumour - a clinical and pathological study of 63 cases,” Postgraduate Medical Journal, vol. 56, no. 653, pp. 149–158, 1980.
View at: Google Scholar
M. Fisher, “An unusual variant of acute idiopathic polyneuritis (syndrome of ophthalmoplegia, ataxia and areflexia),” The New England Journal of Medicine, vol. 255, no. 2, pp. 57–65, 1956.
View at: Google Scholar
B. C. Jacobs, H. P. Endtz, F. G. A. Van der Meche, M. P. Hazenberg, H. A. M. Achtereekte, and P. A. Van Doorn, “Serum anti-GQ(1b) IgG antibodies recognize surface epitopes on Campylobacter jejuni from patients with Miller Fisher syndrome,” Annals of Neurology, vol. 37, no. 2, pp. 260–264, 1995.
View at: Publisher Site | Google Scholar
A. Chiba, S. Kusunoki, T. Shimizu, and I. Kanazawa, “Serum IgG antibody to ganglioside GQ1b is a possible marker of Miller Fisher syndrome,” Annals of Neurology, vol. 31, no. 6, pp. 677–679, 1992.
View at: Publisher Site | Google Scholar
M. Ito, S. Kuwabara, M. Odaka et al., “Bickerstaff's brainstem encephalitis and Fisher syndrome form a continuous spectrum: Clinical analysis of 581 cases,” Journal of Neurology, vol. 255, no. 5, pp. 674–682, 2008.
View at: Publisher Site | Google Scholar
H. J. Willison and J. Veitch, “Immunoglobulin subclass distribution and binding characteristics of anti-GQ1b antibodies in Miller Fisher syndrome,” Journal of Neuroimmunology, vol. 50, no. 2, pp. 159–165, 1994.
View at: Publisher Site | Google Scholar
K. Mizoguchi, A. Hase, T. Obi et al., “Two species of antiganglioside antibodies in a patient with a pharyngeal-cervical-brachial variant of Guillain-Barre syndrome,” Journal of Neurology Neurosurgery and Psychiatry, vol. 57, no. 9, pp. 1121–1123, 1994.
View at: Google Scholar
C. P. O'Leary, J. Veitch, W. F. Durward, A. M. Thomas, J. H. Rees, and H. J. Willison, “Acute oropharyngeal palsy is associated with antibodies to GQ1b and GT1a gangliosides,” Journal of Neurology Neurosurgery and Psychiatry, vol. 61, no. 6, pp. 649–651, 1996.
View at: Google Scholar
K. Kashihara, Y. Shiro, M. Koga, and N. Yuki, “IgG anti-GT1a antibodies which do not cross react with GQ1b ganglioside in a pharyngeal-cervical-brachial variant of Guillain-Barre syndrome,” Journal of Neurology Neurosurgery and Psychiatry, vol. 65, no. 5, p. 799, 1998.
View at: Google Scholar
Y. L. Lo, “Clinical and immunological spectrum of the Miller Fisher syndrome,” Muscle and Nerve, vol. 36, no. 5, pp. 615–627, 2007.
View at: Publisher Site | Google Scholar
M. Mori, T. Takeshima, N. Yuki, and K. Nakashima, “A case of anti-GQ1b-positive atypical Fisher syndrome with internal ophthalmoplegia but without external ophthalmoplegia,” Clinical Neurology, vol. 40, no. 9, pp. 887–890, 2000.
View at: Google Scholar
H. Goldberg-Stern, E. Melamed, and N. Gadoth, “Abnormal evoked potentials in Miller-Fisher syndrome: further evidence of combined peripheral and central demyelination,” Journal of Neurology Neurosurgery and Psychiatry, vol. 57, no. 4, p. 506, 1994.
View at: Google Scholar
V. Wong, “A neurophysiological study in children with Miller Fisher Syndrome and Guillain-Barre syndrome,” Brain and Development, vol. 19, no. 3, pp. 197–204, 1997.
View at: Publisher Site | Google Scholar
N. Yuki, K. Wakabayashi, M. Yamada, and K. Seki, “Overlap of Guillain-Barre syndrome and Bickerstaff's brainstem encephalitis,” Journal of the Neurological Sciences, vol. 145, no. 1, pp. 119–121, 1997.
View at: Publisher Site | Google Scholar
M. Kikuchi, Y. Tagawa, H. Iwamoto, H. Hoshino, and N. Yuki, “Bickerstaff's brainstem encephalitis associated with IgG anti-GQ1b antibody subsequent to Mycoplasma pneumoniae infection: favorable response to immunoadsorption therapy,” Journal of Child Neurology, vol. 12, no. 6, pp. 403–405, 1997.
View at: Google Scholar
J. H. Yeh, W. H. Chen, J. R. Chen, and H. C. Chiu, “Miller fisher syndrome with central involvement: successful treatment with plasmapheresis,” Therapeutic Apheresis, vol. 3, no. 1, pp. 69–71, 1999.
View at: Publisher Site | Google Scholar
A. Chiba, S. Kusunoki, H. Obata, R. Machinami, and I. Kanazawa, “Serum anti-GQ(1b) IgG antibody is associated with ophthalmoplegia in Miller Fisher syndrome and Guillain-Barre syndrome: clinical and immunohistochemical studies,” Neurology, vol. 43, no. 10, pp. 1911–1917, 1993.
View at: Google Scholar
A. Chiba, S. Kusunoki, S. Kuwata, T. Juji, Y. Shibata, and I. Kanazawa, “HLA and anti-GQ1b IgG antibody in Miller Fisher syndrome and Guillain- Barre syndrome,” Journal of Neuroimmunology, vol. 61, no. 1, pp. 85–88, 1995.
View at: Publisher Site | Google Scholar
A. Chiba, S. Kusunoki, H. Obata, R. Machinami, and I. Kanazawa, “Ganglioside composition of the human cranial nerves, with special reference to pathophysiology of Miller Fisher syndrome,” Brain Research, vol. 745, no. 1-2, pp. 32–36, 1997.
View at: Publisher Site | Google Scholar
K. Paparounas, G. M. O'Hanlon, C. P. O'Leary, E. G. Rowan, and H. J. Willison, “Anti-ganglioside antibodies can bind peripheral nerve nodes of Ranvier and activate the complement cascade without inducing acute conduction block in vitro,” Brain, vol. 122, no. 5, pp. 807–816, 1999.
View at: Publisher Site | Google Scholar
M. Roberts, H. Willison, A. Vincent, and J. Newsom-Davis, “Serum factor in Miller-Fisher variant of Guillain-Barre syndrome and neurotransmitter release,” Lancet, vol. 343, no. 8895, pp. 454–455, 1994.
View at: Publisher Site | Google Scholar
H. J. Willison and J. J. Plomp, “Anti-ganglioside antibodies and the presynaptic motor nerve terminal,” Annals of the New York Academy of Sciences, vol. 1132, pp. 114–123, 2008.
View at: Publisher Site | Google Scholar
D. J. Lange, T. DeAngelis, and M. A. Sivak, “Single-fiber electromyography shows terminal axon dysfunction in Miller Fisher syndrome: a case report,” Muscle and Nerve, vol. 34, no. 2, pp. 232–234, 2006.
View at: Publisher Site | Google Scholar
S. Kuwabara, M. Asahina, M. Nakajima et al., “Special sensory ataxia in Miller Fisher syndrome detected by postural body sway analysis,” Annals of Neurology, vol. 45, no. 4, pp. 533–536, 1999.
View at: Google Scholar
H. J. Willison, G. M. O'Hanlon, G. Paterson et al., “A somatically mutated human antiganglioside IgM antibody that induces experimental neuropathy in mice is encoded by the variable region heavy chain gene, V1-18,” Journal of Clinical Investigation, vol. 97, no. 5, pp. 1155–1164, 1996.
View at: Google Scholar
S. Kusunoki, A. Chiba, and I. Kanazawa, “Anti-GQ1b IgG antibody is associated with ataxia as well as ophthalmoplegia,” Muscle & Nerve, vol. 22, no. 8, pp. 1071–1074, 1999.
View at: Google Scholar
A. J. Kornberg, A. Pestronk, G. M. Blume, G. Lopate, J. Yue, and A. Hahn, “Selective staining of the cerebellar molecular layer by serum IgG in Miller-Fisher and related syndromes,” Neurology, vol. 47, no. 5, pp. 1317–1320, 1996.
View at: Google Scholar
A. Inoue, C. S. Koh, and T. Iwahashi, “Detection of serum anticerebellar antibodies in patients with Miller Fisher syndrome,” European Neurology, vol. 42, no. 4, pp. 230–234, 1999.
View at: Google Scholar
R. Bingisser, R. Speich, A. Fontana, J. Gmur, B. Vogel, and T. Landis, “Lupus erythematosus and Miller-Fisher syndrome,” Archives of Neurology, vol. 51, no. 8, pp. 828–830, 1994.
View at: Google Scholar
D. C. Hess, E. Awad, H. Posas, K. D. Sethi, and R. J. Adams, “Miller Fisher syndrome in systemic lupus erythematosus,” Journal of Rheumatology, vol. 17, no. 11, pp. 1520–1522, 1990.
View at: Google Scholar
A. Polizzi, M. Ruggieri, I. Vecchio, S. Genovese, L. Rampello, and R. Raffaele, “Autoimmune thyroiditis and acquired demyelinating polyradiculoneuropathy,” Clinical Neurology and Neurosurgery, vol. 103, no. 3, pp. 151–154, 2001.
View at: Publisher Site | Google Scholar
S. S. Desai, E. Allen, and A. Deodhar, “Miller Fisher syndrome in adult onset Still's disease: case report and review of the literature of other neurological manifestations,” Rheumatology, vol. 41, no. 2, pp. 216–222, 2002.
View at: Google Scholar
M. Guarino, A. Stracciari, F. Cirignotta, R. D'Alessandro, and P. Pazzaglia, “Neoplastic meningitis presenting with ophthalmoplegia, ataxia, and areflexia (Miller-Fisher syndrome),” Archives of Neurology, vol. 52, no. 5, pp. 443–444, 1995.
View at: Google Scholar
Y. Nakatsuji, S. Sadahiro, S. Watanabe et al., “Leptomeningeal signet-ring cell carcinomatosis presenting with ophthalmoplegia, areflexia and ataxia,” Clinical Neuropathology, vol. 20, no. 6, pp. 272–275, 2001.
View at: Google Scholar
T. Csépány, J. Boczán, M. T. Magyar et al., “Miller Fisher syndrome: a presenting clinical manifestation of lung cancer in a previously apparently healthy individual,” Journal of Neurology, vol. 251, no. 7, pp. 898–900, 2004.
View at: Google Scholar
E. Rubio-Nazabal, J. Marey-Lopez, J. P. Torres-Carrete, P. Alvarez-Perez, and P. R. Del Corral, “Miller-Fisher syndrome and Hodgkin's disease,” Journal of Neurology Neurosurgery and Psychiatry, vol. 73, no. 3, p. 344, 2002.
View at: Publisher Site | Google Scholar
L. De Toni, S. Marconi, E. Nardelli et al., “Gangliosides act as onconeural antigens in paraneoplastic neuropathies,” Journal of Neuroimmunology, vol. 156, no. 1-2, pp. 178–187, 2004.
View at: Publisher Site | Google Scholar
S. Gentile, M. Messina, I. Rainero, R. Lo Giudice, P. De Martino, and L. Pinessi, “Miller Fisher syndrome associated with Burkitt's lymphoma,” European Journal of Neurology, vol. 13, no. 4, p. 430, 2006.
View at: Publisher Site | Google Scholar
Z. Aki, O. Aksoy, G. Sucak, R. Kuruoğlu, and M. Yağci, “Miller-Fisher syndrome associated with chronic lymphocytic leukemia,” Neurology India, vol. 56, no. 2, pp. 198–200, 2008.
View at: Publisher Site | Google Scholar
A. A. Tahrani, S. Sharma, S. Rangan, and A. F. Macleod, “A patient with worsening mobility: a diagnostic challenge,” European Journal of Internal Medicine, vol. 19, no. 4, pp. 292–294, 2008.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2012 N. Karsan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

5194

Downloads

1481

Citations