Brain, Vol. 123, No. 1, 116-124,
January 2000
© 2000 Oxford University Press
Guillain–Barré syndrome with antibody to a ganglioside, N-acetylgalactosaminyl GD1a
1 Third Department of Internal Medicine, National Defense Medical College, Saitama-ken and 2 Department of Neurology, School of Medicine, University of Tokyo,Tokyo, Japan
Correspondence to:
Susumu Kusunoki, MD, Department of Neurology, School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan E-mail: kusunoki-tky {at} umin.ac.jp
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Abstract |
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A retrospective case study of 33 Guillain–Barré syndrome (GBS) patients with the antibody to the ganglioside N-acetylgalactosaminyl GD1a (GalNAc-GD1a) was made to investigate the clinical features of GBS with this antibody. Patients were classified into three groups: (i) 25 with IgG antibody (group G, titre
1 : 40); (ii) 16 with high-titre IgG antibody (group G-high, titre 1:320; selected from group G patients), and (iii) eight with IgM antibody but without elevation of IgG (group M, normal range <1:40 for both IgM and IgG). The control group consisted of 72 GBS patients without anti-GalNAc-GD1a antibody. Compared with the control group, the G-high and G group patients were characterized as having had antecedent gastrointestinal infection (87% and 72% versus 31%, both P < 0.001), uncommon cranial nerve involvement (19% and 36% versus 54%, P = 0.02 and 0.2, respectively), distal-dominant weakness (94% and 68% versus 36%, P < 0.001 and P = 0.01, respectively) and no sensory signs (81% and 60% versus 25%, P < 0.001 and P = 0.003, respectively). Electrophysiological findings indicative of axonal dysfunction were significantly more common in the G-high and G group patients (63% and 52% versus 14%, both P < 0.001). The pure motor variant that showed neither sensory signs nor abnormalities in sensory conduction studies was also more frequent in these groups (44% and 32% versus 9%, both P < 0.001). IgG anti-GalNAc-GD1a antibody may be a marker of the pure motor and the axonal variants of GBS, and therefore it, as well as anti-GM1 antibody, must be investigated in these forms in order to diagnose and understand the variants. By contrast, mild weakness, frequent facial palsy (75%) and a high incidence of IgM anti-GM2 antibody reactivity (88%) were characteristic of group M, indicating that the GBS in that group resulted from a different immune mechanism from that in the G group. Guillain–Barré syndrome; GalNAc-GD1a; pure motor variant; motor axonal variant; anti-ganglioside antibody
CMAP = compound muscle action potentials; CMV = cytomegalovirus; ELISA = enzyme-linked immunosorbent assay; GalNAc-GD1a = ganglioside N-acetylgalactosaminyl GD1a; GBS = Guillain–Barré syndrome
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Introduction |
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Frequent elevation of anti-ganglioside antibodies in acute phase sera from patients with Guillain–Barré syndrome (GBS) has been reported (Hartung et al., 1995
), and the clinical spectrum of GBS is suggested to be associated with the reactivity of anti-ganglioside antibodies (Yuki et al., 1990; Chiba et al., 1993; Kornberg et al., 1994; Kusunoki et al., 1994). GBS, which shows no sensory signs and symptoms and gives normal conduction results in sensory nerve conduction studies, is rare, having been reported as a pure motor variant (Ropper et al., 1991; Visser et al., 1995). Visser and colleagues pointed out that motor GBS without sensory loss is characterized by the rapid onset of weakness, early nadir, distal-dominant weakness, sparing of the cranial nerves and a preceding gastrointestinal infection, often subsequent to Campylobacter jejuni infection (Visser et al., 1995). Patients with motor GBS frequently show little evidence of demyelination in nerve conduction studies and have high anti-GM1 antibody titres (Visser et al., 1995).
N-Acetylgalactosaminyl GD1a (GalNAc-GD1a) is a target antigen for serum antibodies in GBS. Patients with IgG anti-GalNAc-GD1a antibody have often had an antecedent gastrointestinal infection and have electrophysiological findings indicative of conduction abnormalities in the most distal portion of the peripheral nerves, or of axonal damage (Kusunoki et al., 1994). Some case reports also suggest that IgG anti-GalNAc-GD1a antibody is a predictor of the motor form of GBS which has few sensory signs, no cranial nerve deficits, distal-dominant weakness or electrophysiological findings indicative of axonal dysfunction (Ihara et al., 1995; Tsuda et al., 1995; Ono et al., 1997). No clinical investigation, however, has been made of a population of patients with anti-GalNAc-GD1a antibody. We here report a retrospective case-control study of GBS patients with and without the antibody that was carried out in order to evaluate the clinical features of GBS with anti-GalNAc-GD1a antibody.
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Material and methods |
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Patients' sera and the enzyme-linked immunosorbent assay
Acute phase sera were collected from patients with clinically defined GBS between January 1992 and January 1998 at various general and teaching hospitals throughout Japan. The patients' clinical data were also sent to us at that time. All the patients met the diagnostic criteria of Asbury and Cornblath (Asbury and Cornblath, 1990
). Serum antibodies against 10 ganglioside antigens (GalNAc-GD1a, GM1, GM2, GM3, GD1a, GD1b, GD3, GT1b, GQ1b and GM1b) were investigated using the enzyme-linked immunosorbent assay (ELISA), as described elsewhere (Kusunoki et al., 1994). GalNAc-GD1a was prepared in our laboratory from bovine brain (Kusunoki et al., 1994) and GM1b from rat ascites hepatoma AH-66 (Iwamori et al., 1986). The other gangliosides were purchased from Sigma (St Louis, Mo., USA). Serum diluted 1:40 with 1% bovine serum albumin in phosphate-buffered saline was added to wells coated with 0.2 µg of antigen. Uncoated wells served as the control. As the secondary antibody, peroxidase-conjugated anti-human IgM (Cappel, West Chester, Pa., USA) (diluted 1:200) or anti-human IgG (Cappel) (1:500) was added to each well. Sera with anti-GalNAc-GD1a antibody were diluted serially from 1:40 to 1:81 920, after which the ELISA was performed. Optical density values were corrected by subtracting the optical density of a control well that had been similarly processed. Antibody titre was expressed as the maximal dilution factor that gave a corrected optical density of more than 0.1. Because the normal range for anti-GalNAc-GD1a antibodies in the normal population is less than 1:40 (Kusunoki et al., 1994), sera with a titre of 1:40 or more were considered positive. Sera giving positive results in the ELISA were overlaid for thin-layer chromatogram immunostaining, as described elsewhere (Kusunoki et al., 1994).
Study population
Patients with IgG or IgM antibodies against GalNAc-GD1a were grouped as follows: (i) IgG anti-GalNAc-GD1a antibody (group G, titre 1:40); (ii) high-titre IgG antibody (group G-high, titre 1:320), i.e. the patients in group G-high were selected from the patients in group G; and (iii) IgM antibody without elevation of IgG (group M, normal range <1:40 for both IgM and IgG). We asked the attending physicians to send us detailed clinical data on each patient with anti-GalNAc-GD1a antibody. Of the GBS patients without anti-GalNAc-GD1a antibody, those for whom clinical and electrophysiological data were available when the serum samples were received formed the control group. Anti-GalNAc-GD1a antibody-positive patients without data on neurological signs and symptoms were excluded. Patients with no information on electrophysiological results or neurological signs and symptoms were excluded from the control group. Patients were recruited to the control group solely on the availability of those data, without bias. Patients' deficits were assessed with functional scores (F-score) as described by van der Meché and colleagues: 0 = healthy; 1 = having minor symptoms and signs but fully capable of manual work; 2 = able to walk 10 m or more without assistance; 3 = able to walk 10 m or more with a walker or support; 4 = bedridden or chairbound; 5 = requiring assisted ventilation for at least part of the day; 6 = dead (van der Meché et al., 1992). Patients were categorized as having motor GBS when there were neither paraesthesias nor sensory deficits at the onset of the illness or during the follow-up. Motor GBS patients whose available electrodiagnostic data indicated normal sensory conduction velocities and sensory nerve action potentials were classified as having pure motor GBS. Clinical features and laboratory data of the G, G-high or M groups and the control group were compared.
Electrophysiological data and classification
The nerve conduction studies were done at various hospitals using conventional recording techniques and standard methods (Kimura, 1989). When the attendant or assessing physicians evaluated the electrophysiological results using the value of the upper and lower limit of normal in use at their laboratories, we used their evaluations. For data not evaluated as above, to ensure impartial evaluation of the results, the upper and lower limits of normal reported by Alam and colleagues were used (Alam et al., 1998). The diagnostic criteria for demyelinating polyneuropathy and axonal motor polyneuropathy were based on motor nerve conduction findings for two or more nerves during the first 4 weeks of illness, as reported by Ho and colleagues (Ho et al., 1997). Using these criteria as modified by Hadden and colleagues (Hadden et al., 1998), a demyelinating feature was disregarded in one nerve if the distal compound muscle action potential (CMAP) amplitudes were <10% of the lower limit of normal. Conduction block or temporal dispersion were considered to exist when the drop in the peak-to-peak amplitude between the proximal and distal sites was >20%, as reported by Cornblath (Cornblath, 1990). Patients whose electrophysiological results showed the absence of motor evoked responses in two or more nerves were classified as inexcitable. Those who were not investigated electrophysiologically, or for whom there was insufficient evidence of demyelination or axonal degeneration, were labelled unclassifiable.
Statistical analysis
Differences in proportions were tested by the 
2 test for independence or by Fisher's exact test. The Bartlett test was used to assess whether the distribution of data variables was equal among the groups. The Kormogorov–Smirnov test was used to verify the normal distribution of data variables in each group. The Kruskal–Wallis and 2 tests for independence were used to compare the different groups (G, G-high, M and control). Scheffe's test was used for post hoc analysis, except for the comparison of the F-score at nadir. The Kruskal–Wallis test was used and the Dunnett test for post hoc analysis when the F-score at nadir was compared among the groups. Two-tailed P-values <0.05 were considered significant throughout. The above analyses were performed with Stat View software.
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Results |
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Study population
We collected sera from 394 GBS patients. Thirty-six sera were identified by the ELISA as having IgG or IgM anti-GalNAc-GD1a antibody. In all positive patients, IgG or IgM antibody reactivity with GalNAc-GD1a was confirmed by overlay thin-layer chromatogram immunostaining. Three of the 36 patients (8%) with these antibodies were excluded because of incomplete clinical data, the data on the remaining 33 patients were used for the clinical analysis. The number of patients in each group and each patient's IgG or IgM class anti-GalNAc-GD1a antibody titre are shown in Fig. 1
. The control group consisted of 72 of 358 patients without anti-GalNAc-GD1a antibody. The remaining 286 patients (80% of the anti-GalNAc-GD1a antibody-negative patients) were excluded because of incomplete clinical or electrophysiological data. Because we asked the attendant physicians for further clinical information only on patients with anti-GalNAc-GD1a antibody, there was a marked difference in the exclusion rates for the groups with and without the antibody.
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Frequencies of anti-ganglioside antibodies
The frequencies and specificities of the other anti-ganglioside antibodies are shown in Fig. 2
. Twenty-four of the 72 patients (33%) in the control group had negative ELISA results. Comparisons among the groups of the frequencies of antibodies to the other gangliosides showed a significantly high frequency only for IgM class antibodies to GM2 (88%) in group M (P < 0.0001, 2 test) (Fig. 2). IgG or IgM class anti-GM1 antibodies were present as follows: group G, IgG 40%, IgM 24%; group G-high, IgG 31%, IgM 25%; group M, IgM 38%; and control group, IgG 26%, IgM 25%; no significant differences in frequency were found among the groups. Seven of 25 patients in group G, four in group G-high and one in group M had only the anti-GalNAc-GD1a antibody. Only one patient in group M had an IgG anti-ganglioside antibody (anti-GQ1b antibody).
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Antecedent infection
The G and G-high group patients had more frequently suffered antecedent gastrointestinal infection than patients in the other groups (Table 1
). Campylobacter jejuni isolated from two patients in group G had the serotypes Penner 8, Lior 2 and Penner 37, Lior 2. In group M, antecedent cytomegalovirus (CMV) infection was proved serologically in two patients, and C. jejuni infection by stool culture in two patients, but the C. jejuni serotypes were not investigated.
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Clinical features
The features of the patients in each group are given in Table 1
. The Kormogorov–Smirnov test showed normal distributions of data variables for the parameters age and CSF protein in each group. Because the Bartlett test used to test the parameters did not show equal distributions of the data variables among the groups, the Kruskal–Wallis test was used. Comparisons of each factor among the groups (G-high, M and control, or G, M and control) showed significant differences, except for sex, onset to nadir (in days) and CSF protein (max.) (the maximum results for CSF protein in the course of GBS). Patients in group G were characterized as having infrequent cranial nerve deficits, predominance of distal weakness and uncommon sensory symptoms and signs, all of which were more remarkable in the G-high group patients. Thirteen patients (81%) in the G-high and 15 (60%) in the G group had motor GBS. Because five of the 13 G-high group patients with motor GBS had not undergone sensory conduction studies and one with a long history of diabetes mellitus had abnormal results in the sensory conduction studies, only seven patients (44%) were classified as having the pure motor variant.
Group M patients were characterized as having younger onset, mild weakness at the peak, more frequent cranial nerve deficits, especially facial palsy, and better recoveries, compared with the control patients. Also, they frequently had sensory deficits. No one in this group exceeded an F-score of 4 at the peak. Half of the patients had only areflexia and cranial nerve deficits without limb weakness. Two patients who had suffered preceding CMV infection had IgM anti-GM2 in addition to the anti-GalNAc-GD1a antibody and presented facial diplegia. Two patients who had suffered antecedent C. jejuni infection had IgM anti-GM2 and anti-GalNAc-GD1a antibodies as well as facial palsy.
Some of the G and the G-high group patients also had IgM anti-GalNAc-GD1a antibodies. Of the six G and five G-high group patients with IgM anti-GalNAc-GD1a antibody, two (33%) and one (20%), respectively, had cranial nerve deficits. Of the six G group patients with IgM anti-GalNAc-GD1a antibody, two patients had IgM anti-GM2 antibodies but no cranial nerve deficits. On the other hand, of the nine G and three G-high group patients with cranial nerve involvement, two (22%) and one (33%), respectively, had IgM anti-GalNAc-GD1a antibody.
The F-score at nadir for all the subjects ranged from 1 to 5, the distributions differing significantly in the comparisons of the G, M and control groups and of the G-high, M and control groups (both P = 0.0002, Kruskal–Wallis test). In each two-group comparison, the G and M group patients had significantly lower F-scores at nadir than the control group patients (Fig. 3). There were no significant differences among the groups as to the incidence of the use of artificial respiration [group G (G-high), 12% (6.3%); group M, 0%; control group, 15%].
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Electrophysiological study
There were significant differences in the proportions of subtypes, axonal or demyelinating polyneuropathy, among each group (P < 0.001,
2 test). The axonal type pattern was significantly more frequent in groups G and G-high than in the control group (Table 1). Two G-high group patients were classified as having demyelination type GBS on the basis of prolonged distal latency in one patient, and prolonged distal latency and conduction block in the other. All four of the G-high group patients, who had only IgG anti-GalNAc-GD1a antibody without the IgM class antibody and no other anti-ganglioside antibodies, were classified as having axonal type GBS. Of the 13 motor GBS patients in the G-high group, eight were classified as having the axonal type, one the demyelination type, two the inexcitable type and two were unclassifiable. Sensory conduction findings were abnormal in three (12%) of the G group, three (19%) of the G-high group, three (38%) of the M group and 33 (46%) of the control group patients. Needle electromyography performed on five of the G-high group patients showed denervation potentials.
Treatment and prognosis
Plasmapheresis was carried out on 18 (72%) of the G group, 11 (69%) of the G-high group, four (50%) of the M group and 57 (79%) of the control group patients. One of the G-high group, two of the G group, three of the M group and two of the control group patients were treated solely with corticosteroids. Four of the G-high group, five of the G group, one of the M group and 10 of the control group patients were given no specific treatment because of their low F-scores and good recovery.
Because the long-term follow-up data were often incomplete, the short-term prognoses 1 month after onset were compared for each group. Fifty-seven patients in the control group had available data on short-term prognoses, which were used for the comparison. M group patients showed significantly better recoveries than control group patients (P = 0.0004, Fisher's exact test). There was no difference in recovery between the G-high or G and control groups.
Subtypes of GBS and anti-ganglioside antibody
The association between such GBS subtypes as the motor axonal or the pure motor variants and the antibodies to nine other gangliosides, excluding GalNAc-GD1a, was analysed in the G, G-high and control groups (Table 2). In the G and G-high groups, there was no significant correlation between the subtypes and these other anti-ganglioside antibodies. In the control group, IgG anti-GM1 antibody was significantly more frequent in patients with motor GBS (P = 0.002, 2 test), but not in those with the motor axonal variant.
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Discussion |
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Our study shows that IgG antibody to GalNAc-GD1a is strongly associated with the pure motor and the axonal variants of GBS. Such clinical features in patients with the IgG antibody as antecedent enteric episodes, infrequent cranial nerve deficits, distal-dominant weakness, few sensory signs and electrophysiological characteristics (axonal type) were more salient when a high cut-off value was used.
The above characteristics of GBS patients with IgG anti-GalNAc-GD1a antibody are identical to those for motor GBS, i.e. GBS without sensory loss, as described by Visser and colleagues, who stated that IgG anti-GM1 antibody is associated with motor GBS (Visser et al., 1995). In our study, IgG anti-GalNAc-GD1a antibody was strongly associated with the motor and axonal variants of GBS. IgG anti-GM1 antibody was not common in the G-high and G group patients with the pure motor or the axonal variants of GBS. The clinical features in the G-high and G groups, therefore, are not due to the existence of IgG anti-GM1 antibody. By contrast, IgG anti-GM1 antibody was significantly associated with motor GBS in the control group patients. We would emphasize that anti-GalNAc-GD1a antibody must also be investigated as an antibody associated with the pure motor or axonal variants of GBS in order to diagnose and understand the variants.
GalNAc-GD1a is present in the human peripheral nervous system (Ilyas et al., 1988), but its localization has yet to be determined. As in a previous study (Kusunoki et al., 1994), our findings suggest that IgG anti-GalNAc-GD1a antibody selectively attacks motor nerves and causes axonal dysfunction or conduction block in the most distal portion of those nerves. It is uncertain whether electrophysiological changes are related to axonal or demyelinating pathology. In motor axonal variants of GBS, motor nerves with very low CMAPs due to axonopathy may have prolonged distal and F-wave latencies or reduced conduction velocity (Brown et al., 1993). In the early phase of GBS, however, pure conduction block in the most distal region of the motor axon may produce only a decrease in the amplitude of the distal CMAP with little increase in distal latency (Parry, 1993). In our series, conduction failure in the motor nerve terminals may have occurred in patients with IgG anti-GalNAc-GD1a antibody whose electrophysiological findings were classified as the axonal type. Detailed serial electrophysiological studies and the follow-up of disabilities should help to clarify the pathogenic role of IgG anti-GalNAc-GD1a antibody in GBS.
The variation in anti-ganglioside antibodies may be due to the difference in the pathogen causing the preceding infection. Specific serotypes of C. jejuni, Penner 19 and Penner 4, have a pathogenic role in the generation of anti-GM1 antibody in GBS (Kuroki et al., 1993; Yuki et al., 1993, 1994). These isolates of Campylobacter have the Gal (ß1–3) GalNAc epitope within their lipopolysaccharides, which may cause an immune response to the Gal (ß1–3) GalNAc residue of GM1 (Yuki et al., 1993). It is also possible that Campylobacter isolates from patients with IgG anti-GalNAc-GD1a antibodies, Penner 8 and Penner 37, have GalNAc-GD1a-like lipopolysaccharides that can trigger immune responses to GalNAc-GD1a or GalNAc-GD1a-like structures on the peripheral nerves.
IgG class anti-ganglioside antibodies, mainly those of the IgG1 and IgG3 subclasses, are more common than IgM class antibodies in GBS and are considered to be more pathogenic (Willison and Veitch, 1994; Ogino et al., 1995). Little, however, is known about the pathogenic role of IgM antibody in GBS. The M group patients had no IgG antibodies to gangliosides, except for GQ1b in one patient, and had the following characteristics that differed completely from those of the G group patients: mild weakness, frequent cranial nerve deficits, good recovery and high frequency of IgM anti-GM2 antibody. In contrast, there was no significant correlation in the G group patients between IgM anti- GalNAc-GD1a antibody and cranial nerve deficits, the reason for which is not clear. There may be differences between the target antigens recognized by the antibodies in the G and M group patients, because the M group patients frequently had IgM anti-GM2 antibody. Considering these findings, in the M group patients IgM antibodies might be involved in the pathogenesis. A pathomechanism distinct from that in the G group patients might function in those patients. T-cell-independent antigens induce only low-affinity, predominantly IgM antibody responses, whereas T-cell-dependent antigens produce high-affinity, predominantly IgG antibody responses with isotype switching to IgG1 or IgG3 (Papadea and Check, 1989; Mond et al., 1995). The T-cell-independent response may be the major pathophysiological mechanism in patients with predominantly IgM anti-ganglioside antibodies. The shorter half-life of the IgM antibody may also be related to the mild weakness and prompt recovery of the M group patients. Why the IgM antibody present in the M group patients often recognized both GalNAc-GD1a and GM2, whereas the IgG antibody was relatively specific to GalNAc-GD1a, is not clear.
In GBS after CMV infection, IgM anti-GM2 antibodies are often elevated (Irie et al., 1996; Jacobs et al., 1997; Khalili-Shirazi et al., 1999) and facial diplegia is common (Visser et al., 1996). Our findings show that C. jejuni infection also produces a combined rise in IgM anti-GM2 antibodies and facial palsy, but whether this combination is meaningful has yet to be confirmed. Irie and colleagues showed that the anti-GM2 antibodies in patients with GBS after acute CMV infection recognize the GalNAc-Gal-Glc residue of glycoconjugates (Irie et al., 1996), whereas Jacobs and colleagues reported that sera of patients with IgM anti-GM2 antibodies recognize GalNAc-Gal-Glc or [GalNAcß1–4(NeuAc
2–3)Gal] residues (Jacobs et al., 1997). The IgM antibodies binding to both GM2 and GalNAc-GD1a in our series should recognize the terminal moiety, [GalNAcß1–4(NeuAc2–3)Gal] common to those gangliosides (Fig. 4), and this moiety may be a target antigen for IgM antibodies on the facial nerves of the M group patients with facial palsy. Interestingly, Cavanna and colleagues recently showed that four GBS patients with IgM anti-GM2 antibodies had IgM anti-GalNAc-GD1a antibodies and sensory impairment, and that three of the four had facial weakness (Cavanna et al., 1999). Their findings are consistent with ours for the M group patients, except that their four patients had moderate to severe disabilities. The reason for this discrepancy in disability between the findings of Cavanna and colleagues and our findings is not clear.
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Acknowledgments |
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We thank Drs Kimiyoshi Arimura (Kagoshima University Hospital), Kohei Oota (Tokyo Women's Medical College Hospital), Muneshige Hida (National Miyagi Hospital), Sayoko Matsuno (Tsukuba University Hospital), Kazuhiro Nishimoto (Kinki University Hospital), Nobumichi Ichikawa (Sendai Red-Cross Hospital), Katsuhisa Ogata (Tokyo University Hospital), Yuko Hayashi and Imaharu Nakano (Jichi Medical School), Hiroko Yamamoto (Fujita Health University Hospital) and Norikazu Miyamoto (National Defense Medical College Hospital) for providing the clinical information on the patients. We also thank Dr Masaki Takahashi (Tokyo Metropolitan Research Laboratory of Public Health) for performing the Penner serotyping of our isolates, Dr Iwamori for providing the GM1b ganglioside antigen and Dr Hiroshi Ashida (Division of Biomedical Information Sciences, National Defense Medical College Research Institute) for useful advice on the statistical analyses. This study was supported, in part, by a Research Grant for Neuroimmunological Diseases from the Ministry of Health and Welfare, Japan and by a Grant-in-Aid for Scientific Research (10670576) from the Ministry of Education, Science, Culture and Sports of Japan.
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Received June 3, 1999. Accepted July 26, 1999.
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