Journal of the Neurological Sciences 364 (2016) 59–64

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Journal of the Neurological Sciences

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Recurrent Guillain–Barré syndrome, Miller Fisher syndrome and

Bickerstaff brainstem encephalitis
Junko Ishii a,⁎, Nobuhiro Yuki b, Michi Kawamoto a, Hajime Yoshimura a, Susumu Kusunoki c, Nobuo Kohara a
a
Department of Neurology, Kobe City Medical Center General Hospital, Japan
b
Brain and Mind Centre, University of Sydney, Australia
c
Department of Neurology, Kinki University School of Medicine, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Objective: Guillain–Barré syndrome (GBS), Miller Fisher syndrome (MFS), and Bickerstaff brainstem encephalitis
Received 27 December 2015 (BBE) are usually monophasic, but some patients experience recurrences after long asymptomatic intervals. We
Received in revised form 29 February 2016 aimed to investigate clinical features of recurrent GBS, MFS, and BBE at a single hospital.
Accepted 2 March 2016 Methods: Records from 97 consecutive patients with GBS, MFS or BBE who were admitted to a tertiary hospital
Available online 3 March 2016
between 2001 and 2013 were reviewed. Clinical and laboratory features of patients with recurrent GBS, MFS,
or BBE were investigated.
Keywords:
Guillain-Barré syndrome
Results: Patients included 55 (32 males) with GBS, 34 (22 males) with MFS, and 8 (6 males) with BBE. Recurrent
Miller Fisher syndrome cases occurred in 2 (4%) of the 55 patients with GBS, 4 (12%) of the 34 patients with MFS, and 2 (25%) of the 8
Bickerstaff brainstem encephalitis patients with BBE. Patients with recurrent MFS had a tendency to be younger at the first episode than patients
Recurrence with non-recurrent MFS (median, 22 versus 37 years old). Symptoms and signs were less severe during relapses
than during the initial episode in recurrent patients.
Conclusions: Recurrences occurred more frequently in patients with MFS or BBE compared with those with GBS.
Patients with recurrent MFS might be younger than those with non-recurrent MFS.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction
Guillain–Barré syndrome (GBS) is characterized by acute onset of
limb weakness [1]. Miller Fisher syndrome (MFS), a variant of GBS, is
characterized by acute ophthalmoplegia and ataxia. Bickerstaff
brainstem encephalitis (BBE), a CNS subtype of MFS, is characterized
by ophthalmoplegia, ataxia, and impaired consciousness. Overlapping
cases of GBS with MFS or BBE and shared laboratory findings support
the notion that GBS is a continuous spectrum of disorders encompassing
MFS and BBE [2,3].
The annual incidence rate of GBS is between 0.75 and 2 per 100,000
[4]. The rates of MFS and BBE are unclear. The incidence of MFS has only
been reported as the percent of all GBS cases [5–13]. While GBS is usu-
ally monophasic, recurrences have been reported in 4%–7% of patients
[14]. On rare occasions, MFS and BBE may also recur. Several cases of re-
current MFS and BBE have been reported [15–22], but the frequency of
recurrent cases in MFS and BBE is not known. Therefore, the aims of this
Abbreviations: GBS, Guillain–Barré syndrome; MFS, Miller Fisher syndrome; BBE,
Bickerstaff brainstem encephalitis.
⁎ Corresponding author at: Department of Neurology, Kobe City Medical Center General
Hospital, 2-1-1, Minatojimaminamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan.
E-mail addresses: ishii-j@kcho.jp (J. Ishii), gbs.yuki.cidp@gmail.com (N. Yuki),
kawamoto@kcho.jp (M. Kawamoto), hajime-y@kcho.jp (H. Yoshimura),
kusunoki-tky@umin.ac.jp (S. Kusunoki), kohara-kcgh@umin.ac.jp (N. Kohara).
study were to examine the percentage all GBS spectrum disorders at a
single hospital that include MFS or BBE, and to analyze the frequency
of recurrent cases of GBS, MFS, and BBE. We also tried to clarify the clin-
ical and laboratory features of recurrences.
2. Methods
2.1. Patients
We retrospectively analyzed 97 consecutive inpatients with GBS
spectrum disorders at the Department of Neurology, Kobe City Medical
Center General Hospital from January 2001 to March 2013 based on
predetermined criteria [1]. Briefly, GBS was diagnosed in patients with
acute bilateral flaccid limb weakness without other etiology. MFS was
diagnosed in patients with ophthalmoplegia and ataxia. Patients with
MFS and limb weakness were included in this group. Among them, pa-
tients with MFS and definite limb weakness (MMT ≤ 3) in at least one
limb were defined as MFS-GBS, a subtype of MFS. BBE was defined as
MFS with hypersomnolence. Patients with BBE and limb weakness
were also included in this group. Among them, patients with BBE and
definite limb weakness (MMT ≤ 3) in at least one limb were defined
as BBE-GBS, a subtype of BBE. We classified all the GBS spectrum disor-
ders into GBS, MFS, or BBE. A recurrent patient was defined as one hav-
ing two or more episodes that fulfilled the above definition with more

http://dx.doi.org/10.1016/j.jns.2016.03.008
0022-510X/© 2016 Elsevier B.V. All rights reserved.
60 J. Ishii et al. / Journal of the Neurological Sciences 364 (2016) 59–64
than 4-month free intervals [23]. We examined the frequency of recur-
rence of GBS, MFS, and BBE and analyzed the median age at the onset of
symptoms, sex, preceding infection, days to the peak of symptoms, du-
ration of hospital stay, and anti-GQ1b IgG antibody status of patients
with recurrent and non-recurrent MFS. Symptoms of the first episode
were compared with those of the recurrence for patients with recurrent
GBS, MFS, or BBE. The severity of each episode was graded according to
the GBS disability scale [24].
2.2. Literature review
Focusing on the clinical course of recurrent MFS, we performed an
extensive literature search of PubMed with the terms ‘MFS’, ‘Fisher syn-
drome’ and ‘recurrent’, ‘relapsing’. The identified articles in English
were reviewed for patients with recurrent MFS. All identified patients
with documented relapse of MFS were analyzed. Clinical courses at
the first episode and at the recurrence of MFS were compared.
2.3. Anti-ganglioside antibodies
Serum IgG and IgM antibodies to gangliosides were measured by an
enzyme-linked immunosorbent assay at the Department of Neurology,
Dokkyo Medical University, Tochigi, Japan from 2001 to 2006 and at
the Department of Neurology, Kinki University, Osaka, Japan from
2006 to 2013 [25,26].
2.4. Statistical analysis
Wilcoxon rank sum test and Fisher's exact test were performed to
compare characteristics of patients with recurrent and non-recurrent
MFS. JMP® 10 for Windows (SAS Institute Inc., Cary, NC, USA) was
used for all statistical analyses, and p values b0.05 were regarded as
significant.
3. Results
A total of 97 patients were included in this study, composed of 55 pa-
tients (32 males) with GBS, 34 (22 males) with MFS, and 8 (6 males)
with BBE. The frequency of GBS, MFS and BBE in our hospital was 57%,
35% and 8% of all GBS spectrum disorders, respectively (Fig 1A). There
were more men than women in all groups. Among MFS patients, 5
cases (5%) of all GBS spectrum disorders had definite limb weakness
(MMT ≤ 3) and were classified as MFS-GBS. Among BBE patients, 2
Fig. 1. Guillain–Barré syndrome spectrum disorders and the frequency of recurrence. A) Ninety-seven patients were classified as having Guillain–Barré syndrome (GBS, n = 55), Miller
Fisher syndrome (MFS, n = 34), or Bickerstaff brainstem encephalitis (BBE, n = 8). Among MFS, 5 cases had definite limb weakness (MMT ≤ 3) in at least one limb, defined as MFS-
GBS. Among BBE, 2 cases had definite limb weakness (MMT ≤ 3) in at least one limb, defined as BBE-GBS. B) The frequency of recurrent cases of GBS, MFS, and BBE were 4% (2/55),
12% (4/34), and 25% (2/8), respectively.
cases (2%) had definite limb weakness and were thought to represent
BBE-GBS. Anti-GQ1b IgG antibodies were positive in 27 (79%) of 34
MFS cases and five (63%) of 8 BBE cases.
Two (4%) of 55 GBS patients, four (12%) of 34 MFS patients, and two
(29%) of 8 BBE patients had recurrences (Fig 1B). One of the four recur-
rent MFS cases was MFS-GBS, and one of the two recurrent BBE cases
was BBE-GBS. One of the patients with recurrent BBE had three epi-
sodes. All other patients with recurrent GBS, MFS, or BBE had only two
episodes. The median interval between attacks was 6 years (range,
3–31 years) in all the recurrent cases.
To examine the clinical and laboratory features of recurrent cases in
more detail, we focused on recurrent and non-recurrent cases of MFS
because recurrent cases of GBS and BBE occurred too infrequently to
allow for statistical comparisons. The median age at the onset of symp-
toms was 37 years (IQR; 23–57) in patients with non-recurrent MFS and
22 years (IQR; 21–26) in patients with recurrent MFS (p = 0.091,
Table 1). Anti-GQ1b IgG antibodies were positive in 23 (77%) of 30
non-recurrent MFS cases and four (100%) of four recurrent MFS. In ad-
dition, no significant difference was found in the percentage patients
who were male, details of the symptom course, or the results of nerve
conduction studies between cases of non-recurrent and recurrent MFS
(Table 1).
Table 2 shows the clinical and laboratory features and the clinical
courses of patients with recurrent GBS, MFS, and BBE. One of the re-
current GBS patients, one of the recurrent MFS patients, and both of
the recurrent BBE patients were admitted to our hospital during
every episode. Others were admitted to other hospitals during their
first episodes, so data were based on the information provided by
other hospitals. In each patient, recurrent episodes occurred at ap-
proximately the same time of year as the first episode and displayed
similar clinical features to the initial presentation. Concretely, one of
the four recurrent MFS cases was MFS-GBS. She presented MFS-GBS
in both episodes. The other three recurrent MFS cases presented MFS
without definite limb weakness in both episodes. One of the two re-
current BBE cases presented BBE without definite limb weakness in
both episodes. The other had three episodes. Her first and second ep-
isodes were BBE-GBS, and the third one was BBE without definite
limb weakness. There was a tendency for the duration of hospital
stay to be shorter during the recurrence compared with the first ep-
isode in individual recurrent patients. Functional grade at peak of re-
currence was the same or lower than that of the first episode. One
representative recurrent MFS case we examined in both episodes
(Patient 3) is described below.
 J. Ishii et al. / Journal of the Neurological Sciences 364 (2016) 59–64
Table 1
Comparison of recurrent and non-recurrent Miller Fisher syndrome patients.
Non-recurrent (n = 30) Recurrent (n = 4) p value
Age at first episode (years) 37 (23–57) 22 (21–26)
Male 67 (20/30) 50 (2/4)
Preceding infection 80 (24/30) 50 (2/4)
Days to peak disability 7 (6–8) 6.5 (5–9)
Functional grade at peak 2 (1–3) 2.5 (1–3)
Days of hospital stay 17 (12–29) 9.5 (4–21)
Anti-GQ1b antibody 77 (23/30) 100 (4/4)
NCS abnormality* 87 (26/30) 100 (4/4)
NCS: nerve conduction study, *: any of lowering of CMAP amplitude, MCV, SNAP ampli-
tude, SCV, or F wave frequency, or prolongation of F wave minimal latency. Data are
shown as medians (interquartile ranges) or percentages (number of patients).
a
Wilcoxon rank sum test.
b
Fisher's exact test.
Patient 3. A 21-year-old woman experienced a sore throat, high fever,
and shivering 3 days after eating raw beef and chicken. She had diarrhea
from days 4 to 6. On day 8 she noticed diplopia, on day 9 she had difficulty
walking, and on day 10 she was admitted to our hospital. She presented
with ophthalmoplegia, ataxic gait, hyporeflexia, paresthesia, and mild
limb weakness. CSF protein concentration was elevated without
pleocytosis on day 10. Her brain MRI was normal. We diagnosed her
with MFS and administered intravenous immunoglobulin (IVIG;
400 mg/kg/day, for 5 days). She gradually recovered within 2 weeks.
Ten years after the initial episode, she again developed mild paresthesia,
mild ataxic gait, trivial limb weakness, and diplopia. This instance oc-
curred without preceding infection. On day 9, symptoms began to im-
prove without treatment, and she was found to have mild ataxic gait,
hyporeflexia, trivial limb weakness, and mild paresthesia. No therapy
was given, and she recovered fully within the following week. At the
first episode, serum anti-GQ1b, anti-GT1a, and anti-GM1b IgG antibodies
were detected, and at the recurrence anti-GalNAc-GD1a IgG antibodies
were detected in addition to those previously found (Fig 2). During the
second episode, symptoms were mild, but positive anti-ganglioside anti-
bodies including GQ1b confirmed the diagnosis.
4. Discussion
To our knowledge, no epidemiological studies have specifically
assessed the prevalence and incidence of MFS. The frequency of MFS
was 3% (4/138 cases) of all GBS spectrum disorders in a population-
based prospective survey in Italy [5], and 7% (7/103 cases) in a prospec-
tive case-control study in England and Wales [6]. In contrast, two retro-
spective single-hospital studies conducted in Taiwan in 1997 and 2000
found the percentage of MFS among GBS was 19% (32/167 cases) and
18% (11/60 cases), respectively [7,8]. A retrospective review of the
case records of all patients with GBS or MFS at a hospital in Singapore
showed the percentage of MFS cases was even greater, 26% (8/21
cases) [9]. Further, an ongoing prospective study of GBS patients in a
multi-ethnic Malaysian cohort found MFS in 47% (17/36 cases) of all
GBS spectrum disorders over 2 years [10]. In Japan a multicenter retro-
spective study and a prospective study demonstrated that MFS
accounted for 26% (53/201 cases) and 26% (79/301 cases) of all GBS
spectrum disorders, respectively [11,12].
Only one study has specifically examined the epidemiology of BBE in
Japan [27]. It estimated that the annual onset of BBE is roughly 100 cases,
and the annual incidence of BBE is approximately 0.078 per 100,000 in-
habitants, or 6.8% of all GBS spectrum disorders. No available reports
have addressed the frequency of BBE in any other country except Japan.
In our study, GBS, MFS, and BBE accounted for 57%, 35%, and 8% of all
GBS spectrum disorders, respectively. This is the first study to provide
the frequency of GBS, MFS, and BBE in a single hospital. The frequency
of MFS and BBE was slightly higher than that found in the previous
Japanese studies likely owing to a small difference in definitions [11,
12]. MFS with severe limb weakness was included in MFS in our
61
study. Despite these differences, similar to the previous studies in
Japan, the frequency of MFS at our hospital was higher than those in
European countries. Because the annual incidence rate of GBS is not so
0.091a
different in these countries [4,28], MFS might occur more frequently
0.60b in Asian countries such as Japan than in western countries.
0.23b Recurrent GBS cases were reported in 4%–7% of patients [14,23,29].
0.70a There are several case reports of recurrent MFS [16–19]. However, we
0.89a
could find only two studies that measured the frequency of recurrence
0.16a
0.56b [13,15]. In two different Japanese hospitals, Chida et al. found four recur-
1.00b rent cases (14%) out of 28 total MFS cases that occurred over 15 years
from 1981 to 1996 [15], and Neshige reported four recurrent MFS
cases (11%) out of 37 total cases [13]. These results are similar to ours
(12%). However, no study has yet been conducted to compare the fre-
quency of recurrent GBS and MFS at a single hospital, and there is no
study that mentions the frequency of BBE. In this study, we first re-
ported that the frequency of recurrence in GBS, MFS, and BBE was 4%
(2/55 cases), 12% (4/34 cases), and 25% (2/8 cases), respectively.
Currently, BBE is thought to exist on the same spectrum as MFS by
virtue of their common clinical and immunological profiles [3]. Recur-
rent BBE has been thought to be quite rare, and there is some doubt re-
garding whether BBE can recur at all [21]. Only three recurrent cases of
BBE have been reported [20–22]. Two patients had no anti-GQ1b anti-
bodies, and therefore could not be definitely diagnosed with recurrent
BBE [20,21]. The present study included two patients with recurrent
BBE. Both had anti-GQ1b IgG antibodies, so we assert that BBE can
recur. Considering MFS and BBE together as anti-GQ1b IgG antibody
syndrome [30], the frequency of recurrent cases with GBS and anti-
GQ1b IgG antibody was 4% (2 of 55) and 14% (6 of 42), respectively.
The frequency of recurrence in MFS or BBE was higher than in GBS, al-
though this difference was not statistically significant (p = 0.07).
We compared characteristics of patients with recurrent MFS with
those with non-recurrent MFS and found no obvious clinical or electro-
physiological differences except the age of onset. Patients with recur-
rent MFS tended to experience their first episode at a younger age
than those with non-recurrent MFS. In a previous single hospital report,
the mean ages of patients with recurrent and non-recurrent MFS were
29 ± 15.4 and 39 ± 16.8 years, again reflecting a tendency for onset
to occur at a younger age in patients with recurrent MFS [15]. In a re-
view article including 28 adult patients with recurrent MFS, the mean
age of onset was 32 [16]. A recent report has described, for the first
time, two children with recurrent MFS [19]. The authors argue that pe-
diatric neurologists may have difficulty recognizing recurrent MFS, so
there might be more children with recurrent MFS, and the mean age
of patients with recurrent MFS might be younger. One study of 32 pa-
tients with recurrent GBS showed that the mean age of onset was signif-
icantly younger in the recurrent group compared with non-recurrent
GBS patients [23]. These studies suggest that younger patients may be
more susceptible to recurrence of GBS spectrum disorders.
The characteristics of recurrent episodes were quite similar to those
of the first episode regardless of the preceding infection. This is consis-
tent with the findings of previous reports [16,23], and suggests that im-
munological host factors play an important role in determining the
clinical phenotype of GBS spectrum disorders. For each recurrent pa-
tient, subsequent episodes happened at similar times of year as the
first one. For example, for Patient 8, the first and second episode hap-
pened in May, and the third happened in June. This could suggest that
seasonal factors like viruses or bacteria may contribute to the onset of
disease. In our recurrent cases, symptoms were less severe during the
recurrence than during the first episode. To determine whether patients
at other institutions displayed a similar pattern, we conducted a
PubMed search that identified studies including a total of 32 (30 adults
and 2 children) patients with recurrent MFS. Details of clinical courses
were described for 14 patients [15,17–19,22,31–37]. There were 18 re-
current episodes in these 14 patients. Six episodes were milder than
the original occurrence, and 12 were more severe than the first episode.
Therefore, no conclusions can be made about the severity of recurrences
 62
Table 2
Clinical feature and laboratory findings in patients with recurrent cases of Guillain-Barré syndrome, Fisher syndrome, and Bickerstaff brainstem encephalitis.

Guillain-Barré syndrome Miller Fisher syndrome Bickerstaff brainstem encephalitis

Patient no. sex 1 Woman 2 Man 3 Woman 4 Woman 5 Man 6 Man 7 Man 8 Woman

J. Ishii et al. / Journal of the Neurological Sciences 364 (2016) 59–64

Interval (years) 3 31 10 6 16 6 5 3 17
Episode First Second First Second First Second First Second First Second First Second First Second First Second Third
Age (years) 67 70 8 39 21 31 23 29 21 37 27 33 53 59 25 28 45
Preceding illness Diarrhea – Diarrhea Diarrhea URI Diarrhea – URI URI URI URI URI – URI URI Diarrhea URI URI URI
Month at the episode December February ** March February March January January March March February November January April May May June
Functional grade at peak 5 2 ** 3 2 1 3 3 2 3 5 4 4 4 1
Days of hospital stay 206 46 ** 15 8 3 47 23 37 5 22 14 60 27 43 60 18
Symptoms
Limb weakness + ± ** + ± ± + + – ± – – – – + + ±
Paresthesia + + ** + + + + + + + – – + + + + +
Areflexia + + ** + + + + + + + – + + + + +
Ataxia + + ** ± + ± + + + + + + + + + + ±
Ophthalmoplegia – + ** – + + + + + + + + + + + + +
Disturbance of consciousness + – ** – – – – – – – – – + + + + +
Respirator care + – ** – – – – – – – – – – – – – –
Facial palsy + – ** – – – + – – – + – – – – – –
Babinski reflex – – ** – – – – – – – – – + n.e. + + +
Involuntary movement – – ** – – – – – – – – – + + –
Subtype MFS-GBS MFS-GBS BBE-GBS BBE-GBS
IgG antibodies to GM1 – ** GD1b GQ1b GQ1b GQ1b±* GQ1b GQ1b* GQ1b GQ1b* GQ1b GQ1b GQ1b n.e. n.e. GQ1b
GT1a GT1a GT1a GT1a GT1a GT1a GT1a GT1a
GM1b GM1b GT1b GD1a
GalNAc-GD1a GD1b GD1b
GM1b
GalNAc-GD1a

GBS: Guillain-Barré syndrome, MFS: Miller Fisher syndrome, BBE: Bickerstaff brainstem encephalitis, URI: upper respiratory infection, Limb weakness +: MMT ≤ 3 at least one limb, Limb weakness ±: MMT ≥ 4, MFS-GBS: MFS with definite limb
weakness (MMT ≤ 3), BBE-GBS: BBE with definite limb weakness (MMT ≤ 3), n.e.: not examined, *: no information about other antibodies except GQ1b, **: no information.
 J. Ishii et al. / Journal of the Neurological Sciences 364 (2016) 59–64
Fig. 2. Anti-ganglioside IgG antibodies profile of a patient with recurrent Miller Fisher
syndrome (Patient 3). Anti-ganglioside IgG antibodies were measured by an enzyme-
linked immunosorbent assay. During the first episode, serum anti-GQ1b, anti-GT1a, and
anti-GM1b IgG antibodies were detected. During the recurrence, antibodies against
GalNAc-GD1a IgG were also detected in addition to the three antibodies detected during
the first episode.
of MFS compared with initial episodes. In Patient 3 in the present study,
the anti-ganglioside antibody profiles of the first and second episodes
were almost identical with the exception of the anti-GalNAc-GD1a anti-
body, which was detected only during the second episode. We could not
check the antibody titers at the recovery phase of the illness, so there is a
possibility that the antibody titers remained elevated from the first to
the second episodes. However, it has been reported that anti-
ganglioside antibody titers peak early in the disease, followed by a grad-
ual decline in patients with GBS or MFS [38]. Therefore anti-ganglioside
antibodies were likely elevated again at the recurrent episode and
showed a pattern similar to that in the initial episode. Production of
the anti-GalNAc-GD1a antibody has been reported to be associated
with gastrointestinal infection and acute motor axonal neuropathy
[39,40], but during the second episode Patient 3 did not notice any pre-
ceding infectious symptoms. Therefore, the role of anti-GalNAc-GD1a
antibody during her second episode is unclear.
We had small number of recurrent cases in this study, and further
large-scale studies would be required to clarify the clinical and labora-
tory features of recurrent patients with GBS, MFS, or BBE.
5. Conclusion
In summary, MFS accounts for a greater percentage of all GBS spec-
trum disorders in East Asian countries such as Japan than in western
countries. Recurrence of MFS or BBE (anti-GQ1b IgG antibody syn-
drome) is not rare and occurs more frequently than recurrence of GBS.
Patients with recurrent MFS had a tendency to be younger at onset
than patients with non-recurrent MFS.
Financial disclosure
Dr. Ishii, Dr.Yuki, Dr.Kawamoto, Dr. Yoshimura, Dr. Kusunoki, and Dr.
Kohara report no disclosures.
Author contributions
Drafting/revising the manuscript: JI. Study concept and design: NY
and NK. Acquisition, analysis, and interpretation of data: MK, HY, and
SK.
63
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