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Neuroepidemiology 2010;34:171183
DOI: 10.1159/000279334
Key Words
Myasthenia gravis, incidence Review literature
Epidemiology
Abstract
Background: A systematic review of literature published between 1980 and 2007, on the incidence of myasthenia gravis,
was undertaken. Methods: All relevant papers found through
searches of Medline, Embase and Science Direct were critically appraised and an assessment was made of the reliability of the reported incidence data. Results: Thirty-one studies were included in the review, the majority of which investigated populations in Europe. The incidence rates reported
were between 3.0 and 30.0/1,000,000/year. However, it is
thought that the rates at the upper end of this range, reported by the prospective studies, provided the most accurate
estimates. Overall, incidence rates have increased over time
owing to a greater awareness of the disease and improved
methods of diagnosis. Conclusions: The most accurate estimate of incidence of myasthenia gravis was around 30/
1,000,000/year. The incidence in children and adolescents
aged 019 years was found to be between 1.0 and 5.0/
1,000,000/year. The rates presented in this review are likely
to be an underestimate of the true incidence rates, as mild
cases will have been missed and cases in the elderly will have
been misdiagnosed.
Copyright 2010 S. Karger AG, Basel
Introduction
Method
Searches of the Medline (1980June 2007), Embase (1980
2007) and Science Direct (19802007) databases were conducted
using the keywords myasthenia gravis and incidence or epidemiology.
The inclusion criteria were that the studies reported original
work, that the estimates of population size and person time contributed were accurate and that no or very few incident cases were
172
Neuroepidemiology 2010;34:171183
Results
Incidence Rates
Geographical Variation
Most of the studies included in this review reported on
incidence rates for populations in Europe: the rates from
1970 to 2000 varied between 4.1 [13] and 30/1,000,000/
year [14]. Six studies reported on regions outside Europe:
Tanzania, Hong Kong, Japan, North America, Cuba and
Curaao and Aruba and the incidence rates found in
these areas ranged from 3.0 to 9.1/1,000,000/year.
Variation with Age and Sex
In most studies reporting incidence rates for males
and females separately, the incidence increased with increasing age. In studies of incidence rates in males, the
rates increased up to the 60- to 80-year age band in most
studies [13, 1525], with 2 showing an increase to the 40year age band [26, 27] and 2 reporting fluctuations in rate
with age but an overall increase [28, 29]. In females, there
was more fluctuation in incidence rates with age with
some studies showing a peak in incidence at 2040 years
and then a second one at 5070 years [15, 17, 1923, 26,
27, 29], others just had a peak in incidence in the latter age
band [13, 18, 24]. In some studies [13, 20, 22, 25, 29, 30]
the incidence in the elderly (65 or 70 years upwards) was
reported to be 0/1,000,000/year, which indicates possible
underdiagnosing or misdiagnosing of patients in this
group [20, 30].
In children (019 years) the incidence in males was
low (up to 3/1,000,000/year) and did not show an overall
association with age; in females it was higher (up to
11/1,000,000/year [24]) and increased with increasing
age.
12 secondary papers
appraised
32 papers rejected
Accuracy of Rates
The main causes of missing cases in the studies were
mild symptoms or cases being diagnosed and managed in
primary care but the case finding strategy of the incidence
study only including secondary care records [1618, 20
25, 27, 30, 37, 40, 41], death before a diagnosis was made
[17, 21, 22, 27, 42] and misdiagnosis [36, 42]. Most studies
used similar methods and criteria for diagnosing cases
Neuroepidemiology 2010;34:171183
173
174
Neuroepidemiology 2010;34:171183
As above
Nagano Prefecture,
Honshu Island, Japan
Norway
East Denmark
(East of the Great Belt)
Eastern Denmark
Peninsula of Jutland
and several islands,
Western Denmark
Viborg County,
Denmark
Amsterdam,
The Netherlands
Northern Region of
South Holland,
The Netherlands
Trento
(Northern Italy)
Storm-Mathisen [16]
Risk of underestimationb
Risk of overestimationa
Cases: 557
Oosterhuis [31]
Risk of underestimationb
Risk of overestimationa
Cases: 17
19511981
incidence:
diagnosis
onset
19821986
19871991
19921996
19972001
19751987
19811990
19611965
19731987
19701979
19801989
19901999
Hong Kong
(Chinese only)
Yu et al. [32]
Risk of underestimationb
Risk of overestimationa
Cases: 202
19881998
Dar es Salaam,
Tanzania (African)
Period
Location
Study
Table 1. Summaries and incidence rates for studies included in the systematic review
10.41
4.1
5.8
7.9
4.4
4.01
both
All
4.61
All (excl. 3.21
thymoma
cases)
101
7.81
5.0
female
3.7
male
Rate/1,000,000 /year
All
All
All
All
All
All
All
All
All
All
All
All
Age
Neuroepidemiology 2010;34:171183
175
Province of Ferrara,
Emilia-Romagna
Region, Italy
Emilia-Romagna
(7 provinces), Italy
North-West Sardinia,
Italy
Emilia-Romagna
Study Group [28]
Risk of underestimationa
Risk of overestimationa
Cases: 86
All
19801994
Greece
UK (9 centres
carrying out most
tests in the UK)
Cambridgeshire, UK
19921997
19971999
19831997
County of Osona,
Barcelona, Spain
Sardinia, Italy
19581986
19581967
19681977
19781986
19821994
19931994
24 (19, 30)1
17 (13, 23)1
All
All
All
All
All
All
11.11
18
2.7
1.7
2.3
3.0
8 (5, 12)1
3.9
9 (5, 15)1
21 (17, 25)1
3.1
1.4
6 (3, 11)1
All
Diagnosis 13.8 (9.8, 21.3)
onset
8.3 (5.7, 13.1)
All
All
19691989
North-East Italy
176
Neuroepidemiology 2010;34:171183
19761996
Retrospective: database records; typical history,
clinical findings including weakness by repeated muscle
contraction with recovery at rest, improvement with AChE
drugs, reduction in electrical amplitude on RNS, detection
of anti-AChR antibodies
Retrospective: hospital and GP records; FMW and positive
response to AChE drugs; other tests also carried out;
Ossermans classification used; incidence at onset7
Retrospective: hospital records; FMW, involvement of
voluntary muscles, fatigue, improvement with AChE
County of the
Coast and Gorskikotar,
Croatia
Belgrade, Yugoslavia
Benghazi, Libya
19801995
Cuba
19701984
19831986
All
All
All
All
All
All
All
19701996
Estonia
19901997
All
Tayside, Scotland
Farrugia [38]
Risk of underestimationa
Risk of overestimationc
Cases: 44
Retrospective: hospital records reviewed; FMW, positive
response to AChE drugs; doubtful diagnoses discussed;
all suspected cases seen by a neurologist
All
13 GP practices in
the London area, UK
All
All
Age
Croydon, UK
Period
Location
Study
Table 1 (continued)
8.36
6.81, 2
5.86
2.11, 2
4 provinces
4 different
provinces
female
male
Rate/1,000,000/year
9.1
4.41, 2
7.16
10.51
30 (8, 70)3
both
including detection of anti-AChR antibodies and identification of clinical features such as abnormal fatigue and
patient response to treatment. Three studies [21, 38, 40]
only included patients who were seropositive for antiAChR antibodies, which will have underestimated the incidence rates by about 15% [1, 4, 40]. Ten investigations
used census or other national statistics data for their denominator [21, 22, 24, 27, 29, 31, 36, 39, 40, 43], one did not
give any denominator data [13] and the others provided
denominator estimates but did not give their source.
Overestimation of incidence rates was thought to be
unlikely where specialists diagnosed or reviewed the cases included [14, 16, 18, 19, 2427, 29, 32, 36, 37]; other
studies reported reliable case identification [40], using a
3-year follow-up period to ensure correct diagnosis [23]
and a regular clinical follow-up to exclude questionable
cases [13]. Another important factor in reducing the possibility of overestimating cases is owing to the changes
that have taken place in diagnosing myasthenia gravis
[22, 28, 33, 36]: Oosterhuis [31] reported that he retested
patients with a diagnosis established before 1985 who
were still alive and traceable and found that 26 of 29 patients were positive for anti-AChR antibodies; the remaining patients were thought to have had seronegative
myasthenia gravis.
Discussion
Table footnote
Figures in parentheses are 95% confidence limits. Incidence rates given/1,000,000/year; risk of under- or overestimation: low (a), medium (b), high
(c). ECT = Edrophinium chloride test; MGFA = Myasthenia Gravis Foundation of America; FMW = fluctuating muscle weakness; MW = muscle weakness; AChE = anticholinesterase; RNS = repetitive nerve stimulation; EMT =
eye movement tests; RF = rapid fatigue; AI = autoimmune. 1 Incidence rate
confirmed using data given in paper; 2 age-adjusted to the Libyan population;
3
age- and sex-adjusted to the UK population; 4 age- and sex-adjusted to the
world standard population; 5 age-adjusted to 1991 Croatian population;
6
standardised to Dolls world population; 7 no details given about criteria
used for diagnosis at onset; Somnier et al. [30] note that onset can be up to
2 years before diagnosis; incidence at diagnosis unless otherwise specified;
8 95% confidence limits calculated from data given in paper.
177
Sex
M
F
04
2.51, 2
0.11, 2
59
01, 2
0.91, 2
1014
0.11, 2
4.31, 2
1519
0.21, 2
6.31, 2
2024
3.31, 2
9.71, 2
2529
3.71, 2
2.61, 2
3034
3.71, 2
5.91, 2
3539
1.31, 2
7.01, 2
4044
2.21, 2
3.91, 2
4549
2.41, 2
4.21, 2
M
F
04
0
1
59
1
0
1014
1
1
1519
3
6
2024
3
17
2529
6
17
3034
3
15
3539
8
18
4044
8
11
4549
14
14
M
F
09
0.1 (0, 0.3)4
0.42 (0, 0.9)4
1019
0.98 (0.4, 1.7)4
4.6 (3.3, 6.2)
2029
2.09 (1.1, 3.2)4
8.6 (6.7, 11.0)4
3039
2.74 (1.6, 4.1)4
8.2 (6.3, 10.7)4
4049
3.7 (2.4, 5.3)4
6.1 (4.5, 8.2)4
M
F
09
1.01
0.21
1019
0.51
5.01
2029
3.01
6.51
3039
2.51
6.01
4049
2.41
5.01
M
F
B
09
0.7 (0.1, 2.6)
1.5 (0.4, 3.8)
1.1 (0.4, 2.4)
1019
1.2 (0.3, 3)
4 (2.1, 6.8)
2.6 (1.5, 4.1)
2029
2.2 (0.9, 4.6)
7 (4.4, 10.6)
4.6 (3.1, 6.7)
3039
2.1 (0.9, 4.4)
6.1 (3.7, 9.5)
4.1 (2.6, 6.1)
4049
2.1 (0.7, 4.8)
5.1 (2.6, 8.8)
3.6 (2.1, 5.7)
M
F
09
0
2.2
1019
2.2
5.4
2029
0.8
4.5
3039
1.6
4.0
4049
1.8
5.0
M
F
B
09
7 (0, 17)4
0
4 (0, 9) 4
1019
2 (0, 7)4
5 (0, 13)4
4 (0, 8)4
2029
2 (0, 7)4
11 (1, 21)4
7 (1, 12)4
3039
7 (1, 15)4
14 (3, 25)4
10 (4, 17)4
4049
5 (2, 11)4
5 (0, 12)4
5 (0, 9)4
M
F
B
09
4.1
0.0
2.1
1019
0.0
3.1
1.5
2029
0.0
14.8
7.2
3039
9.2
13.1
11.1
4049
6.9
10.2
8.6
Giagheddu et al.
[26]
M
F
B
010
0.0
0.5
0.2
1120
1.0
4.7
2.8
2130
0.9
4.4
2.7
3140
1.1
5.7
3.4
4150
4.0
5.2
4.6
Oopik et al.
[20]
M
F
B
09
1.3 (0.3, 3.3)
0.7 (0.1, 2.49)
1 (0.4, 2.2)
1019
2.7 (1.2, 5.4)
5.9 (3.4, 9.5)
4.2 (2.7, 6.3)
2029
1.6 (0.5, 3.6)
5.8 (3.4, 9.2)
3.7 (2.3, 5.5)
3039
2.2 (0.8, 4.7)
7.4 (4.6, 11.3)
4.8 (3.2, 7)
4049
1.9 (0.6, 4.4)
4.5 (2.4, 7.7)
3.3 (1.9, 5.2)
M
F
B
09
0.01, 3
0.01, 3
0.01, 3
1019
0.01, 3
8.01, 3
4.51, 3
2029
4.01, 3
13.61, 3
8.21, 3
3039
3.41, 3
12.91, 3
7.21, 3
4049
5.81, 3
5.81, 3
5.81, 3
M
F
B
09
0.0
0.0
0.0
1019
3.1 (0, 13.6)
9.4 (0, 28.3)
6.2 (0, 13.8)
2029
4.0 (0, 19.7)
19.1 (0, 51.9)
11.5 (0, 24.3)
3039
0.0
8.5 (0, 33.0)
4.3 (0, 13.2)
4049
20.3 (0, 65.3)
0.0
9.8 (0, 24.9)
2029
4.0
8.3
6.2
3039
3.4
9.2
6.4
4049
4.1
9.9
7.0
Somnier et al.
[30]
Vincent et al.
[15]
StormMathisen
[16]
Somnier and
Engel [13]
Christensen
[17]
Wirtz et al.
[18]
Guidetti et al.
[19]
Ferrari and
Lovaste [29]
Lavrnic et al.
[21]
Aiello et al.
[27]
Zivadinov et al.
[22]
M
F
B
019
2.6
0.0
1.4
Casetta et al.
[23]
014
01
41
21
178
M
F
B
Neuroepidemiology 2010;34:171183
1524
31
111
71
2534
141
291
211
3544
151
261
211
4554
231
241
241
5559
8.81, 2
5.81, 2
6064
3.81, 2
6.51, 2
6569
12.21, 2
6.31, 2
7074
18.91, 2
9.41,2
7579
111, 2
6.61, 2
8084
16.11, 2
4.11, 2
8589
0.01, 2
4.31, 2
9094
0.01
0.01
5054
19
21
5559
25
21
6064
36
21
6569
67
39
7074
86
38
7579
94
47
8084
89
43
8589
72
29
9094
39
17
5059
3.7 (2.4, 5.3)4
5.3 (3.8, 7.3)4
6069
7.0 (4.9, 9.6)4
5.0 (3.3, 7.1)4
7079
3.5 (1.4, 5.8)4
6.7 (4.2, 9.6)4
80+
5.0 (0.6, 9.7)4
2.7 (0.1, 5.5) 4
5059
5.51
7.01
6069
13.01
8.01
7079
23.01
12.51
8089
20.01
14.01
5059
5.2 (2.6, 9.2)
7.3 (4.1, 9.2)
6.2 (4.1, 9)
6069
15.1 (10.3, 21.1)
9.7 (5.9, 15)
12.4 (9.2, 16.3)
7079
14.1 (8.3, 22.3)
11.7 (7, 18.3)
12.9 (9, 17.1)
80+
8.6 (2.3, 22.1)
1.3 (0, 7.2)
5 (1.6, 11.6)
5059
6.0
8.0
6069
26.5
18.5
7079
28.5
22.4
80+
24.0
17.0
5059
7 (1, 16)4
10 (0, 19)4
8 (2, 15)4
6069
11 (0, 23)4
17 (5, 30)4
15 (6, 23)4
>70
10 (0, 21)4
9 (0, 17)4
9 (2, 16)
5059
7.7
3.6
5.6
6069
10.1
20.1
15.7
70+
0.0
14.1
8.9
5160
3.3
3.6
3.4
6170
2.9
5.9
4.5
70+
0.9
2.2
1.6
5059
3.6 (1.6, 7.1)
5.9 (3.4, 9.4)
4.9 (3.2, 7.2)
6069
4.5 (1.5, 10.5)
9.7 (5.8, 15.1)
7.8 (5, 11.6)
7079
10.5 (4.5, 20.6)
4.1 (1.6, 8.4)
6.0 (3.4, 9.9)
8089
0.0 (0, 14.2)
0.0 (0, 4.1)
0.0 (0, 3.2)
5059
11.51, 3
7.51, 3
9.81, 3
6069
27.01, 3
9.01, 3
16.51, 3
7079
29.31,3
20.81, 3
23.41, 3
80+
0.01, 3
12.61, 3
7.01, 3
5059
11.7 (0, 50.6)
16.0 (0, 57.9)
13.9 (0, 34.3)
60+
13.6 (0, 46.2)
11.0 (0, 34.7)
12.1 (0, 25.9)
5059
11.4
9.6
10.6
6069
15.3
4.6
9.1
5564
381
321
351
9099
01
41
70+
0.0
15.9
10.6
6574
281
261
271
75+
121
281
221
Neuroepidemiology 2010;34:171183
179
Table 2 (continued)
Study
Sex
EmiliaRomagna
Study Group
[28]
M
F
B
014
0.01
3.31
1.61
Matuja et al.
[39]
019
2.2 (1.4, 3.4)
Aragones et al.
[24]
M
F
B
014
0.0
10.8
5.0
Radhakrishnan et al.
[25]
020
0.0
6.7
3.3
M
F
B
1524
0.01
11.31
5.51
2534
4.31
13.71
8.91
3544
2.51
7.61
5.01
4554
15.11
12.21
13.61
2039
3.2 (2, 4.9)
4059
3.3 (1.4, 6.8)
2039
0.0
13.3
6.5
4059
7.5
0.0
4.0
1564
12.0
17.0
14.7
Figures in parentheses are 95% confidence limits. 1 Incidence rate read from graph; 2 age- and sex-standardised; 3 age- and sex-standardised to the
world population according to Doll; 4 95% confidence intervals calculated from data given in paper.
180
Age
0
(years)
04
59
09
09
09
010
1014
1519
1019
1019
1019
1120
2024
2529
2029
2029
2029
2130
3034
3539
3039
3039
3039
3140
4044
4549
4049
4049
4049
4150
5054
5559
5059
5059
5059
5160
6064
6569
6069
6069
6069
6170
70+
7074
7579
7079
7079
7079
80+
8084
8589
8089
8089
9094
9099
20
40
60
80
100
Males
Females
Neuroepidemiology 2010;34:171183
Ref.
No.
17
19
29
27
22
25
17
19
29
27
17
19
29
27
22
17
19
29
27
22
25
17
19
29
27
22
25
17
19
29
27
22
17
19
29
22
27
25
17
19
29
22
b 17
Age
(years) 0
09
09
09
09
019
020
1019
1019
1019
1019
2029
2029
2029
2029
2029
3039
3039
3039
3039
3039
2039
4049
4049
4049
4049
4049
4059
5059
5059
5059
5059
5059
6069
6069
6069
6069
60+
60+
7079
70+
70+
70+
80+
Incidence (/1,000,000/year)
20
40
60
80
100
Males
Females
6574
32.31
28.41
30.11
75+
10.91
12.31
11.81
60+
3.4 (0.6, 11.3)
65+
55.9
65.8
62.4
60+
13.9
0.0
7.2
Ref.
No.
15
15
18
21
40
23
28
24
15
15
18
21
23
28
15
15
18
21
23
28
15
15
18
21
40
23
28
15
15
18
21
23
28
15
15
18
21
40
23
28
15
24
15
18
21
40
23
28
24
15
15
23
28
18
21
18
21
15
15
c 15
Age
(years) 0
04
59
09
09
019
014
014
014
1014
1519
1019
1019
1524
1524
2024
2529
2029
2029
2534
2534
3034
3539
3039
3039
2039
3544
3544
4044
4549
4049
4049
4554
4554
5054
5559
5059
5059
4059
5564
5564
6064
1564
6569
6069
6069
60+
6574
6574
65+
7074
7579
75+
75+
7079
7079
80+
80+
8084
8589
9094
Incidence (/1,000,000/year)
20
40
60
80
100
Males
Females
Fig. 2. Incidence rates of myasthenia gravis by age band and sex for the 1970s (a),
1980s (b) and 1990s (c).
Neuroepidemiology 2010;34:171183
181
Conclusion
The most accurate estimate of incidence of myasthenia gravis was found to be around 30.0/1,000,000/year
(95% CI 870), with the incidence in children and
adolescents aged 019 years being between 1.0 and 5.0/
1,000,000/year. Few studies of incidence rates in popula-
Appendix
Ref Manager ID
Year published
tions from outside Europe have been published. Therefore, it is not possible to comment on the geographical
variation of rates. Improvements in the diagnosis of myasthenia gravis and a greater knowledge of the disease
have led to an apparent increase in incidence over time.
Although case identification in older people has improved with time, it is likely that the incidence in this
group of people is still underestimated.
Acknowledgements
This work was supported by a grant from GSK Biologicals. The
authors are grateful to Dr. Nicola Giffin, consultant neurologist,
for helpful comments on an earlier draft of the manuscript.
Case definition
Reasons
Low
Medium
Reviewer
High
Original in English?
Number of cases
Translation
Base population:
person years
Base population:
number of people
Excluded?
Notes
Country
Study dates
Region
Run in period
Ref Manager ID
Race
Other ethnic origin
Ethnic distribution
Type of rate
Incidence
Units
Lower CI
Upper CI
Gender
Multiple locations?
Time period
Figures checked?
Figures correct?
Other descriptor
Notes
Age range
182
Neuroepidemiology 2010;34:171183
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