An up-date on health-related quality of life in myasthenia gravis -results from population based cohorts
© Boldingh et al. 2015
Received: 10 April 2015
Accepted: 3 July 2015
Published: 1 August 2015
Current available therapies control Myasthenia gravis (MG) reasonably well, but Health Related Quality of life (HRQOL) remains lower than expected. The aim was provide insights in how HRQOL in MG stands across borders and time, compare the scores to general population controls and other chronic disorders and assess the impact of potential predictors for quality of life such as a) clinical characteristics b) antibodies c) thymoma and d) treatment in a population-based cohort.
We designed a population-based cross-sectional study including 858 patients, 373 from Norway and 485 from the Netherlands. The Short Form Health Survey 36 (SF-36) and a cross-cultural validated questionnaire were used. Data were in addition compared to the general population, other chronic diseases and previous studies.
Mean physical composite score was 59.4 and mental composite score 69.0 with no differences between the countries. The mean HRQOL score was lower in patients with bulbar and generalized symptoms (p < 0.001) compared to sex and age adjusted healthy controls, but not in patients with ocular symptoms or patients in remission. Multivariate analysis revealed that female gender, generalized symptoms and use of secondary immunosuppressive drugs at the time of testing were risk factors for reduced HRQOL.
Remission and absence of generalized symptoms were favorable factors for HRQOL in MG patients. Historically, the HRQOL levels have not changed since 2001 and no new clinical predictors could be detected in this exhaustive population-based study. Further studies should explore the impact of non clinical factors like ethnic variations, socio-economic and hormonal factors on HRQOL.
Overview over previous SF-36 studies amongst Myasthenia gravis patients
Author, country year
Number of patients
Outcome compared to norm population
Paul et al., USA, 2001 
Cohort from Patient organization MGFA
To describe HRQOL in MG patients compared to normative data
All, except mental health and bodily pain reduced compared to normative US population. Ratings of mood scale within 1 SD with US norm.
Generalized 100 %
Padua et al., Italy, 2002 
To evaluate the correlation of physician measures like Osserman and repetitive nerve stimulation to HRQOL outcomes
All domains largely reduced compared to normative Italian population.
Remission: 6.5 %
Ocular: 4.3 %
Generalized: 89 %
SF-36 and MGQ validation
To correlate MGQ, SF-36 and degree of neuromuscular abnormalities measured by single fiber-EMG and repetitive nerve stimulation (RNS)
Remission: 20 %
SF-36 and MGQ versus SF-EMG
Ocular: 20 %
Generalized: 60 %
Leonardi et al., Italy, 2010 
SF-36, WHO-das II
To describe HRQOL and disability profiles according to ICF’s biopsychosocial model.
In patients without symptoms similar to general Italian population, greater difference with more symptoms.
Raggi et al., Italy, 2010  (2 publications)
Remission: 24.5 %
To verify concordance between disease’s severity, HRQOL and disability in MG.
Ocular: 28.4 %
Generalized: 47 %
Winter et al., Germany, 2010 
SF-36, EuroQoL, EQ-5D-index score
To compare HRQOL in patients with amyotrophic lateral sclerosis (ALS), fascial scapula humeral muscular dystrophy (FSHD) and Myasthenia Gravis.
All domains reduced, except bodily pain compared to normative German population
Remission: 0 %
Comparison between ALS, MG and fascial scapula humeral muscular dystrophy.
Ocular: 45.9 %
Generalized: 43.2 %
Twork et al., Germany, 2010 
Cohort from German Myasthenia Associationa
To analyze quality of life and life circumstances
More than one SD from normative population data Germany on the following domains:
Female: PF, GH
Male: PF, RP, GH, SF, RE
Female > male
Clinical cohort, two university hospitalsa
To study factors associated with QOL in MG patients
Females lower scores than males, however P-value is not given.
Basta et al., Serbia, 2012 
SF-36, QMG, Hamilton rating, social support
To assess factors that might influence the HRQOL in MG patients
No population data available.
Remission: 39.1 %
Ocular: 8.7 %
Generalized: 52.2 %
These studies show that the disease has an extensive impact on physical, psychological and social wellbeing: the more severe muscle symptoms and disability, the lower the physical components of the outcome [1, 2, 7–10]. There are contradictory results as to what extend the mental wellbeing is affected in MG. Reported predictors for reduced HRQOL are among others use of prednisolone and side-effects, disease severity, depression, anxiety and disease duration, however, many others are also mentioned (Table 1). There are few larger studies and the impact of clinical subgroups based on antibodies, age of onset, thymus histology and clinical presentation remains unanswered [11–13].
Chronic immunomodulation with corticosteroid, other immunosuppressive drugs and thymectomy are often necessary to control the disease. Immunosuppressive medication produce marked improvement, however in many cases does the improvement not persist if treatment is discontinued. Consequently, treatment in MG is often a lifelong proces . The choice of treatment depends on the severity of the symptoms, the specific subgroups and the pace of progression . It is reported that MuSK MG and Thymoma MG are more likely to require secondary immunosuppressives than AChR MG and that elderly are more prone to side-effects [14–17]. As more advanced immunotherapy becomes available for MG patients, it is relevant to use HRQOL as an outcome for choice of treatment strategies. Long-term follow-up studies of representative MG cohorts assessing change of HRQOL during the last decades are lacking.
Up-to-date, there is no study reflecting the HRQOL of population-based MG cohorts covering the whole spectre of disease activity and immunological markers. Based on previous studies we hypothesized that serological subgroups, thymoma, disease course and treatment strategy are factors affecting HRQOL in MG patients. Our aim was to examine these factors and HRQOL in a MG cohort as large as possible, by combining population-based MG cohorts from two countries. We also compared the HRQOL outcomes of the MG patients to healthy controls, previous studies and other chronic diseases in order to get an impression of the burden of the disease.
The details of the study are reported in a previous study [19, 20]. The patients were mailed a self-administered validated questionnaire including the Short Form-36 (SF-36) and questions about disease severity and current treatment for the last three months . Reminders were sent to non-responders twice and missing data was completed by phone or mail.
Clinical characteristics, disease onset and course, presence of antibodies and thymus histology were collected from medical records.
Disease course was grouped into remission; either complete stable or pharmocological, ocular, bulbar or generalized symptoms at the time of testing. We subgrouped the ocular symptoms in those who started ocular and remained ocular throughout disease course (Ocular MG) and those who had residual ocular symptoms after generalized disease in the MG subgroup analysis. Non-steroid immunosuppresive medicines included azathioprine, cyclosporine, mycophenolate mofetil, tacrolimus, rituximab and cyclophosphamide.
The Norwegian and Dutch translations of SF-36 (version 1) was used to assess HRQOL [22, 23] in the past four weeks. This instrument is constructed for population surveys, is short and easy and has good psychometric qualities.
The SF-36 consist of 36 questions, organized into eight domains. The eight domains are physical functioning (PF), Role physical (problems with work or daily acitivites as a results of physical health, RP), Bodily pain (BP), general health evaluation (GH), Vitality (VT), Social functioning (SF), Role emotional (RE; severe problems with work or daily acitivites as a result of emotional health) and mental health (MH). All items are coded, scaled and transformed linearly from 0 (worst health) to 100 (best health). The first four can be summarized into a physical composite score (PCS; PF, RP, BP, GH) and the last four into a mental summary score (MCS; VT, SF, RE, MH).
We compared the two cohorts with published normative data, including reference data for chronic diseases (15 different conditions) and two population-based studies of Multiple sclerosis and Parkinsons disease [22, 24–26].
Regulatory and ethical issues
We obtained informed constent from all participants and approval of the regional ethical committee of South-Norway, the ethical review committee of the Leiden University Medical Center (LUMC), The Netherlands, and the Medical Review Ethics Committee (METC) of South-West Holland.
The statistical analysis was done using SPSS 22.0 (statistical package for social sciences, IBM, Armonk, NY, USA) and STATA 14 (StatCorp, Texas, USA). Scoring and calculation of the SF-36 scores were done according to the improved methods of Ware, McHorney and Sherbourne for version 1 [27, 28]. Method for impute missing data was followed for 0.7 % of the data. The MG patients were analyzed by domains and composite scores. Since the composite scores are considered as the most robust outcome measurement for the SF-36, we have focused on them in our comparisons. Differences in continuous variables were tested by independent sample t-tests and chi-square tests for contingency tables for categorical variables. When at least 25 % of expected cell frequencies were less than 5, Fischer’s exact test was applied. P < 0.05 was considered significant. Adjustment for the confounding effect of age, gender, disease severity and differences between both countries’ samples was done using linear regression analysis and stratum-specific estimates. We used the population-based cohort for all analysis (n = 837) either stratified by gender or country or pooled all together. For the immunological subgroup analysis, we included the responders of a national sample of MuSK MG patients (n = 21), leaving in total 856 MG patients for the analysis since the information about antibodies of eight patients was missing.
To examine the relationship between PCS/MCS and the significant covariates we used multiple regression analysis (p < 0.05) Afterwards, the model was employed on the MG subgroups with regard to antibodies to identify if the predictors played the same role in the subgroups.
Clinical characteristics of the population-based study cohort
Total cohort, n = 837
Dutch MG Cohort, n = 464
Norwegian MG Cohort, n = 373
Age [mean ± SD]
Mean age at onset [yrs ± SD]
Disease duration [yrs ± SD]
AChR MG b
Missing n = 9 (0.9 %)
Age at onset [n;%]
EOMG (<50 year)
LOMG (>50 year)
Juvenile MG (<16 years)
Disease course [n;%]
Current treatment [n;%]:
SF-36 [mean ± SD]
Physical composite score
Mental composite score
Comparison to healthy controls (Fig. 2)
The total cohort of MG patients had lower scores than healthy controls (p-value <0.005, adjusted for age and gender), except for the domains of bodily pain (BP) and problems with daily activities due to mental health problems (RE). Female MG patients systematically scored lower than male MG patients, with significant p-values <0.001 on all domains and composite scores (Additional file 1: Table e-1).
Patients in remission (MGFA class 0) (n = 196, 23.4 % of the cohort) and those with ocular symptoms (MGFA class 1) (n = 102, 12.2 %) scored similar or better than their national normative controls on composite scores. For both groups, the HRQOL of the domains were similar to controls, except for the domain of general health (GH), were the score was significantly worse in male MG patients in both the Netherlands as in Norway.
MCS in particular showed age-dependent divergent results (Additional file 1: Table e-1). In the Netherlands, the MCS was lower for those below 60 years of age; 50 % of the females and 31 % of the males compared to controls. In contrast, the elderly MG patients from 70 years of age had reduced MCS in Norway compared to controls, representing 16.3 % of the females and 46 % of the males.
HRQOL results in MG subgroups
SNMG (n = 115)
AChR MG (n = 626)
MuSK MG (n = 41)a
Thymoma-MG (n = 70)
Female [n, %]
Age at study entry [yrs, SD]
Mean age at onset [yrs, SD]
47.1 (22) c
Mean age at diagnosis [yrs, SD]
48.7 (21) c
Disease duration [yrs, SD]
Disease course [n, %]
Current treatment [n, %]
SF- 36 [mean, SD]
Despite different disease course and more immuno-suppressives in MuSK MG and Thymoma MG, there were no differences in HRQOL. No differences were observed between early and late onset MG groups (adjusted for age). Patients with generalized and bulbar symptoms had lower HRQOL scores compared to those with OMG, residual ocular symptoms after generalized disease and those in remission (p < 0.001). No difference could be detected between those with OMG and those with residual ocular symptoms after generalized disease. No difference in PCS or MCS could be detected when stratifying the cohort into those early MG (0-3 years after onset) and longer follow-up (>3 years after onset).
HRQOL and treatment
Current treatment with non-steroid immunosuppressive drugs affected PCS negatively independent of disease activity (p-value <0.05 when adjusted for age, sex and disease activity). Prednisolone alone did not lower the PCS, but did so in combination with other immunosuppressive medicines (p = 0.002) . Thymectomy did not affect HRQOL, regardless of the histology results, thymoma, atrophy or hyperplasia.
Correlations between SF 36 composite scores and clinical variables
Regression coefficients of physical composite score in 850 MG patients
Predictor variable Physical composite score
95 % CI
Muscular weakens in legs
Muscular weakness in neck
Muscular weakness in arms
Use of immunosuppressive drugs
R 2 change from basis model
Weakness legs and dyspnoe
Weakness legs and neck
Weakness legs and arms
Weakness legs and dyspnoe
Regression coefficients of mental composite score in 850 MG patients
Predictor variable Mental composite score
95 % CI
Muscular weakness in legs
Muscular weakness in neck
Muscular weakness in arms
R 2 change from basis model
Weakness neck, and female gender
Comparison to other chronic diseases (Fig. 4)
We compared a stratified sample of Norwegian MG patients with symptoms in their early disease phase (0-3 years after onset) with patients with Norwegian Multiple sclerosis, Parkinson’s disease and Swedisch Rheumatoid Arthritis of similar disease duration and mean age. MG patients scored similar than MS patients and higher than Parkinson patients and Rheumatoid Arthritis patients (tested by t-test).
In this population-based double cohort study, we report a reduced self-perceived HRQOL in Myasthenia Gravis patients with bulbar and generalized symptoms, while patients in remission, those with OMG and those with residual symptoms after generalized disease scored similar to healthy controls. Generalized disease course, gender, and treatment with secondary immunosuppressives were risk factors for decreased HRQOL. Having a distinct subgroup with an antibody marker, thymoma or early or late onset subtype did not influence the HRQOL outcome.
In addition to generalized weakness, dyspnoe and dysphagia, female gender, usage of secondary immunosuppressives were minor risk factors to reduced HRQOL, similarly to results form previous studies [9, 30, 31]. Some of the gender variability could be explained by a general gender effect as the pattern is similar as seen in the normal population [22, 24]. However, we know that hormonal factors affect the symptoms [32, 33] and could thus also contribute. The second finding may suggest that long term immunosuppressive therapy may not be as harmless as assumed. This is supported by a HRQOL study from Japan, which documented an impact of steroids and calcineurin inhibitors in two studies [30, 31]. The negative effects may be related to side-effects or to the burden of constant need of medication. As reviewed by Sanders , the initial goal of therapy should be reducing weakness as much and as quickly as possible. Balancing side effects of immunotherapeutic agents and treatment effect remains a challenge for the clinician. The correlation between secondary immunosupressive agents and reduction of HRQOL in MG patients indicates that it is important to keep in mind the benefits of usage contra the side effects, and aim at reducing dosage to lowest possible maintenance dose. This may in particular be important for ocular MG in which no RCT has yet documented effect of any secondary immunosuppressive treatment, neither on symptoms remission nor on prevention of generalized disease [34, 35].
Early MG scored similar to early MS, however when looking at longer follow- up reports HRQOL turns worse in MS . The explanation is probably because MS and Parkinsons’ disease have often a more progressive course with no or less treatment that stops progression. Rheumatoid arthritis, on the other hand, is associated with more pain and disability than MG which can explain the marked lower scores. Improvement of HRQOL scores are reported in RA within the same patients, but also improvement over the last decades [37, 38]. According to Grob et al.’s lifetime study of MG, the distribution, severity and course of disease is determined within the first two years  and many MG patients experience the worst phase of the disease in these years. One should therefore expect improvement in HRQOL with longer disease duration. Our study design was cross-sectional and limits therefore interpretation of HRQOL over time in the same patient. Hence, follow-up studies both of individuals over time are needed to learn more about HRQOL in MG. With better treatment strategies and therapautic options we do also expect improvement over the last decade, however the comparison with earlier studies did not confirm this. Limitations in these inter-study comparisons are that the patients are not matched in the study and many variables are not controlled, therefore the results are purely indicative.
The main strength of the study is the design, which is a true population-based, cross sectional survey of two well defined groups. Finding the same levels of HRQOL in both countries makes the results more reliable. All clinical subtypes of MG were present in sufficient numbers to give useful results. Disease specific questionnaires have been advocated for MG, and indeed may enable a more specific follow-up for the patients . Our intention was, however, to use a broadly validated questionnaire to provide insights in how HRQOL in MG stands across borders and time, compare the scores to general population controls and other chronic disorders. Correlations between the SF-36 and MG disease status has been proven in several studies, and may thus be trusted to give a fair picture of the burden of MG disease. A more disease specific instrument would be able to detect smaller changes in vision, speaking, chewing and swallowing better [1, 4–6], which was not the purpose in this study. Since the SF-36 has norm-based scoring, group level results of this study can be used to compare MG patients across countries and further improve the quality of health care systems in places where it is not optimal.
Taken together, this population based study of 857 MG patients found the same HRQOL levels as in 2001 , indicating no improvement in quality of life for MG patients despite more available immunotherapy choices and better diagnostics of MG subgroups. Although we included a large sample and patients with different clinical characteristics, we could not find any new clinical predictors for reduced HRQOL compared to the other studies. Therefore we suggest that the impact of non-clinical factors like job, socio-economic factors, physical activity and hormonal factors on HRQOL in MG patients should be explored in order to improve the quality of life in MG patients.
The authors are grateful to all participating neurological departments and clinics in Norway and the Netherlands. We also thank all MG patients for their participation. We are grateful to Marit Elverhøy (technical assistance) and collaborators within the FIGHT-MG project for their contribution in the study.
The project was mainly supported by FIGHT- MG EU FP7 frame program grant no 242210 (to MIB) and Euromyasthenia EU FP7 no 2005105 (to AHM). The project was also supported by grants from Unifor.no, Valsøe’s foundation, Wilhelmsen’s foundation, the Norwegian association for patients with muscle disease, Princes Beatrix foundation, Association Francaise contre les Myopathies.
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