Demographic-clinical profile of the patients with Myasthenia gravis

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1 611 Demographic-clinical profile of the patients with Myasthenia gravis Daiva Rastenytė, Antanas Vaitkus 1, Rimas Neverauskas 1, Valerijus Pauza 2 Institute of Cardiology, Kaunas University of Medicine, 1 Kaunas Medical University Hospital, 2 Clinic of Neurology, Kaunas University of Medicine, Lithuania Key words: myasthenia gravis, early signs, course, treatment. Summary. The aim of the study. To evaluate demographic and clinical features of the patients with myasthenia gravis. Material and methods. Retrospective analysis of medical data on 82 patients with myasthenia gravis, referred to the University Hospital of Kaunas during 1992 to Results and conclusions. More than a half of all patients with myasthenia gravis were female, and almost four fifths fell ill before the age of 50 years. The most common first sign of myasthenia gravis was unilateral or bilateral ptosis and diplopia. The Osserman-Genkins grade at onset was I in 34.1%, IIA in 35.4% and IIB in 30.5% of cases. Among thymectomised patients, the percentage of thymomas in late-onset group ( 50 years) was higher than in the early-onset group (<50 years). Mortality rate was 7.3%. Myasthenic crisis was the main cause of death in all cases. Overall, 99% of patients were treated with acethylcholinesterase inhibitors and 92% with prednisolone at some time. Pharmacological remission was observed in more than 40% of patients. Prospective design of the study is recommended for the research of chronic noncomunicable diseases since it allows to evaluate the course and progression of the disease, effectiveness and side-effects of the treatment in more precise way. We used retrospective data in this study, therefore the results should be considered keeping in mind the possibility of bias and as the basis of prospective autoimmune myasthenia gravis studies in future. Introduction Myasthenia gravis is an acquired autoimmune disease, the main feature of which is a production of IgG-class antibodies against postsynaptic nicotinic acetylcholine receptors (AChRs). Because of that reduction of functional AChRs occurs and neuromuscular transmission deteriorates. Myasthenia gravis is one of the relatively rare diseases of nervous system; there are 2-11 new cases of myasthenia gravis per 1 million population per year (1-3). With the implementation of modern treatment modalities, mortality has changed from 25-30% to 5% during the last few decades (4,5). Also, the patient s quality of life has improved considerably. Pharmacological remissions are achieved in 30-50% of patients within 5 years from onset (6,7). Since myasthenia gravis is a chronic disease with a spontaneous remission rate only 1% per year (8), specific treatment has to be given over long periods, even lifelong. On the other hand, although pathogenesis of myasthenia gravis is rather well known and specific treatment is accessible to everybody, due to differences in gene pool, differences in socio-economic conditions, there may be some differences in the clinical features, course and prognosis of certain diseases in different populations. Except some results of thymectomy (9), peculiarities of the disease occurrence, course, and treatment were not analyzed in Lithuania so far. Therefore in this paper we present results of the retrospective analysis of demographic and clinical features of the patients with myasthenia gravis treated in the Department of Neurology of Kaunas University Hospital. Material and methods In this study, medical data on 82 patients with myasthenia gravis, referred to Kaunas University Hospital in , were analyzed. The records Correspondence to D.Rastenytė, Institute of Cardiology, Kaunas University of Medicine, Sukilėlių 17, 3007 Kaunas, Lithuania

2 612 Daiva Rastenytė, Antanas Vaitkus, Rimas Neverauskas, Valerijus Pauza Men of all patients were reviewed retrospectively. In total 285 records were reviewed. Data concerning the early phase of the disease and the diagnosis were collected, particularly demographic data, first symptoms, course of the disease, diagnostic and treatment methods, and results of treatment. Diagnosis of myasthenia gravis was based on following diagnostic criteria: 1) fluctuating muscle weakness with early fatigability; 2) improvement of strength after rest; 3) reduction in, or disappearance of signs after i.v. acetylcholinesterase (AChE) inhibitors. The severity of the disease at the time of diagnosis was classified according to Osserman and Genkins (1) as follows: I ocular disease only (ptosis, diplopia); IIA mild generalized (ocular and extremities) with no prominent bulbar signs; IIBmoderate generalized (ocular and/or bulbar signs, variable limb muscle involvement), no crises; III acute fulminating generalized signs with prominent bulbar involvement and crises; IV- late severe generalized and prominent bulbar signs and crises. To evaluate the outcome of various treatments, patients were divided into four groups according to the classification of Newsom and Davis (11): 1) patients of all ages with thymoma (n = 15); 2) generalized myasthenia gravis, early-onset (<50 years), without thymoma (n = 45); 3) generalized myasthenia gravis, late-onset ( 50 years), without thymoma (n = 13); 4) ocular myasthenia gravis (n = 9). Treatment results were classified using a simple 4-grade scheme: remission, improvement, no change or deterioration (12) The diagnosis of thymoma was made histologically in all cases. Statistical analysis was performed with the use of standard statistical packages. In order to test hypothesis of statistical difference between means of two variables, Student (t) test was used. P-value of less than 0.05 was considered as statistically significant. Results The distribution of the patients according to age at onset and sex is given in Figure. The disease started before the age of 50 in 74.3% (female to male ratio = 2.8:1). Above the age of 50 the female to male ratio was 1.3:1. Mean age at onset of the disease was 36.4 ± 2.1 years (men 47.1 ± 3.4 years, women 31.7± 2.3 years). The Osserman-Genkins grade at onset I was in 34.1%, IIA in 35.4% and IIB in 30.5% of cases. None of the patients was categorized as being of grade III or IV at onset. The most common first sign was unilateral or bilateral ptosis, followed by ptosis associated with extraocular muscle weakness (diplopia). The disease has started as or has changed during the course to a generalized form in Women 1 <19 < >= Number of cases Number of cases Age (years) Fig. Age at onset (years) and gender of 82 patients with myasthenia gravis

3 Demographic-clinical profile of the patients with Myasthenia gravis 613 Table 1. Associated autoimmune diseases in patients with myasthenia gravis Condition Early onset Late onset (<50 years) ( 50 years) N n Rheumatoid arthritis 1 Hyperthyroidism 6 4 Hypothyroidism 1 Syndromum hipothalamicus 1 Diabetes mellitus 1 Tuberculosis 2 Total of 82 (89.0%) patients. Of 28 patients with pure ocular myasthenia gravis at onset, 19 (67.9%) became generalized later on. A transsternal thymectomy was performed in 54 (65.9%) patients (13 men and 41 women). Histologically a thymoma was present in 15 patients (27.8%) of all operated on (54% men and 20% women). A thymitis was present in 2 patients, and other thymuses showed hyperplasia. The percentage of thymomas in lateonset group ( 50 years) was higher than in the early-onset group (<50 years), 23.5 and 16.4 %, respectively (p < 0.05). In 1 patient a thymoma has been removed before myasthenia gravis became clinically manifest: latent period between thymectomy and disease onset was 6.7 years. Associate autoimmune diseases were present in 16 (19.5%) patients (6 men and 10 women), especially in the early-onset group (Table 1). The most common associate autoimmune disease was hyperthyroidism in 10 patients. The diagnosis of myasthenia gravis was made within 1 year from onset in 90.1%. The diagnosis was delayed for more than 2 years in 7 or 8.6% of the patients. In this cohort the diagnosis was made at a little bit earlier stage in men than in women: within 1 year of onset the diagnosis was made in 92% of men and in 89.3% of women (p > 0.05). It should be noted that in none patients antibodies to AChR were determined. A proserine test was found to be positive in all patients. A repetitive nerve stimulation test (RNS-EMG) was performed in 28 patients: a decrement was found in 11 (39.3%). In total 6 (7.3%) patients died. Two patients were from early-onset group, and four from the late-onset group. The mean duration of the disease until death was 3.7 ± 0.8 years. Thymectomy was performed in 4 patients; a thymoma was confirmed in 3. The main cause of death was myasthenic crisis complicated by pneumonia and pulmonary edema in all cases. All patients were followed from 0.8 to 7.1 years. The mean duration of the follow-up period was 3.58 ± 0.24 years. Table 2 shows the main results of treatment. Remission occurred in 34 (41.5%) patients, 10 of whom were on AChE inhibitors only. The highest percentage (22 out of 34 patients, or 64.7%) of remissions was found in the early-onset group. Thirteen patients (86.7%) from the thymoma group, 20 (44.4%) from the early-onset group, 11 (84.6%) from the late-onset group and 8 (89.9%) from the group with ocular myasthenia gravis made up the population of 52 patients remaining dependent on immunosuppressive drugs at the moment of last visit. At the end of the follow-up period 75 (91.5%) patients were using AChE inhibitors and 68 (82.9%) - prednisolone. Overall, 99% of patients were treated with AChE inhibitors and 92% with prednisolone at some time. Azathioprine was prescribed just for one patient. Discussion Myasthenia gravis has traditionally been regarded as a disorder of young women and older men (3, 13). The incidence of myasthenia gravis is still higher among young women than it is among young men, but recent studies have demonstrated that both sexes now show a bimodal curve for age at onset of myasthenia gravis (2, 3, 14). The first age peak at onset is between 20 and 29 years among women and between 40 and 49 years among men; the second age peak is now the same for both sexes, between 60 and 79 years. Thus, the composition of the series in the present study matched that of reported by others (1, 4, 5). Myasthenia gravis is often associated with other autoimmune diseases among which diseases of thyroid are diagnosed in 3-9.5% of cases (2, 15). In the present study, associated autoimmune diseases were seen in more than one fifth of all patients. Hyperthyroidism was diagnosed in 10 (12.2%) patients with myasthenia gravis. A thymoma was more frequently detected in the lateonset group. These results are also similar to those described by other authors (2, 3, 13). Patients as first sign of the disease most frequently reported unilateral or bilateral ptosis and diplopia. Although we estimated the recall of symptoms by patients as reliable, a certain bias towards

4 614 Daiva Rastenytė, Antanas Vaitkus, Rimas Neverauskas, Valerijus Pauza Table 2. Results of therapy for myasthenia gravis Medication Thymomas Early onset Late onset Ocular Total R I N D R I N D R I N D R I N D Only AchE inhibitors Only prednisolone AchE inhibitors and prednisolone No therapy Total R remission; I improvement; N no change; D deterioration. more prominent signs could be predicted. On the other hand, studies from USA, Holland, Germany, Great Britain and other countries report initial ptosis and diplopia in more than two thirds of patients with myasthenia gravis (3, 7, 11). According to the results of the present study, the diagnosis of myasthenia gravis was made within 1 year from the onset in 90% of patients. That is much better compared to that in other studies. In a study by Beekman R. et al. (2), the diagnosis of myasthenia gravis was delayed even in 26% of all patients by more than 2 years. Similar results were reported in a study from Italy (5). In the present study, in men, the diagnosis of myasthenia gravis was made at a little bit earlier stage than in women (92 and 89 %, respectively). Other authors report similar tendency as well (2, 5). One of the possible explanations, which is also mentioned by foreign authors, could be because in general doctors take women with vague complaints less seriously. As was reported in the literature, the neostigmine/edrophonium test has a relatively high sensitivity (94-100% for generalized and 69-91% for ocular myasthenia gravis) but rather low specificity (15). The test may be false positive in the case of Lambert-Eaton syndrome, amyotrophic lateral sclerosis or in case of cerebral lesion with mass effect (15). In the present study, in all patients, the proserine (neostigmine methylsulfate) test was performed. Serological tests in order to detect antibodies to AChRs protein were not performed for any of the study group patients. According to data of literature, serological test is most sensitive diagnostic test of myasthenia gravis. The sensitivity for generalized myasthenia gravis varies between 89 and 95%, and for ocular - between 50 and 70% (7). RNS-EMG was found to be positive in 39.3% of the 28 patients tested. The reported sensitivities in literature are between 59 and 77% (4, 5). The relatively low sensitivities found in the present study Table 3. Comparison of results Reference R.Mantegazza D.H.Donaldson H.J.G.H. Oosterhuis R. Beekman S.P. Saha Present (5) (4) (8) (2) (16) study Period? Patients (n =) Follow-up (yr.) ? 3.6 Remission 35 % 50 % 37 % 43 %? 41.5 % Died 4 % 0 % 5 % 0 % 9.6 % 7.3 % Thymectomy 72 % 65 % 46 % 56 % 36.9 % 65.9 % Prednisolone 54 % 84 % 28 % 49 %? 80.5 % Azathioprine 18 % 24 % 28 %? 1.2 %

5 Demographic-clinical profile of the patients with Myasthenia gravis 615 were possibly because some patients were on the treatment with AChE inhibitors at the time of the test. In Table 3 the follow-up results of this study are compared with the four others. It is important to notice the difference in length of the follow-up periods and composition of the populations. In the present study the percentage of thymectomies was relatively high. Also, the percentage of patients who received prednisolone was rather high. On the other hand, azathioprine was considerably more frequently prescribed to patients in other series. Mortality in the present study was also comparable with the results of other studies. Prospective design of the study is recommended for the research of chronic non-communicable diseases since it allows to evaluate the course and progression of the disease, effectiveness and sideeffects of the treatment in more precise way. We used retrospective data in this study, therefore the results should be considered keeping in mind the possibility of bias and as the basis of prospective autoimmune myasthenia gravis studies in future. Conclusions 1. More than a half of all patients with myasthenia gravis were female, and almost four fifths fell ill before the age of 50 years. 2. The most common first sign of myasthenia gravis was unilateral or bilateral ptosis and diplopia. 3. The Osserman-Genkins grade at onset was I in 34.1%, IIA in 35.4% and IIB in 30.5% of cases. 4. Among thymectomized patients, the percentage of thymomas in late-onset group ( 50 years) was higher than in the early-onset group (<50 years). 5. Mortality rate was 7.3%. Myasthenic crisis was the main cause of death in all cases. 6. Overall, 99% of patients were treated with acetylcholinesterase inhibitors and 92% with prednisolone at some time. Pharmacological remission was observed in more than 40% of patients. Sergančiųjų Myasthenia gravis demografinės ir klinikinės charakteristikos Daiva Rastenytė, Antanas Vaitkus 1, Rimas Neverauskas 1, Valerijus Pauza 2 Kauno medicinos universiteto Kardiologijos institutas, 1 Kauno medicinos universiteto klinikų Neurologijos skyrius, 2 Kauno medicinos universiteto Neurologijos klinika Raktažodžiai: myasthenia gravis, ankstyvieji požymiai, eiga, gydymas. Santrauka. Darbo tikslas. Išnagrinėti myasthenia gravis sergančių ligonių demografines ir klinikines charakteristikas. Tyrimo medžiaga ir metodai metais Kauno medicinos universiteto klinikų Neurologijos skyriuje gydytų 82 myasthenia gravis sergančių ligonių retrospektyvioji medicininių duomenų analizė. Rezultatai ir išvados. Daugiau kaip pusė ligonių, sergančių myasthenia gravis, buvo moterys, ir beveik keturiems penktadaliams liga pasireiškė iki 50 metų. Dažniausias pirmasis klinikinis myasthenia gravis simptomas vieno ar abiejų vokų ptozė bei dvejinimasis akyse. Ligos pradžioje myasthenia gravis I tipas nustatytas 34,1 proc., IIA 35,4 proc., IIB 30,5 proc. ligonių. Tarp operuotų ligonių, timoma dažniau diagnozuota tiems ligoniams, kuriems myasthenia gravis simptomų pasireiškė sulaukus 50 metų ir vėliau, negu tiems, kurie susirgo iki 50 metų. Analizuotos ligonių grupės mirštamumo rodiklis 7,3 proc. Visų mirusiųjų mirties priežastis buvo miasteninė krizė. Acetilcholinesterazės inhibitoriais buvo gydomi 99 proc., o prednizolonu 92 proc. analizuojamos grupės ligonių. Farmakologinė remisija konstatuota daugiau kaip 40 proc. ligonių. Lėtinių ligų tyrimams rekomenduojama naudoti perspektyvųjį duomenų kaupimo metodą, kadangi galima tiksliau įvertinti ligos eigos bei jos progresavimo ypatumus, gydymo veiksmingumą bei nepageidaujamus poveikius. Šiam darbui naudotas retrospektyvusis duomenų rinkimo būdas, todėl pateikiami duomenys turėtų būti vertinami turint tam tikrą paklaidos tikimybę bei kaip pagrindas planuojant, vykdant perspektyviuosius autoimuninės myasthenia gravis tyrimus. Adresas susirašinėjimui: D.Rastenytė, KMU Kardiologijos institutas, Sukilėlių 17, 3007 Kaunas

6 616 Daiva Rastenytė, Antanas Vaitkus, Rimas Neverauskas, Valerijus Pauza References 1. Somnier FE, Keiding N, Paulson OB. Epidemiology of myasthenia gravis in Denmark. A longitudinal and comprehensive population survey. Arch Neurol 1991;48: Beekman R, Kuks JB, Osterhuis HJGH. Myasthenia gravis: diagnosis and follow-up of 100 consective patients. J Neurol 1997;244: Robertson NP, Deans J, Comspton DAS. Myasthenia gravis: a population based epidemiological study in Cambridgeshire, England. J Neurol Neurosurg Psychiatry 1998;65: Donaldson DH, Ansher M, Horan S, Rutherford RB, Ringel SP. The relationship of age tooutcome in myasthenia gravis. Neurology 1990;40: Mantegazza R, Beghi E, Pareuson P, Antozzi C, Peluchetti D, Sghirlanzoni A, et al. A multicentre follow-up study of 1152 patients with myasthenia gravis in Italy. J Neurol 1990;237: Oosterhuis HJGH. Myasthenia gravis. Edinburgh: Churchill Livingstone; Drachman D.B. Myasthenia gravis. N Engl J Med 1994; 330: Oosterhuis HJGH. The natural course of myasthenia gravis: a long term follow up study. J Neurol Neurosurg Psychiatry 1989;52: Bagdonas E, Vilčinskas A, Lopaitienė D, Gudauskas P, Čikotas P, Petrauskas V, ir kt. Timomų ir miastenijos chirurhinis gydymas.(surgical treatment of thymoma and myasthenia gravis.) Medicina 1999;35(7): Osserman KE, Genkins G. Studies in myasthenia gravis: review of a twenty year experience in over 1200 patients. Mt Sinai J Med 1971;38: Newsom-Davis J. Autoimmunity in neuromuscular disease. Ann NY Acad Sci. 1988;540: Lindner A, Schalke B, Toyka KV. Outcome in juvenileonset myasthenia gravis: a retrospective study with longterm follow-up of 79 patients. J Neurol 1997;244: Aarli JA. Late-onset myasthenia gravis: a changing scene. Arch Neurol 1999;56: Christensen PB, Jensen TS, Tsiropoulos I. Incidence and prevalence of myasthenia gravis in western Denmark: 1975 to Neurology 1993;43: Oosterhuis HJGH. Diagnosis and differential diagnosis. In: Baets MH de, Oosterhuis HJGH, editors. Myasthenia gravis. CRC Press, Boca Raton, 1994, p Saha SP, Mukherjee S, Das SK, Ganguly PK, Roy TN, Maiti B, et al. Clinical profile of myasthenia gravis. J Assoc Physicians India. 1998;46: Received 11 December 2001, accepted 20 May 2002

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