Short-term Effects of Corticosteroid Therapy on Cardiac and Skeletal Muscles in Muscular Dystrophies
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1 ORIGINAL ARTICLE Short-term Effects of Corticosteroid on Cardiac and Skeletal Muscles in Muscular Dystrophies Gehan Hussein, MD,* Lobna Mansour, MD,Þ Hadeer Abdel Ghafar, MD,þ Fatma Alzahraa Mostafa, MD,* and Lubna Fawaz, MDþ Background: Duchenne muscular dystrophy (DMD) is the most common muscular dystrophy of childhood. It leads to progressive deterioration in cardiac and skeletal muscles. Corticosteroids are considered an effective therapy. Objective: This study aimed to evaluate the role of short-term prednisone therapy in improving left ventricular (LV) systolic function, LV mass (LVM), and motor power in cases of muscular dystrophies. Patients and Methods: Twenty-five cases of muscular dystrophy including 17 cases of DMD, 3 cases of Becker muscular dystrophies, and 5 cases of female patients with DMD-like phenotype were included in the study. The diagnosis of 12 patients was confirmed by muscle biopsy with immunohistochemistry; the patients were subjected to motor assessment, measurement of creatine kinase level, and echocardiographic examination before and after prednisone therapy. Transthoracic echocardiographic assessment of the LV systolic function (fractional shortening) was done. Myocardial performance index and LVM were calculated. Intermittent dosage of prednisone was administered 5 mg/kg per day on 2 consecutive days weekly for 3 months. Results: Fractional shortening improved on prednisone therapy (P = 0.009) and LVM increased (P = 0.012); improvement in walking was detected in 77% of the patients, climbing stairs improved in 88.9%, Gower sign improved in 70%, and rising from chair improved in 60%. Prednisone had no effect on the patients with marked motor impairment (on wheelchair). The creatine kinase level was significantly lower after steroid therapy (P = 0.04). Conclusions: Three months of intermittent prednisone therapy could improve cardiac and skeletal muscle function in congenital muscular dystrophy. Key Words: muscular dystrophy, prednisone, left ventricular systolic function, myocardial performance index, left ventricular mass, creatine kinase (J Investig Med 2014;62: 875Y879) Duchenne muscular dystrophy (DMD), an X-linked, recessive disorder with onset before the age of 5 years, is the most common and severe form of childhood muscular dystrophy. 1,2 It is characterized by progressive skeletal muscle weakness leading to loss of ambulation, respiratory failure, and death in the second to third decades of life. 3 Duchenne muscular dystrophy and Becker muscular dystrophy (BMD) are variable From the Departments of *Pediatric Cardiology, and Pediatric Neurology, Faculty of Medicine, Cairo University, Cairo; Department of Pediatric Neurology, Faculty of Medicine, Fayoum University, Giza, Egypt. Received January 19, 2013, and in revised form March 21, Accepted for publication March 24, Reprints: Gehan Hussein, MD, Zahraa El Maadi, Tiba, number 8, flat 107, First Floor, Cairo, Egypt. gehanha@hotmail.com. The authors did not receive funds from any organization to do this work. Copyright * 2014 by The American Federation for Medical Research ISSN: DOI: /01.JIM ce phenotypic expressions of a gene defect at the XP21 site with reduced muscle content of the structure protein dystrophin. 4 Severe childhood autosomal recessive muscular dystrophy is characterized by a severe DMD-like phenotype in both sexes. Most such cases represent >- orf-sarcoglycanopathies. 5 This term has been classified as limb-girdle muscle dystrophy (LGMD). 6 Cardiac involvement in muscular dystrophy has been recognized for decades. Although the extent of involvement varies, cardiac disease is present by 20 years of age in essentially all boys with DMD. 7 The most common cardiac abnormality in DMD is dilated cardiomyopathy. It is usually associated with congestive heart failure, in its symptomatic phase, leading to premature death. 8 Studies on patients with BMD showed that most patients have left ventricular (LV) dilatation, that the severity of LV dysfunction is not related with age, and that all these patients should have echocardiographic assessment for LV function. 9 Cardiac function in muscular dystrophy can be measured by fractional shortening (FS). 10 Currently, there is no cure for DMD. Oral steroids are the only effective long-term therapy. The benefits of prednisone therapy have been advocated for more than 15 years. 10,11 The addition of long-term steroid therapy, using either deflazacort or prednisone, has prolonged ambulation, stabilized pulmonary function, and reduced scoliosis. 12 It also has been suggested that deflazacort has beneficial effects on cardiac function. 13 However, several adverse effects from long-term steroid treatment are predicted to be detrimental to cardiac function including obesity, ventricular hypertrophy, hypertension, and lipid abnormalities. Consensus has been reached regarding the benefits observed with steroid therapy. 10 The Cochrane database mentioned prednisolone therapy for 6 months to 2 years in a dose of 0.75 mg/kg to be the most effective regimen. 14 An alternative dosing schedule for prednisone is 5 mg/kg per day on 2 consecutive days each week. This regimen resulted in a benefit similar to what was seen in controls treated with daily prednisone but with minimum adverse effects. 12 We aimed to determine the extent of involvement in the LV systolic and diastolic functions to assess the effects of shortterm corticosteroid therapy (5 mg/kg per day, twice weekly for 3 months) on the LV systolic and diastolic function as well as on motor power in pediatric cases of muscular dystrophies and to determine the incidence of drug adverse effects in this group of patients. PATIENTS AND METHODS A prospective follow-up study was conducted on 25 patients with muscular dystrophies with age ranging from 3 to 14 years. The study was approved by the hospital research ethics committee. Written consent was taken from the parents. The patients were recruited from the Neuropediatrics Clinic, Pediatric Department, Faculty of Medicine, Cairo University. Journal of Investigative Medicine & Volume 62, Number 6, August
2 Hussein et al Journal of Investigative Medicine & Volume 62, Number 6, August 2014 The conditions of the patients were diagnosed on the basis of clinical criteria, electromyography, nerve conduction velocity, and markedly elevated serum creatine kinase (CK) level. Molecular diagnosis and muscle biopsies with immunohistochemistry were done in 12 patients for dystrophin protein analysis to establish the diagnosis. The patients were assessed clinically and echocardiographically as well as through laboratory test (CK) before and 3 months after steroid therapy. Clinical assessment criteria included anthropometric measurements, assessment of blood pressure, cardiac examination, and neurologic examination including motor assessment with evaluation of the performance of 4 functions (walking, climbing stairs, Gower signs, and rising from chair) as documented by Bonifati et al. 15 in Clinical assessment was done with particular emphasis on the development of corticosteroid adverse effects such as weight gain, development of hypertension, and development of cushingoid appearance. Blood pressure measurement was done using mercury sphygmomanometer with suitable cuff size. Values were plotted into percentiles according to age, sex, and height, and those above the 95th percentile were considered hypertensive. 16,17 Transthoracic echocardiography was done using Hewlett- Packard 5500 Sonos ultrasonic machine phased array sector scanner with the 4- and 8-MHz probes that were used according to age. The linear measurements of the LV cavity were obtained. Left ventricular end-diastolic diameter (LVEDD), LV endsystolic diameter, interventricular septum, and posterior wall were measured. The calculation of FS as an indicator of LV systolic function was done according to the recommendations of the American Society of Echocardiography. 18 Peak velocities of the E wave and delta wave, the ratio of the E wave to the delta wave, and the deceleration time were measured in a standard manner. 19 Isovolumic relaxation time was measured as the time from aortic valve closure to the start of mitral inflow. Myocardial performance index (MPI) was calculated as the ratio of the sum of isovolumic contraction time and relaxation time over the ejection time (ET). 20 The calculation of LV mass (LVM) was done using the following equation 21 : LVMð gþ ¼ 0:80 f1:04 ½ð septal thickness þ LV internal diameter þ posterior wall thicknessþ 3 j ð LV internal diameterþ 3 Šg þ 0:6 g: A dosage of 5 mg/kg per day of oral prednisone on 2 consecutive days (Thursday and Friday) each week for 3 months was used in accordance with the dosing schedule described by Connolly et al. 12 in No cardiac medications were given (diuretics, angiotensin-converting enzyme inhibitors, positive inotrops, or A-blockers). STATISTICAL METHODS All data were entered onto Statistical Package for the Social Sciences version 10 for analysis. Simple frequencies were used for data checking. Descriptive statistics (arithmetic mean and SD) were used for summarizing the quantitative data. Appropriate statistical tests of significance were used to test the null hypothesis in comparing the studied groups. The Student t test was initially used for comparison of means in the studied groups and after stratification by potential confounders. Bivariate correlations were used to study the correlation between quantitative outcome variables and other independent variables in the study. Pearson correlation was used when data were normally distributed, and nonparametric Spearman test was used when data were not normally distributed. A P value of less than 0.05 was used for detecting the statistical significance in all tests. RESULTS The study included 25 patients with muscular dystrophies with a mean age of 7.4 (SD, 2.9) years that ranged between 3 and 14 years; they were 20 boys and 5 girls. Of the 20 boys, 17 were diagnosed with DMD and 3 with BMD. The clinical diagnosis was confirmed by dystrophin deficiency analysis in muscle biopsy in 2 patients with BMD and 7 patients with DMD. All girls were diagnosed with LGMD2C or LGMD2D because of the presence of sarcoglycan deficiency in their muscle biopsy with immunohistochemistry with normal dystrophin content in girls with features identical to DMD. 6 None of the examined patients had clinical signs of heart failure. Table 1 summarizes motor function in the examined patients before and after starting prednisone therapy. prednisone therapy, motor function was improved (Table 1) but had no effect on patients with marked motor impairment (on wheelchair). Blood pressure remained on the normal percentiles. The systolic blood pressure showed no change, whereas the mean diastolic blood pressure was slightly higher; the rise was not statistically significant (P = 0.2). Only 1 patient experienced the adverse effect of steroid therapy in the form of weight gain and cushingoid appearance. His blood pressure remained on the 75th percentile for his age, height, and sex. All girls with LGMD and 1 patient with BMD had normal cardiac function. Age was negatively correlated with FS, but this correlation was not statistically significant (P = 0.18; r = j0.27). There was a positive significant correlation between age and LVEDD (P = 0.04; r = 0.4). Left ventricular systolic function improved on prednisone therapy, and the difference was statistically significant (P = 0.009). It was impaired in 7 patients (5 patients with DMD and 2 patients with BMD) with FS of less than 28% before starting the prednisone therapy. All these patients improved, leaving only 1 patient, despite improvement of his FS from 21% to 25%, to still have an FS of below 28%. Two patients had an MPI of above the upper limits of normal (90.36), 21 which normalized. The CK level decreased significantly (Table 2). The CK level was not correlated to FS (P = 0.9; r = j0.16), or LVEDD (P = 0.6; r = j0.09) or MPI (P = 0.8; r = 0.03). There was no significant correlation between CK and age (P =0.3; r = 0.2). The LVM increased significantly (P = 0.039). DISCUSSION The prolongation of walking is one of the major aims of treatment in cases of muscular dystrophies. 22 Currently, there is no cure for DMD; oral steroids are the only effective therapy that prolong ambulation and delay the need for a wheelchair. 23 It has been known that the deterioration of skeletal muscular function and cardiac function must be carefully monitored in patients with DMD. 24 The normal motor function in some of the patients enrolled in this study before the treatment was caused by the early diagnosis because of screening the family members of clinical cases attending the Neuropediatrics Clinic. Prednisone could stabilize their normal motor functions. This finding was in concordance to the study of Biggar et al. 25 in 2001, who reported that deflazacort could preserve gross motor function. In the current study, prednisone improved motor function in ambulant patients during the period of 3 months, which is a shorter duration of therapy than other studies that used it for 6 months 876 * 2014 The American Federation for Medical Research
3 Journal of Investigative Medicine & Volume 62, Number 6, August 2014 Corticosteroids in Muscle Dystrophy TABLE 1. Motor Function of the Studied Cases and Prednisone Parameter DMD (n = 17) LGMD (n = 5) BMD (n = 3) /Motor Parameter Total Improvement n (%) Walking Normal 3 Stable 2 2 stable 2 2 stable 10 (40) Affected 9 6 improved improved V Improved V V Climbing stairs Normal V V V V 2 V Affected improved 5 5 improved 1 1 improved 16 (64) Gower sign Normal Affected 12 7 improved 5 4 improved 3 3 improved 14 (44) Rising from chair Normal 10 V 2 V 3 V Affected 2 1 improved 3 2 improved V V 3 (12) minimally. 22 Follow-up for our patients is mandatory to determine the duration of persistence of these effects. We found no improvement on motor functions among the patients with marked motor impairment (on wheelchair), which can be explained by the late stage at starting treatment after developing contracture. Our results are in agreement with other investigators who recommended the early use of steroid therapy in ambulant patients with DMD. 26 In the studied cases, the lack of clinical signs of heart failure as exertional symptom could be explained by the fact that motor function was already weak and activity was limited. None of them had dyspnea at rest. The subclinical cardiomyopathy of the 7 (28%) patients with low FS might be presented clinically if their motor power and effort were normal. Our findings are in agreement with what was previously reported: that cardiac symptoms typically appear late in the course of the cardiomyopathy, more often in patients older than 18 years. 27 None of our patients was in this age group, and hospital admission due to cardiac problem was not indicated in any of our patients. The percentage of cases with impaired LV systolic function in our study is similar to what was reported by other investigators 28 and is higher than that of others who reported it to be 16.7%. 29 However, the overall incidence of dilated cardiomyopathy in our study is lower than that of most authors who recorded it in 44% of their cases. 27,30 This wide variation among different reports is mostly caused by a difference in the age of the examined patients. In the current study, the difference is likely caused by earlier referral for cardiac evaluation and younger age group. In the current study, ventricular remodeling was observed after prednisone therapy in the form of decrease in LVEDD and increase in both FS and LVM. Fractional shortening improved in all patients but normalized in 6 patients and remained below normal in 1 (G28%) patient. Those patients did not receive any cardiac medications during the study (angiotensin-converting enzyme inhibitors, diuretics, A-blockers, or cardiac inotrops), indicating that it is a pure effect of prednisone therapy on cardiac muscle. It was mentioned by other investigators that LVM is lower in patients with muscular dystrophy than in the control group. 31 In the current study, a significant increase in LVM after therapy was observed. Although no significant change in blood pressure was detected in the examined patients, this effect was assumed to be related to prednisone. Although this steroid effect was not mentioned previously in the literature, it might be of value in TABLE 2. Laboratory and Echocardiographic Data of the Examined Patients and Prednisone Steroids, Mean (SD) Steroids, Mean (SD) CK, U/L 13,589.6 (14,099.7) 7631 (5587.6) 0.047* LVEDD, mm (6.8) 33 (6.2) 0.001Þ LVESd, mm (6.13) 23.4 (5) FS% 32 (8.6) 36.8 (6.8) E value 0.88 (0.18) 0.86 (0.17) A value 0.64 (0.71) 0.55 (0.12) E/A ratio 1.7 (0.34) 1.6 (0.3) 0.037* EDT (27.6) 87.5 (16.1) AO, mm 18.5 (1.9) 18.9 (3.1) LA, mm (2.75) (3.34) RV, mm (2.82) (3.42) IVS, mm 6.37 (1.4) 6.38 (1.52) LVPW, mm 6.09 (1.37) 7.04 (1.9) LVM, g 88.4 (44.6) (59.8) 0.012* MPI 0.32 (0.17) 0.33 (0.15) 0.03* *Statistically significant. Highly significant. AO indicates aorta; EDT, E deceleration time; IVS, interventricular septum; LA, left atrium; LVESd, LV end-systolic diameter; LVPW, LV posterior wall; RV, right ventricle. P * 2014 The American Federation for Medical Research 877
4 Hussein et al Journal of Investigative Medicine & Volume 62, Number 6, August 2014 improving force of myocardial contractility, and further studies on this effect are needed. There was a significant increase in the FS and a significant reduction in the CK level after prednisone therapy, indicating an improvement in both the LV systolic function and a decrease in skeletal muscle destruction as well. We found that age was negatively correlated to FS. Although this correlation was not statistically significant, it may indicate that the LV systolic function deteriorates with age in cases of muscular dystrophies. This is in agreement with other investigators. 10 Diastolic dysfunction was observed in the current study as evidenced by low E deceleration time (G150 milliseconds). This is coinciding with what was reported in other series. 29,32 Prednisone had no effect on deceleration time as a parameter of impairment of diastolic function in our cases. Myocardial performance index is a well-documented global measure of combined systolic and diastolic function, particularly diastolic function. 21 The index is markedly increased in patients with dilated cardiomyopathy compared with that in healthy subjects. 21 In the current study, 2 of the 7 patients who have systolic dysfunction had an MPI of above the upper limits of normal (90.36), indicating associated diastolic dysfunction. Both patients showed normalization of the MPI after the prednisone therapy. These data support the hypothesis that the progressive decline in cardiac muscle functions can be altered by steroid treatment. 10,13 Only 1 patient in this study showed adverse effects to prednisone therapy in the form of excessive weight gain and cushingoid appearance. Interestingly, this patient did not benefit from the treatment of motor improvement. However, he showed marked improvement in FS. None of our patients developed serious adverse effects that might necessitate discontinuation of the drug. This is a main advantage of the short-term therapy over the long-term therapy, which resulted in major adverse effects in the study of previous investigators who reported cataracts, hypertension, behavioral changes, excessive weight gain, and vertebral fracture used to occur in long-term therapy 33,34 ;inaddition, adverse effects were more evident in short-term regimen of 6 months to 2 years. 22 However, randomized trial proved that weekend dosing of prednisone is equally beneficial to the standard daily dosing with no significant difference in adverse effect profiles between both dosing regimens. 35 The impact of steroid therapy on cardiac function extends beyond the duration of treatment in the course of 6 months. 10 Further studies are needed to assess the duration of the effect of short-term prednisone therapy of 3 months as well as when and how often it is to be repeated. CONCLUSIONS Echocardiographic assessment of the LV systolic function should be done as a routine in cases of muscular dystrophies even in the absence of clinical cardiac manifestations. Intermittent short-term 3-month prednisone therapy improved the LV systolic function and motor function in congenital muscular dystrophy with relatively minimal adverse effects compared with longer duration of therapy in other studies. ACKNOWLEDGMENT The authors thank the patients of the Departments of Pediatric Neurology and Cardiology, Abu El Reesh Hospital, Faculty of Medicine, Cairo University, Egypt. REFERENCES 1. Hoffman EP. Dystrophinopathies. In: Karpati G, Hilton-Jones D, Griggs R, eds. Disorders of Voluntary Muscle. 7th Edition. Cambridge, United Kingdom: Cambridge University Press; 2001:385Y Wong BL, Christopher C. Corticosteroids in Duchenne muscular dystrophy: a reappraisal. J Child Neurol. 2002;17:183Y Boland BJ, Silbert PL, Groover RV, et al. 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Steroid therapy and cardiac function in Duchenne muscular dystrophy. Pediatr Cardiol. 2005;26(6):768Y Hoffman EP, Reeves E, Damsker J, et al. Novel approaches to corticosteroid treatment in Duchenne muscular dystrophy. Phys Med Rehabil Clin N Am. 2012;23(4):821Y Connolly AM, Schierbecker J, Renna R, et al. High dose weekly oral prednisone improves strength in boys with Duchenne muscular dystrophy. Neuromuscul Disord. 2002;12:917Y Silversides CK, Webb GD, Harris VA, et al. Effects of deflazacort on left ventricular function in patients with Duchenne muscular dystrophy. Am J Cardiol. 2003;91:769Y Manzur AY, Kuntzer T, Pike M, et al. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev. 2008;(1):CD Bonifati MD, Ruzza G, Bonometto P, et al. A multicenter, double-blind, randomized trial of deflazacort versus prednisone in Duchenne muscular dystrophy. Muscle Nerve. 2000;23(9):1344Y Park MK, Menard SM. 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5 Journal of Investigative Medicine & Volume 62, Number 6, August 2014 Corticosteroids in Muscle Dystrophy 21. Devereux RB, Alonso DR, Lutas EM, et al. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986;57:450Y Manzur AY, Kuntzer T, Pike M, et al. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev. 2004;(2):CD Fenichel GM, Florence JM, Pestronk A, et al. Long-term benefit from prednisone therapy in Duchenne muscular dystrophy. Neurology. 1991;41(12):1874Y Utsunomiya T, Mori H, Shibuya N, et al. Long-term observation of cardiac function in Duchenne s muscular dystrophy. Evaluation using systolic time intervals and echocardiography. Jpn Heart J. 1990;31(5):585Y Biggar WD, Gingras M, Fehlings DL, et al. Deflazacort treatment of Duchenne muscular dystrophy. J Pediatr. 2001;138(1):45Y Beenakker EA, Fock JM, van Tol MJ, et al. Intermittent prednisone therapy in Duchenne muscular dystrophy: a randomized controlled trial. Arch Neurol. 2005;62:128Y Jefferies JL, Eidem BW, Belmont JW, et al. Genetic predictors and remodeling of dilated cardiomyopathy in muscular dystrophy. Circulation. 2005;112:2799Y Kirchmann C, Kececioglu D, Korinthenberg R, et al. Echocardiographic and electrocardiographic findings of cardiomyopathy in Duchenne and Becker-Kiener muscular dystrophies. Pediatr Cardiol. 2005;26(1):66Y Gulati S, Saxena A, Kumar V, et al. Duchenne muscular dystrophy: prevalence and patterns of cardiac involvement. Indian J Pediatr. 2005;72:389Y Sasaki K, Sakata K, Kachi E, et al. Sequential changes in cardiac structure and function in patients with Duchenne type muscular dystrophy: a two-dimensional echocardiographic study. Am Heart J. 1998;135(6 pt1):937y Cil E, Topalo?lu H, Ca?lar M, et al. Left ventricular structure and function by echocardiography in congenital muscular dystrophy. Brain Dev. 1994;16(4):301Y Brockmeier K, Schmitz L, von Moers A, et al. X-chromosomal (p21) muscular dystrophy and left ventricular diastolic and systolic function. Pediatr Cardiol. 1998;19:139Y Balaban B, Matthews DJ, Clayton GH, et al. Corticosteroid treatment and functional improvement in Duchenne muscular dystrophy: long-term effect. Am J Phys Med Rehabil. 2005;84(11):843Y Ricotti V, Ridout DA, Scott E, et al. Long-term benefits and adverse effects of intermittent versus daily glucocorticoids in boys with Duchenne muscular dystrophy. J Neurol Neurosurg Psychiatry. 2013;84(6):698Y Escolar DM, Hache LP, Clemens PR, et al. Randomized, blinded trial of weekend vs daily prednisone in Duchenne muscular dystrophy. Neurology. 2011;77(5):444Y452. * 2014 The American Federation for Medical Research 879
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