Correlation of Electromyogram and Muscle Biopsy in Myopathy of Young Age

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1 780 ORIGINAL ARTICLE Correlation of and Muscle Biopsy in of Young Age Jihoon Chang, MD, Yoon Ghil Park, MD, PhD, Young-chul Choi, MD, PhD, Jung Hwa Choi, MD, Jae Ho Moon, MD ABSTRACT. Chang JH, Park YG, Choi YC, Choi JH, Moon JH. Correlation of electromyogram and muscle biopsy in myopathy of young age. Arch Phys Med Rehabil 2011;92: Objective: To investigate the accuracy of electromyogram (EMG) compared to muscle biopsy in young myopathic patients. Design: Observational study. Setting: A university rehabilitation hospital. Participants: Cases (N 62) were included if the patient was 18 years or younger, and if data were available from muscle biopsy, EMG, and final clinical diagnosis. Intervention: No intervention. Main Outcome Measure: Sensitivity of EMG. Results: EMG showed myopathic findings in 55 patients, and microscopy revealed myopathy in 50 patients and nonspecific findings in 5 patients. Twenty-eight out of 33 patients showed myogenic EMG findings with a conventional EMG, and histology revealed myopathy in 24 patients. In comparison, turns/amplitude analysis (TAA) with a conventional EMG detected myogenic findings in 27 of 29 patients. Twenty-six of these 27 patients showed myogenic findings in the biopsy. Conclusions: We concluded that EMG is useful for the detection of myopathy in young patients. In addition, TAA may be helpful in cases of no definite conventional EMG findings and less cooperative patients. Key Words: Biopsy; Electromyography; Muscles; Neuromuscular diseases; Rehabilitation by the American Congress of Rehabilitation Medicine INTERVIEWS, PHYSICAL examinations, genetic tests, electrodiagnosis, and muscle tissue biopsies are all used to diagnose neuromuscular diseases. Confirmative diagnoses are typically made based on a combination of various test results. Muscle tissue biopsy has the disadvantage of being an invasive procedure when compared to genetic testing and EMG. Genetic testing and muscle tissue biopsies cannot determine which muscles are affected or obtain information regarding the progression of the disease. Prior to muscle tissue biopsy, the degree and distribution of muscle disease can be examined through evaluation of motor units. 1-3 From the Department of Rehabilitation Medicine and Rehabilitation Institute of Muscular Disease (Chang, Park, JH Choi, Moon) and Department of Neurology (YC Choi), Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Correspondence to Yoon Ghil Park, MD, PhD, Department of Rehabilitation Medicine and Rehabilitation Institute of Muscular Disease, Gangnam Severance Hospital, Yonsei University College of Medicine, 712, Eonjuro, Gangnam-gu, Seoul, South Korea, Zip code: , drtlc@yuhs.ac /11/ $36.00/0 doi: /j.apmr Electrodiagnosis of muscle disease is typically difficult in young patients. Special attention is required when diagnosing children due to the immaturity of the nervous system, technical errors due to the small size of the subjects, insufficiency of reference data regarding pediatric cases, and poor cooperation regarding muscle relaxation and gradual contraction. 4 The concordance rate between electrodiagnostic results and final diagnosis is generally low in young patients. Accuracy is also lower in children who have muscular diseases compared to those who have neurologic disorders. 5 In previous studies evaluating floppy infants, the concomitant use of needle EMG with neuromuscular conduction tests was helpful for differentiating a central from peripheral nervous system abnormalities. It was also useful for ruling out the possibility of neurogenic disorder. 6 Primary use of electrodiagnosis would be helpful in pediatric patients who are suspected of having neuromuscular disease or floppy infant syndrome. Interference pattern analysis is helpful for diagnosis of myopathy. However, in patients who cannot collaborate, such as children for contracting muscle at minimal degrees, we hardly acquire enough data for analysis of interference pattern. Quantitative analysis of the interference pattern based on needle EMG is used as the diagnostic method for neuromuscular disease because it can be easily performed in patients who do not collaborate well when compared with a conventional analysis of the motor unit action potential. 7 TAA, one of the quantitative analysis of interference pattern analysis, reflects the motor units which are induced in an entire range of force. 8 This is useful for assessing muscle activity, muscle fatigue, chronic myalgia, and abnormal muscle contractions after botulinum toxin injections. Errors between the tester and the laboratory can be minimized, and differences in results based on disease evolution in the same patient can also be determined with TAA. 7,8 TAA has been reported to be useful for diagnosis of various myopathy. 9,10 In this study, data from young patients, including infants, who underwent both muscle tissue biopsy and electrodiagnostic testing, were analyzed in order to determine the accuracy and usefulness of electrodiagnostic tests. We believed that an additional TAA might be useful for electrodiagnostic study in young patients with poor compliance. By comparing conventional and quantitative EMG, we were able to assess the accuracy of TAA and determine whether or not it was useful for making a diagnosis. CI DMD EMG MLPA TAA List of Abbreviations confidence interval Duchenne muscular dystrophy electromyogram multiplex ligation-dependent probe amplification turns/amplitude analysis

2 ELECTROMYOGRAM AND BIOPSY IN MYOPATHY, Chang 781 METHODS This study was reviewed and approved by the Institutional of Gangnam Severance Hospital, Yonsei University College of Medicine. Participants During the period ranging from 2002 to 2009, 62 young patients ( 18y old) who were suspected of having myopathy underwent muscle tissue biopsy and EMG at Gangnam Severance Hospital, Seoul, South Korea. Those patients who were found to have neurogenic disorders, muscular dystrophy, inflammatory myositis, and no specific neuromuscular disorders were enrolled in this study. Only subjects with normative nerve conduction studies were included, and needle EMG was a necessity for diagnosis. The patients included 15 girls and 47 boys (age range, 1mo 18y). TAA was only added to the conventional EMG evaluation since 2006, as a result, there was no TAA data for patients who visited from 2002 to EMGs were performed on all patients with suspected myopathy before the muscle biopsy. All EMG tests were performed by a physician and a physiatrist, who is a member of the American Board of Electrodiagnostic Medicine and have more than 10 years of experience conducting EMGs, and they were not aware of the final diagnosis. In all cases, EMG was performed before the muscle biopsy. The EMG equipment that was used for the evaluation of all enrolled patients was made by MedelecSynergy. a Nerve conduction studies included at least 2 sensory nerves and 2 motor nerves in the upper extremities, and 1 sensory nerve and 1 motor nerve in the lower extremities. The amplitude, latency, and conduction velocity of the compound muscle action potential and sensory nerve action potential were recorded. These were compared to a standard table of reference values in our EMG laboratory. The subjects showed nerve conduction parameters within the reference value. The disposable monopolar needle electrodes of Teca-Needles were used. a Needle EMG was performed in muscles in both the upper and lower extremities, selecting preferentially those with mild to moderate clinical weakness. When TAA was performed, the concept of a cloud was used. 11 The disposable monopolar needle electrodes of TecaNeedles a were used. EMG was performed in muscles in both the upper and lower extremities, selecting preferentially those with mild to moderate clinical weakness. When TAA was performed, the concept of a cloud was used. 11 The range of the filtering frequency was set at 10Hz for the low-frequency filter and 10KHz for the high-frequency filter. The sweep duration was 500 milliseconds. The patterns of muscle contractions in the biceps brachii and tibialis anterior were observed and analyzed for the quantitative analysis of the interference pattern. Muscle contraction was gradually increased in a stepwise manner and the induced interference pattern was obtained. The interference pattern was obtained at least 20 times in each muscle. The resting period was set at several seconds in order to reduce fatigue between contractions. 12 In order to vary the location of the needle and to prevent overlapping interference, we advanced the EMG needle from anterior to posterior or from left to right to give a minimal displacement of more than 5mm. The test was performed in 3 to 5 sites per muscle. 13 Turns per second versus mean amplitude are plotted during 3 to 5 steps of gradual muscle contraction on multiple sites of a tested muscle. Based on the EMG, patients were divided into 3 groups: the myopathy group, the neurogenic disorder group, and the nonspecific group. There are several needle EMG criteria for myopathy. 1,5,14 In this study, myopathy was defined as a needle study showing: short duration, polyphasic, low-amplitude motor unit potentials, usually early appearance of maximum interference pattern in weak muscles, and normal or abnormal spontaneous activity. 5 A disorder of myopathic origin on TAA was defined as more than 10% of the plots of turns per second versus the mean amplitude being located downward from the reference cloud after more than 20 plots. 11 A neurogenic disorder was defined as the presence of abnormal spontaneous potential during the resting phase and high amplitude polyphasic motor unit potential with a long duration. A disorder of neuropathic origin on TAA was defined as more than 10% of the plots of the turns per second versus the mean amplitude being located upward from the reference cloud after more than 20 plots. cases were defined as having no specific EMG or radiculopathy findings, and cases with a definite diagnosis was impossible. In order to establish reference values for the cloud, we used the methods described by Stålberg et al. 11 We measured conversion point, amplitude, activity, limit frequency, and the number of phases. The tests were performed on the biceps brachii and tibialis anterior of healthy people at our EMG laboratory. 15 Furthermore, in order to examine the accuracy of additional TAA, a comparison was made between a conventional EMG (needle EMG with nerve conduction study) and a TAA (TAA with conventional EMG). A conventional EMG was defined as a needle EMG with a nerve conduction study but no additional TAA. Muscle Biopsy and Gene Analysis Open muscle biopsies were performed by an orthopedic surgeon at Gangnam Severance Hospital on a muscle showing signs of weakness and abnormal EMG findings. Muscle biopsy samples were interpreted by 2 pathologists and a neurologist. The results were then classified into 3 groups; the myopathy group, the neurogenic disorder group, and the nonspecific group. Muscle specimens were stained with hematoxylin-eosin, periodic acid-schiff, trichrome, reduced form of nicotinamideadenine dinucleotide, and adenosine triphosphatases (ph 9.4, 4.6, 4.2). Genetic tests were performed using polymerase chain reaction or MLPA. For genetic analysis prior to April 2007, polymerase chain reaction was used for the dystrophin gene test. After April of 2007, MLPA methods were used for gene analysis. MLPA is a new technique for the detection of deletions and/or duplications in various genetic diseases. 16 Statistical Analysis A statistical analysis of the data was performed using SPSS 12.0 for Windows. b A Fisher exact test was used to verify the differences in sensitivity, depending on the differences of test methods between the conventional group and the TAA group. Statistical significance was set at P less than.05. RESULTS A muscle tissue biopsy and an EMG were performed on a total of 62 patients. The ages of enrolled patients ranged from 1 month to 18 years. The diagnoses of enrolled patients included DMD, Becker muscular dystrophy, congenital myopathy, and dermatomyositis. All nerve conduction velocities of 62 patients were within reference values which were adjusted to their ages.

3 782 ELECTROMYOGRAM AND BIOPSY IN MYOPATHY, Chang Table 1: Patient Characteristics and Diagnostic Information No. Age C-EMG TAA Biopsy 1 1mo N NT N 2 8mo NS NT NS 3 9mo M M M 4 14mo M NT M 5 17mo M M M 6 28mo M NT M 7 29mo M NT M 8 29mo M NT M 9 31mo M M M 10 4 M NT NS 11 4 M NT M 12 4 M M M 13 4 M NT M 14 5 M NT M 15 5 NS M M 16 5 M NT M 17 5 M NT M 18 5 M M M 19 5 M NT M 20 5 M NT M 21 6 NS M M 22 6 M NT M 23 6 NS M M 24 6 M NT M 25 6 M NT M 26 6 M NT NS 27 6 M M M 28 6 M M M 29 6 N N N 30 7 M NT M 31 7 M NT M 32 7 M NT M 33 7 M NT M 34 7 M NT M 35 8 M M M 36 8 M NT M 37 8 M M M 38 9 NS NT N 39 9 M M M 40 9 M NT M 41 9 M M M 42 9 M M M 43 9 M M M NS M M M NT M M M M M M NS M M M M M M M NT NS M M M M M M M NS NS M NT M M M M M NT NS NS NT M M M M M M M M M M M NT M NS NT NS NOTE. Age is in years or as otherwise noted. Abbreviations: C-EMG, conventional EMG; M, myogenic type; N, neurogenic type; NS, not specific; NT, not tested. Fifty-five of the 62 patients who underwent EMG had findings suggestive of myopathy (table 1). Two patients had findings suggestive of neurogenic disorders. Five patients did not have findings of either myopathy or neurogenic disorders (table 2). Fifty of the 55 patients who had findings suggestive of myopathy on the EMG were diagnosed with myopathy based Table 2: Comparison of EMG and on a muscle tissue biopsy. There were no notable findings on a tissue biopsy in the other 5 patients. One of the 5 patients who had no notable findings on the EMG was diagnosed with myopathy based on a tissue biopsy. One was diagnosed with a neurogenic disorder, and 3 showed nonspecific findings from the tissue biopsy. Twenty-seven of the 51 patients who were diagnosed with a myopathy were found to have DMD. One had Becker muscular dystrophy; 9 patients had a congenital muscular dystrophy; 4 patients had dermatomyositis; 6 patients had limb-girdle muscular dystrophy; and 4 patients had an unidentified muscle disease. There were 3 patients with a neurogenic disorder, and 8 patients with nonspecific findings based on the muscle tissue biopsy. The sensitivity of EMG for the diagnosis of muscle disease were found to be 98% (50 out of 51; 95% CI, ). A total of 33 patients underwent only conventional EMG, which included needle EMG. Based on these results, 28 patients had myopathy, 1 had a neurogenic disorder, and 4 patients had nonspecific findings (table 3). Twenty-four of the 28 patients who had myopathy according to the conventional EMG were diagnosed based on a tissue biopsy. However, 4 patients had no abnormal findings on the tissue biopsy. When a conventional EMG was used to diagnose a myogenic disorder, the sensitivity was 96% (24 out of 25; 95% CI, ). A total of 29 patients were given an additional TAA. The results of the TAA were marked with cloud. Twenty-seven patients were found to have myopathy; 1 patient had a neurogenic disorder; and 1 patient had nonspecific findings (table 4). Twenty-six of the 27 patients with myopathy were also diagnosed based on a tissue biopsy. One had no abnormal findings on the tissue biopsy. In the patients who had an additional TAA to diagnose muscle disease, the sensitivity was 100% (26 out of 26; 95% CI, ). There were no significant difference in the sensitivity (P.49) between the conventional EMG and TAA groups. In regards to the TAA, there were 4 patients (aged 49, 61, 65, and 113mo) whose conventional EMG did not show any abnormal spontaneous activities, even in muscle resting phase. In these patients, myopathic findings were revealed through TAA. Based on the tissue biopsies and clinical manifestations, 4 patients were diagnosed with a myopathy. Three of these patients were diagnosed with DMD, and 1 patient was diag- Table 3: Comparison of Conventional and Final Diagnosis Classical (N 62) (n 33) (n 51) (n 25) (n 3) (n 2) (n 8) Myogenic disorder Neurogenic disorder (n 6) Myogenic disorder Neurogenic disorder

4 ELECTROMYOGRAM AND BIOPSY IN MYOPATHY, Chang 783 Table 4: Comparison of TAA and Quantitative Electromyography (n 29) (n 26) (n 1) (n 2) Myogenic disorder Neurogenic disorder nosed with limb-girdle muscular dystrophy. One child with myopathic findings on the conventional EMG was diagnosed as not myopathic after TAA. The child was 151 months old, and conventional EMG showed some polyphasic short amplitude motor units and a few denervation potentials. However, the additional TAA and muscle biopsy result were normal. DISCUSSION In this study, EMG and muscle biopsy were performed in young patients who were clinically suspected to have a muscle disease. A comparison was made between the conventional EMG group and additional TAA group to confirm whether the successful diagnostic rate of additional TAA group for muscle diseases would rise. In a few patients with myopathy on biopsy, the only EMG abnormality was seen in the TAA, but the overall sensitivity of EMG was not improved by the addition of TAA to qualitative EMG assessment with this sample size. Nineteen of 27 patients with DMD as final diagnosis had genetic study data from our hospital. In these records, 10 patients had DMD gene abnormality, and 9 patients had without DMD gene abnormality. In this study, 7 patients were found with a discrepancy between the EMG findings and the results of the tissue biopsy. Two of these patients had nonspecific EMG findings: 1 was ultimately diagnosed with a congenital myopathy based on a muscle biopsy and the other was diagnosed with neurogenic disorder. Five patients who had findings suggestive of myopathy on an EMG showed nonspecific biopsy findings. The mean age of the patient group in which the EMG findings and the results of a tissue biopsy were congruent was 87 months (median, 74mo). In mean age of the 7 patients who had no consistency between the EMG findings and the results of a tissue biopsy was 118 months. The ages of these 7 patients were 37, 68, 97, 140, 151, 165, and 167 months. Due to the technical difficulties of performing an EMG in young patients, it was expected that the mean age would be lower in the group without consistency between the EMG findings and the results of a muscle biopsy. An analysis of the interference pattern based on TAA reflects the motor unit that was induced by all degrees of the forces. This means that we were able to record signals formed by the involvement of action potential of all types of motor units. Patient compliance is a relatively less important factor for TAA than for traditional interference pattern analysis. Signals can be obtained faster and the data can also be processed faster. This can be helpful for young patients in whom there was insufficient extent of cooperation and a small magnitude of force could not be induced. The electrical activity of a muscle contraction should be analyzed while the subject is contracting the muscle. This is especially important in patients who have impaired cognition or paralysis and show poor compliance during an EMG, or those who were unable to exhibit gradual muscle contractions. There are limitations to the classical analysis of the motor unit and interference patterns. 15 In this study, TAA was helpful in 5 patients. In 4 patients who we could not conclude myopathy with conventional EMG, TAA showed myopathic findings. TAA also helped us to conclude normative status in 1 patient. In 2 of the previouslymentioned 4 patients, lack of cooperation made analysis of the motor unit difficult. In the other 2, abnormal EMG findings could not be detected when we used a conventional EMG alone. After the additional use of a TAA, the results of an EMG analysis corresponded to a myopathy. Unlike previous studies, we included data about DMD and Becker type dystrophy and gave helpful information about EMG of DMD. 5 The patients of the previous study had congenital myopathies (n 5, 18%), nonspecific myopathies (n 6, 22%), congenital myasthenic syndrome (n 3, 11%), juvenile myasthenia gravis (n 1, 4%), arthrogryposis multiplex congenita (n 2, 7%), hereditary motor and sensory neuropathy (n 1, 4%), bilateral peroneal motor neuropathies (n 1, 4%), and were healthy (n 8, 30%). Study Limitations There were a number of study limitations, some of which have already been noted. Our sample size of 62 subjects was small, and the data were from a single muscular disease center, so our results should be generalized with caution. Because the above data was collected from a muscular disease center at a university hospital that also has a pulmonary rehabilitation center for muscular disease, the proportion of patients with severe forms of muscular disease, such as DMD, was high. There was the problem of selection bias. We also noted the technical problems. We tried to induce 3 children ( 3y old) to contract their muscles in different force levels with the use of an external stimulation. However, gradual muscle contractions were not completely successful. The monopolar needle electrodes have a slightly larger surface area than concentric needle electrodes, and thus the amplitude of the motor unit appears larger and a borderline myopathy may be missed. No control group data of healthy young patients were available. Although our analysis provided some accuracy analysis of EMG and TAA, this was a retrospective study, and the participants were not recruited randomly. Future research is needed to address these limitations. CONCLUSIONS In this study, there was more consistency between EMG findings and muscle tissue biopsy when diagnosing myopathy when compared to previous reports. 5,17 In Korea, there had been no previous studies comparing EMG findings and tissue biopsies. An EMG is a test that is expected to accurately diagnose muscle disease. However, successful administration of EMG tests requires patient cooperation. A TAA could be helpful for making a diagnosis of a muscle disease in pediatric patients whose cooperation is poor or in patients with equivocal needle EMG findings. Future studies about TAA and myopathy in a larger patient population may determine the usefulness of TAA in diagnosis of myopathy. References 1. Buchthal F. Electromyography in the evaluation of muscle diseases. Neurol Clin 1985;3: Dumitru D, Amato AA. Introduction to myopathies and muscle tissue s reaction to injury. In: Dumitru D, Amato AA, Zwarts MJ, editors. Electrodiagnostic medicine. 2nd ed. Philadelphia: Hanley & Belfus; p Wilbourn AJ. The electrodiagnostic examination with myopathies. J Clin Neurophysiol 1993;10:

5 784 ELECTROMYOGRAM AND BIOPSY IN MYOPATHY, Chang 4. Kerman K, Shahani B. Pediatric electromyography. Indian J Pediatr 1990;57: Rabie M, Jossiphov J, Nevo Y. Electromyography (EMG) accuracy compared to muscle biopsy in childhood. J Child Neurol 2007;22: Darras BT, Jones HR. Diagnosis of pediatric neuromuscular disorders in the era of DNA analysis. Pediatr Neurol 2000;23: Ryu HH, Park YG, Moon JH, Ryu JS, Lee YJ. Comparison of interference pattern between normal and myopathy group used by quantitative EMG. J Korean EMG Eletrodiag 2007;3: Fuglsang-Frederiksen A. The utility of interference pattern analysis. Muscle Nerve 2000;23: Puvanendran K, Cheah JS, Naganathan N, Wong PK. Thyrotoxic myopathy: a clinical and quantitative analytic electromyographic study. J Neurol Sci 1979;42: Fuglsang-Frederiksen A. The role of different EMG methods in evaluating myopathy. Clin Neurophysiol 2006;117: Stålberg E, Chu J, Bril V, Nandedkar S, Stålberg S, Ericsson M. Automatic analysis of the EMG interference pattern. Electroencephalogr Clin Neurophysiol 1983;56: Garcia HA, Milner-Brown HS, Fisher MA. Turns analysis in the physiological evaluation of neuromuscular disorders. J Neurol Neurosurg Psychiatry 1980;43: Nirkko AC, Rosler KM, Hess CW. Sensitivity and specificity of needle electromyography: a prospective study comparing automated interference pattern analysis with single motor unit potential analysis. Electroencephalogr Clin Neurophysiol 1995;97: Dumitru D, Amato AA. The electrodiagnostic medicine consultation. In: Dumitru D, Amato AA, Zwarts MJ, editors. Electrodiagnostic medicine. 2nd ed. Philadelphia: Hanley & Belfus; p Park KD, Lee SC, Park YG, Moon JH. Analysis of interference pattern of quantitative electromyography in early adolescence. J Korean Acad Rehab Med 2007;31: Sellner LN, Taylor GR. MLPA and MAPH: new techniques for detection of gene deletions. Hum Mutat 2004;23: Blijham PJ, Hengstman GJ, Ter Laak HJ, Van Engelen BG, Zwarts MJ. Muscle-fiber conduction velocity and electromyography as diagnostic tools in patients with suspected inflammatory myopathy: a prospective study. Muscle Nerve 2004;29: Suppliers a. Viasys Healthcare, Manor Way, Old Woking, Surrey, GU22 9JU, UK. b. SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL

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