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International neurological journal 2 (88) 2017

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Imaging methods in Duchenne muscular dystrophy (literature review)

Authors: D.I. Rudenko, A.V. Pozdnyakov, V.M. Suslov
State Budget Institution of Higher Professional Education “Saint-Petersburg State Pediatric Medical University” Ministry of Health of the Russian Federation, Saint-Petersburg, Russia

Categories: Neurology

Sections: Specialist manual

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Дана стаття присвячена літературному огляду методів візуалізації скелетних м’язів при м’язовій дистрофії Дюшенна. Проведено аналіз як історично значущих наукових робіт, так і останніх досягнень в галузі нейровізуалізації. У статті розглянуто такі методи, як ультразвукова діагностика, комп’ютерна та магнітно-резонансна томографія скелетних м’язів, а також магнітно-резонансна спектроскопія. Відзначено і обґрунтовано актуальність і перспективність неінвазивних, безпечних і об’єктивних методів оцінки скелетних м’язів при м’язовій дистрофії Дюшенна.

Данная статья посвящена литературному обзору методов визуализации скелетных мышц при мышечной дистрофии Дюшенна. Проведен анализ как исторически значимых научных работ, так и последних достижений в области нейровизуализации. В статье рассмотрены такие методы, как ультразвуковая диагностика, компьютерная и магнитно-резонансная томография скелетных мышц, а также магнитно-резонансная спектроскопия. Отмечены и обоснованы актуальность и перспективность неинвазивных, безопасных и объективных методов оценки скелетных мышц при мышечной дистрофии Дюшенна.

This article presents a literary review of the methods for imaging skeletal muscles in Duchenne muscular dystrophy. The analysis of both historically significant scientific works and recent achievements in the field of neuroimaging was carried out. The article considers such methods as ultrasound diagnostic, computedand magnetic resonance tomography of skeletal muscles, as well as magnetic resonance spectroscopy. The urgency and perspective of non-invasive, safe and objective methods for evaluating skeletal muscles in Duchenne muscular dystrophy were identified and substantiated.


м’язова дистрофія Дюшенна; скелетні м’язи; магнітно-резонансна спектроскопія; магнітно-резонансна томографія; комп’ютерна томографія; ультразвукова діагностика; біомаркери

мышечная дистрофия Дюшенна; скелетные мышцы; магнитно-резонансная спектроскопия; магнитно-резонансная томография; компьютерная томография; ультразвуковая диагностика; биомаркеры

Duchenne muscular dystrophy; skeletal muscle; magnetic resonance spectroscopy; magnetic resonance imaging; computer tomography; ultrasound diagnostics; biomarkers

Duchenne muscular dystrophy (DMD) — one of the most frequent form of childhood muscular dystrophy. Inheritance — autosomal recessive, linked to the X chromosome. The frequency of disease is 3 to 10 thousand newborn boys. The disease was first described by French scientist Duchenne in 1868.
The first symptoms appear between the ages of 2–5 years, beginning with atrophy and weakness of the muscles of the pelvic girdle and thighs. Because of the involvement of the muscles of the pelvic girdle and torso lumbar hyperlordosis arises. There are a violation of gait, frequent falls, difficulty in climbing stairs. The patient can’t get up from a sitting position on his heels without hands (Gowers’ sign). 
Also patients having hypertrophy. Most often they occur in the calf muscles, but can also involve the deltoid, gluteal, chewing muscles and the muscles of the tongue. The weakness of the extensor and hip flexion contractures in the hip and knee joints leads to compensatory hip abduction, building installation equinovarus feet, while moving the patient comes to the outer edge of the foot.
Subsequently formed joint contractures. Over time, there is a weakness and atrophy of the muscles of the shoulder girdle with the development of scapular winging and difficulty lifting hands up. There flattening of the chest in the anteroposterior direction. Also there is a weakness of facial muscles.
Bulbar muscles usually are not affected. In 30–50 % of cases there is dementia, which is associated with a deficiency of dystrophin in brain. It is often diagnosed disorders of the cardiovascular system, manifested in the form of a sinus tachycardia or fibrillation, pacemaker migration, possible congestive heart failure in the later stages of the disease.
In the biochemical analysis of blood is a high evaluation of CK levels. Duchenne muscular dystrophy is a severe disabling disease by the age of 12, patients lose the ability to move independently. Over time, developing cardiac and pulmonary insufficiency, joining secondary infection, which is one of the main causes of deaths.
Evaluation of physical muscle strength through a variety of physical methods and the scale has several disadvantages. The first is the inability to reliably assess the condition of each muscle separately. Especially difficult is in childhood, as well as in the later stages of the disease. The question of the muscle imaging has been raised in the last century and remains relevant to this day. The most popular methods are: ultrasound, CT and MRI, as well as magnetic resonance spectroscopy.
US skeletal muscle was first introduced in 1968 and Ikai Fukunaga, who appreciated the thickness and cross-section of muscle. Later, Kramer, Yong et al. [9] conducted the first examination of the patient with muscle disease. Using ultrasound muscles in the evaluation of neuromuscular diseases started to gain interest by 1980 (Heckmatt, Dubowitz and Leeman, 1980 [6]; Heckmatt, Leeman and Dubowitz, 1982) [7]. This method is still used in the clinic to identify muscle damage (Mercuri et al., 2007) [12] and to assist in the selection of the muscle biopsy. However, the usefulness of ultrasound in skeletal muscle is limited by the fact that for this technique requires special training of specialists and not all muscles can be adequately assessed. 
In the history of the study of Duchenne muscular dystrophy is important to highlight the work of Japanese scientists H. Aizawa, S. Kozima et al., рublished in the journal Rinsho Shinkeigaku (1989) [1], the work on the application of the method of ultrasound diagnostics in assessing the state of the muscle tissue. 30 children with DMD were taken, as well as 16 people in the control group. Each patient was evaluated quadriceps muscle, the gastrocnemius and soleus muscles. According to the study, the control group themselves skeletal muscles were barely echogenic. However, the surface of the bone and fascia were clearly echogenic. Transverse scan of all the muscles in DMD patients showed increased echogenicity, making bones image or fascia less intense. Evaluation was carried out by Heckmatt criteria. There was a significant correlation between the disability of patients with DMD and abnormal echogenicity quadriceps. A similar correlation was also observed between the clinical evaluation of muscle strength and ultrasonic imaging. In the soleus is usually observed less variation than in the calf during ultrasonic imaging. This study helped to better understand the diagnostic value of ultrasonography in neuromuscular diseases.
Considering the research of our day, it should be noted the work of Craig M. Zaidman, Anne M. Connolly et al. [5]. In 2010 they published in the journal Neuromuscular disorders article on the calibrated muscle backscatter (CMB). In this work, the method aims to visualize and quantify changes in muscle tissue in Duchenne and Becker muscular dystrophy. The study involved 55 patients with a confirmed diagnosis, as well as taken control group of 77 people. The age range of patients with DMD — 9 months up to 19 years, and patients with BMD — from 1 year to 47 years. As the data were compared with the strength of the muscles and their functionality.
As a result of CMB research biceps muscle, as well as in the rectus femoris (in patients with DMD) in different groups with DMD, BMD and the control group. The difference from the control group is determined by the majority of boys with DMD to 5 years of age and becomes an expression, reaching a peak in adolescence. At the same age have difficulties in assessing the strength and functionality of muscles in patients with DMD. While the CMB is possible to evaluate objectively and without patient effort. This makes it possible to use this method as a clinical marker in children who, due to increasing weakness and rapid progression of the disease, it is impossible to reliably estimate the strength of muscles in any other way.
Two years later, in 2012, M. Jansen, N. Alfen et al. [10] conducted a study published later in the same journal. Their work has been focused on a quantitative ultrasound of skeletal muscle in DMD. It spends long study in the dynamics of the muscles of the upper and lower limbs in 18 patients. Also the results of 11 patients were compared with the data of the clinical assessment of muscular strength. The study was noted in all patients, a significant increase in signal intensity, which indicates the degree of damage to dystrophic muscle tissue as the disease progresses. The same results were correlated with muscular strength of patients and their mobility. On the basis of the study it can be concluded that quantitative ultrasound skeletal muscle — it is fast (takes less than 20 minutes), reliable and gentle to the child a tool to carry out observation in dynamics.
In the same year a similar research presented Chinese colleagues Shi Yr, Liu Xq et al. [16]. They published article in the Chinese Journal of Contemporary Pediatrics their task was to develop and identify opportunities of high-frequency ultrasound in the evaluation of skeletal muscle in DMD children. For the study were selected rectus femoris, gastrocnemius and soleus muscles were examined 8 children with Duchenne muscular dystrophy, is taken for comparison control group of 10 healthy children. The study muscle in children with DMD showed increased echogenicity as compared with the control group. This study confirm the diagnostic value of high frequency ultrasound imaging of skeletal muscle in DMD.
Considering the relatively recent studies, it should be noted the work C.M. Zaidman, E.C. Malkus, A.M. Connolly [18]. Published in 2015 in the journal «Muscle & Nerve» study focuses on the application of the method of quantitative ultrasound in the diagnosis of skeletal muscles of DMD. A total of 5 boys diagnosed with DMD between the ages of 5 months to 2.8 years. Applies an inverse scattering method of muscle, showing the intensity of the echo signal indicators. Then the results were compared with the clinical evaluation of muscle strength and ultrasound data in the control group of muscles (0,6–3,1 s) taken from a cross-sectional study. As a result, all patients with increase in signal intensity was observed over time.
Another work, published in the journal «Muscle & Nerve», was done by I. Shklyar, T.R. Geisbush, A.S. Mijialovich [8].
The aim of the work was to compare the two methods. They used quantitative backscatter analysis (QBA), which the intensity of the echo signal is determined by the amplitude of the acoustic energy is reflected back from the tissue to the ultrasonic transducer. In the future, the received data compress in 256 levels of grayscale (GSL).The authors compared the QBA and GSL in 25 boys with DMD and 25 healthy children aged from 2 to 14 years. Also was revealed a correlation with the NSAA scale (North Star Ambulatory Assessment). For this research were taken mm. deltoideus, biceps brachii, flexor digitorum, quadriceps femoris, tibialis and medial head of the gastrocnemius.
Results: performance QBA and GSL were raised in DMD in the surface areas of the muscles. Quadriceps femoris characterized greatest intensity of the echo signal than any other muscles (QBA: p < 0.05, GSL: р < 0.03), except in the medial gastrocnemius muscle in the QBA (р = 0.06). Even the youngest group with DMD (age 8 or younger, n = 16), the findings are still valid.
Performance of GSL and QBA during the examination of the majority of muscles increased with age. The same correlation was observed with the NSSA scale displaying increasing weakness, mainly in the lower limbs. 
Thus, we can conclude that both GLS, and QBA may carry the same reliability quantitative assessment of skeletal muscle in DMD.
As for computed tomography, it should be noted that it has not been widely used in the diagnosis and study of muscular dystrophy. The lack of reports in the literature confirms this.
One study on the use of computed tomography imaging method in the muscles, belongs to M. Jiddane, J.L. Gastaut, J.F. Pellissier et al. [11]. The article was published in the «American Journal of Neuroradiology» in 1981. The sample of 75 patients with neuromuscular diseases. Of these, 9 patients with DMD between the ages of 4 to 14 years, with 10 facio-scapulo-humeral muscular dystrophy between the ages of 17–40 years; 25 patients with limb-girdle muscular dystrophy, aged 20 to 65 years; and 7 patients with Steinert myotonic dystrophy.
In the study of the muscles of the forearm made one slice, two slices of arms, two or three slices of the scapular and pelvic girdle, three slices of the thighs and three slices of lower leg. Received data studied primarily for evidence of morphological (atrophy and hypertrophy) and diffuse or local changes (areas of necrosis, fatty infiltration, etc.).
The study was able to identify patterns of skeletal muscle lesion, corresponding to modern concepts of development of the disease, as well as to differentiate the nature of pathological changes in skeletal muscle. 
There are a few reports of CT muscles. In 1976 the value of CT was evaluated in the study of neurogenic muscular atrophy (Wolf, unpublished presentation). In 1979 Bulcke et al. [3] reported a study of skeletal muscles from the CT 24 healthy people. They proposed density scale for each muscle, but did not report any pathological cases. In 1981 Bulcke et al [2] presented the results of muscle CT of three cases of Becker disease. In 1977 O’Doherty et al. [13] had a CT study of muscles in 10 patients. Five of them had Duchenne muscular dystrophy, one had facio-scapulo-humeral muscular dystrophy, have two kugelberg-welander disease, one subacute polymyositis, and one patient with sarcoid myopathy.
However, in view of the shortcomings of this method, first of all because of the high radiation exposure, as well as due to the rapid development capabilities of magnetic resonance imaging, now muscle computed tomography has lost its relevance in this direction.
Currently, magnetic resonance imaging is one of the key techniques in the diagnosis of Duchenne muscular dystrophy. It is a safe, noninvasive method that can reliably detect the symmetry, the severity and pattern of degenerative lesions in the muscle in muscular dystrophy, which reveals a primary lesion of the skeletal muscles, and to evaluate the progression of the disease over time, is also a great help for muscle biopsy, specifying the most suitable for biopsy muscle fibers. As the data useful in the selection of more preferred genetic test.
Magnetic resonance spectroscopy is also non-invasive sampling biochemical method, it was used in conjunction with an MRI to quantify lipid fraction and metabolic products inside the muscle (Prompers et al., 2006) [14].
In 2014, the University of Florida, USA, R.J. Willcocks, I.A. Arpan, S.C. Forbes et al. [15] used MRI to evaluate the skeletal muscles in boys with DMD diagnosis. It was aimed at researching and comparing changes in the lower leg muscle sections over a long period of time. The group of patients and control group in age from 5 to 13 years were taken, there were 15 people in both groups. Lower legs were chosen because of the possibility of long-term studies, as they are involved in the pathological process more slowly compared to thighs.
Pathological changes in the soleus muscle, found in the T2 were significantly higher in the age group of 9–13 years compared to 5–8 year-old patient. The relative change in soleus T2 was 5.5 ± 6.6 % (5–6 yrs: 3.5 ± 5.9 %; 7–8 yrs: 3.5 ± 4.3 %; 9–13 yrs: 11.4 ± 8.5 %) over one year and 9.5 ± 7.4 % (5–6 yrs: 6.9 ± 7.1 %; 7–8 yrs: 7.2 ± 4.3 %; 9–13 yrs: 16.9 ± 7.1 %) over two years. A significant correlation between the MRI readings and muscle strength, as measured by functional tests was found.
While, as T2 of soleus and peroneal muscles increased already been practically within 2 years, the involvement of tibial muscles were slight.
This is shown by previous studies, also noted fatty infiltration mainly in the soleus and peroneal muscles compared with tibial muscle. Long-term observations showed a tendency to a different rate of change in these muscles, but it did not reach statistical significance. This issue remains relevant, further research in this area require a longer period of observation, as well as greater image resolution for a better understanding of the rate of change in the muscles, especially for exploring the relationship between the patient’s age and disease progression in various muscle groups.
Changes in lower legs is increasing more rapidly in 9–13 year old patients than in groups 5–6 and 7–8 years.
This research confirms the practical significance of skeletal muscle in MRI imaging pathological changes as well as the relevance of the method in evaluating the dynamics of disease progression, including the assessment of the impact of drug therapy on muscle.
Another research was in 2014 and published in the journal «Neuromuscular Disorders» authored Wokke, Versluis, Niks et al. [17], designed to assess the skeletal muscles of the legs in children with DMD using quantitative MRI. They made muscle MRI of thighs and lower legs (quadriceps and biceps femoris, tibialis anterior and gastrocnemius muscles) for 16 boys with Duchenne muscular dystrophy and in 11 healthy children from the control group between the ages of 8 and 15. As a result, it was found that in the quadriceps thigh marked reduction in total and contractile cross-sectional area, which was due to muscle atrophy. Total (but not contractile) cross-sectional area was increased in the calf muscles, indicating hypertrophy. Neurological examination also confirmed the decline in muscle strength in the lower legs. 
Magnetic resonance imaging allows you to visualize and differentiate these pathological processes — fatty infiltration, atrophy and hypertrophy. Special diagnostic efficacy of the combination gives a quantitative MRI and skeletal muscle function tests, which allows to assess the progression of the disease over time.
In 2015 R. Claudia, J. Lott Donovan et al. [4] published in the Journal of American physical therapy association work, including both magnetic resonance imaging and MR spectroscopy. 4 boys aged 8–14 years with a diagnosis of DMD were followed for two years, during which time they were examined four times to assess the progression of the disease over time. Control group was examined only in the beginning. Also, 30-foot walking test was used, as well as tests with the rise of the stairs for a comparative evaluation. For the research were selected lower legs, as they are the most suited to long-term studies due to their lesser involvement in the pathological process speed than thighs.
The first boy (8A) at the beginning of the research was 8.1 years. Diagnosis it is set to 6 years. He could walk, but had a pronounced lumbar lordosis, walking on toes and waddling gait. He often stopped to rest, holding on to the wall for support and balance. On a scale of Brook, which assesses lower limbs, he was awarded 4 points, because he was able to walk and get up from the chair on their own. This patient was the only one who had muscular contractures of the calf muscles, hip abductor muscles, hip flexors and hamstrings.
According to MRI in this patient, inflammatory and degenerative changes in the foot flexor muscles (mainly in the soleus muscle) was found in T2. The pathological process characterized by a slow progressive course, reaching a peak at the end of the research. The cross-section after 2 years has increased by 1.25 times in comparison with the initial data. Regarding the lipid profile throughout the study it was characterized by rapid progression. A particularly marked increase in fatty infiltration observed in the final stage of the study (11 % fatty infiltration at the initial stage of research compared to 70 % detected in 2 years).
Test with a 30-foot walking was significantly difficult for the patient in the beginning. 6 months after the study began, the patient has lost the capacity for independent movement, which made it impossible to continue testing.
The second boy (8B) was at the age of 8.9 years. He could move easily and readily carried out a test with 30-foot fast walk. At the beginning of the study, it was not any obvious abnormalities in gait and 1 point in Brook scale, which means that he is able to walk and climb stairs without assistance. DMD was diagnosed at age 4, when the family noticed the difficulty when he played with his peers.
Analysis of T2 images showed only a slight change in the muscles. These figures have remained stable throughout the two-year study. While the cross-sectional area of the muscles in the beginning of the research was almost 3 times higher than the control group (patients 44 cm2 and 16 cm2 in the control group). The area gradually increased throughout the two years. Baseline lipid soleus muscle was slightly higher than that of the control group and by the end of the research increased by only 4 %. 30-foot walking test a slightly different from normal children. Overall, these results, except for the cross sectional area, show the progression of mild DMD patient.
Third boy for 11 years. At the time of the first examination he was 9 years old. The diagnosis was 6 years old when the family noticed first minor symptoms. On a Brooke scale, as well as the previous patient, he had 1 point. Gait was also not changed, he stepped from heel to toe without any deviations. At the beginning of the study there was no contractures.
Just as the previous patient (8B) on T2 it was observed not very pronounced muscle damage compared to the control group (49.1 DMD and 44.2 milliseconds healthy child). This figure has remained stable over the past two years. Muscle cross-sectional area was initially higher than that of the control group and at endpoint rate exceeded 1.5 times. Spectroscopy revealed no obvious differences lipid from healthy children (5 % in DMD and 3 % in the control group). 30-foot walking test also comparable to the control group (5.2 and 4.8 sec), Indicators are not deteriorated in 2 years. These data suggest that despite the increase in muscle tissue, the disease remains stable in this patient.
The fourth boy was at the age of 13.9 years at baseline. He retained the ability to walk without help, but did it slowly and with caution. Diagnosis “Duchenne muscular dystrophy” from 8 years, after several years of treatment from problems with coordination. He had lumbar lordosis, as well as walking on his toes, and waddling gait, on a Brooke scale he had 4 points (the ability to walk and get up from a chair by yourself, but can’t climb stairs). The examination revealed no muscle contractures.
On T2 images pathological changes in muscles throughout the research were 32 % higher than the control group (61.1 ms and 44.2 ms). The cross sectional area of soleus muscles greater than control group of 1.7 times. These rates also remained unchanged.
MR spectroscopy and the 30-foot walking test on the contrary characterized by rapid progression. At baseline, the accumulation of fat in the muscle was 28 % (from a healthy child 1 %), it has reached 48 % after two years. 30-foot walking test was performed in 2.33 times slower than normal (11.3 sec and 5.1 sec). In addition, this indicator deteriorated over time, and a year later this boy lost the opportunity of independent walking. In aggregate, we can conclude a moderate progression of DMD.
Magnetic resonance imaging and spectroscopy — objective, non-invasive and safe methods of assessing muscle pathology and can be used regardless of the patient’s functional abilities. They have a high importance in monitoring the progression of Duchenne muscular dystrophy, evaluating the effectiveness of therapeutic interventions and rehabilitation measures, as well as may be the helper methods in the selection of muscle for biopsy.
Conflicts of interests. Authors declare the absence of any conflicts of interests that might be construed to influence the results or interpretation of their manuscript. 


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