Pediatr Radiol (1992) 22:584-586
Pediatric Radiology 9 Springer-Verlag 1992
Spinal muscular atrophy: MR evaluation G.-C. Liu 1, Y.-J. Jong 2, C.1H, Chiang 2, C.-W. Yang 1 Department of Radiology, Kaohsiung Medical College, Kaohsiung, Taiwan, ROC 2Department of Paediatrics, Kaohsiung Medical College, Kaohsiung, Taiwan, ROC Received: 8 July 1992/Accepted: 8 August 1992
Abstract. The neurogenic myopathy of spinal muscular atrophy (SMA) is degeneration of anterior horn cells of the spinal cord and associated muscle weakness. In three patients with the severe type, according to Dubowitz's classification, magnetic resonance imaging (MRI) of the lower extremity showed severe atrophy of the entire muscle bundles of the thigh and the calf. Nine intermediate type patients had ragged atrophy of muscle bundles of the thigh and the calf with selective preservation of adductor longus muscle. Five patients with the mild type had fatty infiltration of muscle bundles and increased intermuscular fat planes. MRI was insufficient for the evaluation of cervical cord abnormalities. MRI of the lower extremity was a reliable complementary modality for the diagnosis and follow-up of SMA patients.
Spinal muscular atrophy (SMA) is a group of autosomal recessive disorders in which there is degeneration of anterior horn cells of the spinal cord and associated muscle weakness [1]. The diagnosis of degeneration of anterior horn cells has remained difficult even with imaging modalities such as computed tomography (CT). According to Dubowitz's clinical criteria, SMA is classified as three types: severe, intermediate and mild, based on the inability to sit, the inability to walk and the ability to walk, respectively [1]. Because the new imaging modality magnetic resonance imaging (MRI), has been proven as an excellent modality for the evaluation of the musculoskeletal system [2-4] and the central nervous system (CNS) [5], we tried to image the proximal muscles of the lower extremities and cervical spinal cord for the evaluation of SMA patients.
Correspondence to: Gin-Chung Liu, MD, Department of Radiology, Kaohsiung Medical College, N. 100 Shih-Chuan 1st Road, Kaohsiung, Taiwan, ROC
Materials and methods Seventeen patients (12 male, 5 female) with biopsy-proven SMA underwent MRI studies. These patients included the severe type in 3, the intermediate type in 9, and the mild type in 5 cases. The severe-type patients were one 8-month-old and two 2-month-old infants. The intermediate-type patients ranged from 3 to 11 years of age (mean 6.5 years). The mild-type patients were between 3 and 17 years of age. The studies were performed on a 0.5 T superconductive MR scanner (GE-MR MAX, Milwaukee, Wis., USA). Axial and coronal projections were routinely obtained through the calf, thigh and pelvis. The pulse sequence was a Tl-weighted spin-echo sequence (TR/TE = 600/20 ms). The total scanning time was approximately 15 rain. The evaluation of the cervical spinal cord was performed on 12patients, excluding the 3 intermediate- and 2 mild-type patients. Gradient recalled images (TR/TE/angle= 350 ms/20 ms/20 ~ were obtained on both sagittal and axial projections. This part of study consumed an additional 20 rain, including changing the surface coil and position. Secobarbital sedation was given rectally if clinicallyindicated.
Results The MRI findings of SMA in the lower extremity and cervical spinal cord are summarized in Table 1. In the patients with the severe form, MRI revealed severe atrophy of the muscle bundles in both the thigh and the calf (Fig. 1). The intermediate-form patients showed ragged atrophy of most of the thigh muscles (9/9) (Fig. 2) with selective preservation of adductor longus muscles (6/9) (Fig. 3). The calf muscles were also involved. The mildform patients had the MRI findings of fatty infiltration (5/5) and increased intermuscular planes (2/5) in the thighs (Fig. 4). The muscle bundles were intact without atrophic or ragged change. Both the severe and intermediate types had significantly increased subcutaneous fat. The initial 12 patients underwent MRI studies of the cervical cord, but these showed no significant abnormality. Therefore, the last 5 patients did not receive the cervical cord examinations.
585 Table L MRI findings of spinal muscular atrophy in the lower extremity and cervical cord
Increased subcutaneous fat severe mild Ragged atrophy Calf muscle involvement Increased intermuscular fat plane Severe atrophy of muscle bundles Selectively preserved adductor longus muscle Fatty infiltration Cervical cord abnormality
Severe n =3
Intermediate n=9
Mild n =5
2/3 1/3 0 3/3 0 3/3
7/9 2/9 9/9* 6/9 0
0 2/5 0 t/5 2/5 0
0 0 0/3
6/9 9/9 0/6
0 5/5 0/3
9/9 b
Discussion M R I provides high contrast b e t w e e n tissues [6]. T h e musculoskeletal system, therefore, is well analysed by this new imaging m o d a l i t y [2]. A n o t h e r m a j o r asset of M R I is its flexibility t h r o u g h which the t o m o g r a p h i c plane of section m a y be r a n d o m l y oriented. It is also fi'ee from impediments such as the b e a m - h a r d e n i n g artefact in CT. A l t h o u g h earlier M R I studies t e n d e d to provide less spatial resolution than CT, they have b e e n i m p r o v e d by specialized surface coils and higher magnetic field strengths [7, 8]. Besides the a b o v e - m e n t i o n e d advantages, our studies lasted only 15 min and were therefore not time consuming. Because most of the S M A patients were children, the f r e e d o m of radiation exposure by M R I was a n o t h e r advantage. M R I , therefore, provides a reasonable modality for the evaluation of musculoskeletal disorders in children.
a Three cases were mildly involved b Two cases were mildly involved
Fig. 1 a, b. Spinal muscular atrophy (SMA), severe type. A 2-monthold male infant suffered from the severe type of SMA with atrophic change of the entire muscle bundles of the hamstrings and adductors of the thigh (a) and diffuse atrophic change of the calf muscles (b). The subcutaneous fat was prominent Fig.2a-c. SMA, intermediate type. An 11-year-old boy had significant subcutaneous fat increase. All of the muscle bundles of the thigh (a) and calf (b) were ragged. The coronal images of the thigh (c) revealed a fascicular appearance of the muscle bundles
Fig. 3. Selective preservation of adductor longus muscle in a 6-yearold boy (arrow) Fig. 4a. b. SMA, mild type, A 17-year-old boy with the mitd type of SMA showed fatty infiltration with increased signal intensity in the quadriceps and hamstrings. The intermuscular fat planes were slightly prominent on axial (a) and coronal (b) projections
586 SMA is a neurogenic myopathy. The histology of the severe type shows extensive muscle atrophy affecting the whole bundle of fibres. Clusters of large fibres are of uniform histochemical type i [1]. The MRI finding of severe atrophy of the entire muscle bundles without fatty infiltration was compatible with the histological change. It also confirmed the previous CT finding that neural disease first shows as muscle atrophy [9]. In the intermediate form, the ragged atrophy of most of the thigh muscles corresponded to the pathological findings of bundles of uniformly atrophic fibres and isolated groups of large reinnervated fibres. The selective preservation of adductor longus muscle in 6 out of 9 cases (Fig. 3) remains inexplicable because, pathophysiologically the neural myopathy diffusely involved the muscle bundles [10-12]. However, another report of a single case of SMA stated that the selectively involved muscles were quadriceps, adductors, hamstrings, sartorius and gracilis [4]. The partially preserved muscle, therefore, was rectus femoris. Our cases should provide more accurate information because of our larger numbers. In patients with the mild form of SMA, a large group Of atrophy plus variable groups of normal or enlarged fibres are found. The normal muscle bundle architecture may still preserve fibres type grouping. The MRI findings of increased fatty infiltration and increased intermuscular fat planes were also compatible with the histological concepts. Only one of the five mild type patients had calf muscle involvement represented the clinical report of initial proximal muscular involvement. The pathological location of SMA is the anterior horn cell of the spinal cord. Although MRI is excellent for the evaluation of CNS abnormalties, imaging of the cervical cord in our cases showed no definite abnormality. One previous report suspected the possibility of segmental cord atrophy, but was uncertain [13]. Other studies reported the same results as ours [14, 15]. This m a y b e due to insufficient quality of MRI for spinal cord pathology. Further advances in MRI instruments and techniques may lead to significant results. In conclusion, the MRI findings in the lower extremities of different types of SMA were characteristic for each group and were in agreement with histological change. With the advantages of non-invasiveness, simplicity, speed (15 min per examination) and characteristic findings, MRI of the lower extremities should be strongly
considered as a good complementary modality for the diagnosis and follow-up of patients with SMA.
Acknowledgement. We thank Mrs. Y. E. Chiu and F. O. Hsu for their technical assistance and Ms. C. C. Lin for typing the manuscript,
References 1. Dubowitz V (1989) A color atlas of muscle disease in childhood. Wolfe, London 2. Ehman RL, Berquist TH, McLeod RA (1988) MR imaging of the musculoskeletal system: a 5 year appraisal. Radiology 166: 313320 3. Jacobson HG (1989) Musculoskeletal applications of magnetic resonance imaging. JAMA 262:2420-2427 4. Murphy WA, Tony WG, Carroll JE (1986) MRI of normal and pathologic skeletal muscle. A JR 146:565-574 5. Bradley WG Jr, Waluch V, Yadley RA, Wycodd RR (1984) Comparison of CT and MR in 400 patients with suspected disease of the brain and cervical spinal cord. Radiology 152:695-702 6, Ehman RL (1987) Interpretation of magnetic resonance images. In: Berquist TH, Ehman RL, Richardson ML (eds) Magnetic resonance of the musculoskeletal system. Raven, New York, pp 23~54 7. Middleton WD, Macrander S, Lawson TL et al (1987) High resolution surface coil magnetic resonance imaging of the joints anatomic correlation. Radiographics 7:645-683 8. Ehman RL (1985) MR imaging with surface coils. Radiology 157: 549-550 9. Hawley RJ, Schellinger DS, O'Doherty DS (1984) Computed tomographic patterns of muscles in neuromuscular diseases. Arch Neuro141: 383-387 10. Bulcke JAL, Baert AL (1982) Clinical and radiological aspects of myopathies. Springer, Berlin Heidelberg New York, pp 114-120 11. Visser M de, Verbeeten B (1985) Computed tomography of the skeletal musculature in Becker-type muscular dystrophy and benign infantile spinal muscular atrophy. Muscle Nerve 8:435-444 12. Calo M, Crisi G, Martinelli C, Colombo A, Schoenhuber R, Giberton M (1986) CT and the diagnosis of myopathies: preliminary findings in 42 cases. Neuroradiology 28:53-57 13. Oaio JM, Lechevalier B, Hommel M, Viader F, Chapon F, Perret J (1989)Chronic spinal amyotrophyinvolving the upper limbs in young adults (O'Sullivan and McLeod syndrome). MRI study of the cervical spinal cord (in French). Rev Neurol (Paris) 145: 163168 14. Visser M de, Ongerboer de Visser BW, Verbeeten B Jr (1988) Electromyographic and computed tomographic findings in five patients with monomelic spinal muscular atrophy. Eur Neurol 28:135-138 15. Chou SM, Gilbert EF, Chun RW, et al (1990) Infantile olivopontocerebellar atrophy with spinal muscular atrophy. Clin Neuropathol 9:21-32
Pediatric Radiology 9 Springer-Verlag 1992
Spinal muscular atrophy: MR evaluation G.-C. Liu 1, Y.-J. Jong 2, C.1H, Chiang 2, C.-W. Yang 1 Department of Radiology, Kaohsiung Medical College, Kaohsiung, Taiwan, ROC 2Department of Paediatrics, Kaohsiung Medical College, Kaohsiung, Taiwan, ROC Received: 8 July 1992/Accepted: 8 August 1992
Abstract. The neurogenic myopathy of spinal muscular atrophy (SMA) is degeneration of anterior horn cells of the spinal cord and associated muscle weakness. In three patients with the severe type, according to Dubowitz's classification, magnetic resonance imaging (MRI) of the lower extremity showed severe atrophy of the entire muscle bundles of the thigh and the calf. Nine intermediate type patients had ragged atrophy of muscle bundles of the thigh and the calf with selective preservation of adductor longus muscle. Five patients with the mild type had fatty infiltration of muscle bundles and increased intermuscular fat planes. MRI was insufficient for the evaluation of cervical cord abnormalities. MRI of the lower extremity was a reliable complementary modality for the diagnosis and follow-up of SMA patients.
Spinal muscular atrophy (SMA) is a group of autosomal recessive disorders in which there is degeneration of anterior horn cells of the spinal cord and associated muscle weakness [1]. The diagnosis of degeneration of anterior horn cells has remained difficult even with imaging modalities such as computed tomography (CT). According to Dubowitz's clinical criteria, SMA is classified as three types: severe, intermediate and mild, based on the inability to sit, the inability to walk and the ability to walk, respectively [1]. Because the new imaging modality magnetic resonance imaging (MRI), has been proven as an excellent modality for the evaluation of the musculoskeletal system [2-4] and the central nervous system (CNS) [5], we tried to image the proximal muscles of the lower extremities and cervical spinal cord for the evaluation of SMA patients.
Correspondence to: Gin-Chung Liu, MD, Department of Radiology, Kaohsiung Medical College, N. 100 Shih-Chuan 1st Road, Kaohsiung, Taiwan, ROC
Materials and methods Seventeen patients (12 male, 5 female) with biopsy-proven SMA underwent MRI studies. These patients included the severe type in 3, the intermediate type in 9, and the mild type in 5 cases. The severe-type patients were one 8-month-old and two 2-month-old infants. The intermediate-type patients ranged from 3 to 11 years of age (mean 6.5 years). The mild-type patients were between 3 and 17 years of age. The studies were performed on a 0.5 T superconductive MR scanner (GE-MR MAX, Milwaukee, Wis., USA). Axial and coronal projections were routinely obtained through the calf, thigh and pelvis. The pulse sequence was a Tl-weighted spin-echo sequence (TR/TE = 600/20 ms). The total scanning time was approximately 15 rain. The evaluation of the cervical spinal cord was performed on 12patients, excluding the 3 intermediate- and 2 mild-type patients. Gradient recalled images (TR/TE/angle= 350 ms/20 ms/20 ~ were obtained on both sagittal and axial projections. This part of study consumed an additional 20 rain, including changing the surface coil and position. Secobarbital sedation was given rectally if clinicallyindicated.
Results The MRI findings of SMA in the lower extremity and cervical spinal cord are summarized in Table 1. In the patients with the severe form, MRI revealed severe atrophy of the muscle bundles in both the thigh and the calf (Fig. 1). The intermediate-form patients showed ragged atrophy of most of the thigh muscles (9/9) (Fig. 2) with selective preservation of adductor longus muscles (6/9) (Fig. 3). The calf muscles were also involved. The mildform patients had the MRI findings of fatty infiltration (5/5) and increased intermuscular planes (2/5) in the thighs (Fig. 4). The muscle bundles were intact without atrophic or ragged change. Both the severe and intermediate types had significantly increased subcutaneous fat. The initial 12 patients underwent MRI studies of the cervical cord, but these showed no significant abnormality. Therefore, the last 5 patients did not receive the cervical cord examinations.
585 Table L MRI findings of spinal muscular atrophy in the lower extremity and cervical cord
Increased subcutaneous fat severe mild Ragged atrophy Calf muscle involvement Increased intermuscular fat plane Severe atrophy of muscle bundles Selectively preserved adductor longus muscle Fatty infiltration Cervical cord abnormality
Severe n =3
Intermediate n=9
Mild n =5
2/3 1/3 0 3/3 0 3/3
7/9 2/9 9/9* 6/9 0
0 2/5 0 t/5 2/5 0
0 0 0/3
6/9 9/9 0/6
0 5/5 0/3
9/9 b
Discussion M R I provides high contrast b e t w e e n tissues [6]. T h e musculoskeletal system, therefore, is well analysed by this new imaging m o d a l i t y [2]. A n o t h e r m a j o r asset of M R I is its flexibility t h r o u g h which the t o m o g r a p h i c plane of section m a y be r a n d o m l y oriented. It is also fi'ee from impediments such as the b e a m - h a r d e n i n g artefact in CT. A l t h o u g h earlier M R I studies t e n d e d to provide less spatial resolution than CT, they have b e e n i m p r o v e d by specialized surface coils and higher magnetic field strengths [7, 8]. Besides the a b o v e - m e n t i o n e d advantages, our studies lasted only 15 min and were therefore not time consuming. Because most of the S M A patients were children, the f r e e d o m of radiation exposure by M R I was a n o t h e r advantage. M R I , therefore, provides a reasonable modality for the evaluation of musculoskeletal disorders in children.
a Three cases were mildly involved b Two cases were mildly involved
Fig. 1 a, b. Spinal muscular atrophy (SMA), severe type. A 2-monthold male infant suffered from the severe type of SMA with atrophic change of the entire muscle bundles of the hamstrings and adductors of the thigh (a) and diffuse atrophic change of the calf muscles (b). The subcutaneous fat was prominent Fig.2a-c. SMA, intermediate type. An 11-year-old boy had significant subcutaneous fat increase. All of the muscle bundles of the thigh (a) and calf (b) were ragged. The coronal images of the thigh (c) revealed a fascicular appearance of the muscle bundles
Fig. 3. Selective preservation of adductor longus muscle in a 6-yearold boy (arrow) Fig. 4a. b. SMA, mild type, A 17-year-old boy with the mitd type of SMA showed fatty infiltration with increased signal intensity in the quadriceps and hamstrings. The intermuscular fat planes were slightly prominent on axial (a) and coronal (b) projections
586 SMA is a neurogenic myopathy. The histology of the severe type shows extensive muscle atrophy affecting the whole bundle of fibres. Clusters of large fibres are of uniform histochemical type i [1]. The MRI finding of severe atrophy of the entire muscle bundles without fatty infiltration was compatible with the histological change. It also confirmed the previous CT finding that neural disease first shows as muscle atrophy [9]. In the intermediate form, the ragged atrophy of most of the thigh muscles corresponded to the pathological findings of bundles of uniformly atrophic fibres and isolated groups of large reinnervated fibres. The selective preservation of adductor longus muscle in 6 out of 9 cases (Fig. 3) remains inexplicable because, pathophysiologically the neural myopathy diffusely involved the muscle bundles [10-12]. However, another report of a single case of SMA stated that the selectively involved muscles were quadriceps, adductors, hamstrings, sartorius and gracilis [4]. The partially preserved muscle, therefore, was rectus femoris. Our cases should provide more accurate information because of our larger numbers. In patients with the mild form of SMA, a large group Of atrophy plus variable groups of normal or enlarged fibres are found. The normal muscle bundle architecture may still preserve fibres type grouping. The MRI findings of increased fatty infiltration and increased intermuscular fat planes were also compatible with the histological concepts. Only one of the five mild type patients had calf muscle involvement represented the clinical report of initial proximal muscular involvement. The pathological location of SMA is the anterior horn cell of the spinal cord. Although MRI is excellent for the evaluation of CNS abnormalties, imaging of the cervical cord in our cases showed no definite abnormality. One previous report suspected the possibility of segmental cord atrophy, but was uncertain [13]. Other studies reported the same results as ours [14, 15]. This m a y b e due to insufficient quality of MRI for spinal cord pathology. Further advances in MRI instruments and techniques may lead to significant results. In conclusion, the MRI findings in the lower extremities of different types of SMA were characteristic for each group and were in agreement with histological change. With the advantages of non-invasiveness, simplicity, speed (15 min per examination) and characteristic findings, MRI of the lower extremities should be strongly
considered as a good complementary modality for the diagnosis and follow-up of patients with SMA.
Acknowledgement. We thank Mrs. Y. E. Chiu and F. O. Hsu for their technical assistance and Ms. C. C. Lin for typing the manuscript,
References 1. Dubowitz V (1989) A color atlas of muscle disease in childhood. Wolfe, London 2. Ehman RL, Berquist TH, McLeod RA (1988) MR imaging of the musculoskeletal system: a 5 year appraisal. Radiology 166: 313320 3. Jacobson HG (1989) Musculoskeletal applications of magnetic resonance imaging. JAMA 262:2420-2427 4. Murphy WA, Tony WG, Carroll JE (1986) MRI of normal and pathologic skeletal muscle. A JR 146:565-574 5. Bradley WG Jr, Waluch V, Yadley RA, Wycodd RR (1984) Comparison of CT and MR in 400 patients with suspected disease of the brain and cervical spinal cord. Radiology 152:695-702 6, Ehman RL (1987) Interpretation of magnetic resonance images. In: Berquist TH, Ehman RL, Richardson ML (eds) Magnetic resonance of the musculoskeletal system. Raven, New York, pp 23~54 7. Middleton WD, Macrander S, Lawson TL et al (1987) High resolution surface coil magnetic resonance imaging of the joints anatomic correlation. Radiographics 7:645-683 8. Ehman RL (1985) MR imaging with surface coils. Radiology 157: 549-550 9. Hawley RJ, Schellinger DS, O'Doherty DS (1984) Computed tomographic patterns of muscles in neuromuscular diseases. Arch Neuro141: 383-387 10. Bulcke JAL, Baert AL (1982) Clinical and radiological aspects of myopathies. Springer, Berlin Heidelberg New York, pp 114-120 11. Visser M de, Verbeeten B (1985) Computed tomography of the skeletal musculature in Becker-type muscular dystrophy and benign infantile spinal muscular atrophy. Muscle Nerve 8:435-444 12. Calo M, Crisi G, Martinelli C, Colombo A, Schoenhuber R, Giberton M (1986) CT and the diagnosis of myopathies: preliminary findings in 42 cases. Neuroradiology 28:53-57 13. Oaio JM, Lechevalier B, Hommel M, Viader F, Chapon F, Perret J (1989)Chronic spinal amyotrophyinvolving the upper limbs in young adults (O'Sullivan and McLeod syndrome). MRI study of the cervical spinal cord (in French). Rev Neurol (Paris) 145: 163168 14. Visser M de, Ongerboer de Visser BW, Verbeeten B Jr (1988) Electromyographic and computed tomographic findings in five patients with monomelic spinal muscular atrophy. Eur Neurol 28:135-138 15. Chou SM, Gilbert EF, Chun RW, et al (1990) Infantile olivopontocerebellar atrophy with spinal muscular atrophy. Clin Neuropathol 9:21-32
