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Bilaterally symmetric cervical spondylotic amyotrophy: A novel presentation and review of the literature
Journal of the Neurological Sciences 290 (2010) 142–145
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Clinical Short Communication
Bilaterally symmetric cervical spondylotic amyotrophy: A novel presentation and review of the literature Sisay Gizaw Gebere-Michael a, James C. Johnston a,b,⁎, Guta Zenebe Metaferia a, Mehila Zebenigus Wuhib a, Hubert Henery Fernandez c a b c
Department of Neurology, Medical Faculty, Addis Ababa University, Addis Ababa, Ethiopia Neurology Services, Legal Medicine Consultants, Seattle, Washington, USA Department of Neurology, College of Medicine, University of Florida, Gainesville, Florida, USA
a r t i c l e
i n f o
Article history: Received 8 September 2009 Received in revised form 25 November 2009 Accepted 8 December 2009 Available online December 31 2009 Keywords: Cervical spondylosis Cervical spondylotic amyotrophy Cervical spondylotic myelopathy Motor dissociation syndrome Vulpian–Bernhardt syndrome Flail arm syndrome
a b s t r a c t Background: Cervical spondylotic amyotrophy (CSA) is considered a syndrome of (1) unilateral upper extremity weakness and atrophy, (2) affecting either the proximal or distal musculature, (3) without sensory impairment or lower extremity dysfunction. Aims of study: The authors report a novel case of bilaterally symmetric CSA with blurring of the proximal– distal distinction, discuss the pathophysiology, and review the literature. Methods: A 45 year old man presented with a several year history of insidiously progressive bilaterally symmetric upper extremity weakness and wasting, profound in the proximal musculature and moderate to severe in the distal muscle groups. Results: Based on the clinical, neuroimaging and electrodiagnostic features, this patient harbors a more severe phenotype of the classical syndrome. Conclusion: The authors propose expanding the generally accepted definition of CSA to include this bilaterally symmetric form of disease, thereby minimizing diagnostic error or delay. Additionally, based on this case and a review of the literature, adherence to the proximal–distal distinction should be avoided since it is commonly blurred. Accurate diagnosis is crucial since this presentation mimics the motor neuron disease variant Vulpian–Bernhardt syndrome. The importance of early diagnosis is underscored by reports of significant improvement with timely surgical decompression. © 2009 Elsevier B.V. All rights reserved.
1. Introduction
2. Case report
Brain et al. first described cervical spondylosis presenting with upper extremity muscle atrophy and weakness in the absence of sensory impairment or myelopathy [1]. Keegan labeled the condition “dissociated motor loss syndrome,” Crandall and Batzdorf suggested the term “motor system syndrome,” and ensuing reports settled on the phrase “cervical spondylotic amyotrophy” (CSA) [2–4]. This condition is rare, characteristically described as unilateral, and classified according to the most predominantly affected muscle groups as either proximal (scapular, deltoid and biceps) or distal (triceps, forearm and hand) [5]. We present a novel case of bilaterally symmetric proximal CSA with spillover into the distal myotomes, and discuss the pathophysiological implications of this unusual syndrome.
A 45 year old male without significant past medical history or trauma presented to the Tikur Anbessa Hospital Neurology Department in Addis Ababa, Ethiopia with insidiously progressive bilaterally symmetric upper extremity weakness and wasting over the past 6 years. Additionally, he described a two year history of fasciculations in the involved musculature and diffuse intermittent aching of the left upper arm. Family history is negative for neurological disease. He is a government employee, married with seven children, and has no history of alcohol, tobacco or illicit drug use or abuse. Cognitive functions and cranial nerves were normal. Motor examination demonstrated severe atrophy throughout both shoulder girdles, as well as the bicep and tricep muscles, all being flaccid with spontaneous fasciculations. [Fig. 1] The bilateral forearm and hand muscles demonstrated moderate weakness with atrophy, and there were spontaneous fasciculations throughout the intrinsic hand musculature. Lower extremity motor examination revealed normal tone, bulk and strength. Sensory examination was normal to all primary modalities throughout the upper and lower extremities. Autonomic functions were preserved. Muscle stretch reflexes were
⁎ Corresponding author. Neurology Services, Legal Medicine Consultants, 321 High School Road NE, Suite D3-750, Bainbridge Island, Seattle, WA, USA 98110. Tel.: +1 206 2013618; fax: +1 206 2013619. E-mail address: [email protected] (J.C. Johnston). 0022-510X/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2009.12.009
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in the bilateral forearms and hand. The trapezius and lower extremity muscles had normal insertional activity, normal motor unit potentials and full recruitment. Magnetic resonance (MR) imaging of the cervical spine with and without gadolinium demonstrates loss of the normal lordosis with multi-segmental degenerative arthritis and degenerative disc disease, pronounced C3–C7 stenosis, and multi-segmental bilateral foraminal encroachment at C4–C5 and C5–C6, as well as left C3–C4 and right C6–C7 foraminal narrowing. There are multiple levels of marked extradural compression (anteroposterior canal diameters of 10 mm or less at C3–C4, C4–C5, and C5–C6), resulting in significant flattening of the cord with a compression ratio of 0.4. [Fig. 2-A] These findings are pathognomonic for spondylogenic compression of the spinal cord. T2-imaging demonstrates linear, circumscribed non-enhancing high signal intensity (HSI) lesions in the anterior horn (AH) regions consistent with spondylotic myelomalacia. [Fig. 2-B] 3. Discussion
Fig. 1. Severe wasting of the bilateral shoulder girdle musculature and biceps, and moderate wasting of forearms and hands.
hyporeflexic but symmetric in the upper extremities, and normoreflexic in the lower extremities with flexor plantar responses. Stance and posture demonstrated an adducted, hanging position of the arms. Gait including tandem walking was normal except for the absence of armswing. Routine hematologic studies, CPK and sedimentation rate were normal. HIV testing (ELISA) was negative. Salient features of the nerve conduction studies included mild right ulnar conduction slowing across the olecranon, and bilateral absence of ulnar F-waves. Electromyography of the bilateral deltoid, supraspinatus and infraspinatus demonstrated no spontaneous activity and an absence of motor units. Chronic neurogenic motor unit potentials were evident
CSA is considered a syndrome with unilateral upper extremity weakness and atrophy of either the proximal or distal musculature, without sensory impairment or lower extremity dysfunction. The proximal variant encompasses a broad phenotypic spectrum including boule musculaire in prodromal or mild stages;[6,7] unilateral wasting of a single muscle;[8] unilateral shoulder girdle wasting, which may occur with distal electromyographic denervation and, in more severe cases, distal weakness;[5,9] unilateral features with electromyographic denervation in the contralateral limb;[10] and unilateral shoulder girdle wasting with mild contralateral weakness [9]. Sporadic case reports have focused on the pathophysiology in order to unravel this clinically heterogeneous disorder [2,8–15]. Keegan, reporting the first autopsy of CSA, demonstrated a normal AH appearance and attributed the pathophysiology to selective intradural ventral nerve root (VNR) compression by posterolateral osteophytes [2]. Matsunaga et al. supported this view by correlating
Fig. 2. A. Axial MR images at C3–C4 (top) and C4–C5 (bottom) demonstrating marked extradural compression with a maximal anteroposterior canal diameter of 10 mm, and flattening of the cord with a compression ratio of 0.4. B. T2-weighted sagittal MR image demonstrating severe multi-segmental degenerative spondylotic disease with C3–C7 canal stenosis and circumscribed non-enhancing intramedullary HSI lesions.
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S.G. Gebere-Michael et al. / Journal of the Neurological Sciences 290 (2010) 142–145
11 cases of proximal dissociated motor loss with isolated selective spondylotic compression of preforaminal anterior nerve roots [11]. However, subsequent reports based on delayed enhanced computed tomographic myelography (CTM) and MR imaging provided convincing evidence that AH compression or vascular insufficiency caused CSA. Asaka et al. suggested an ischemic etiology after describing one case of proximal dissociated motor loss with CTM and MR imaging evidence of AH cavities indicating cystic necrosis [12]. Fujiwara refined this view, albeit in a case of predominantly distal CSA, through CTM and MR imaging localization of AH cystic necrosis ipsilateral to the symptomatic arm [13]. Kameyama et al. and Shibuya et al. each described three proximal CSA patients with multi-segmental AH HSI lesions on T2-weighted MR imaging consistent with vascular insufficiency [9,14]. However, intramedullary lesions are not ubiquitous in proximal CSA. Mori et al. reported three proximal CSA patients, two with VNR compression and one with spinal cord compression, without evidence of intramedullary pathology, and based on significant improvement after anterior decompression suggested they had not developed irreversible cystic necrosis [10]. Shinomiya et al. and Fujiwara et al., with the advent of invasive electrodiagnostic testing during surgical intervention, corroborated both VNR compression and multi-segmental AH necrosis, independently or jointly, as etiopathogenetic mechanisms of CSA [8,15]. It is the widely variable location, extent and severity of the underlying pathology that accounts for the clinical heterogeneity of CSA. In the instant case, the clinical features, neuroimaging studies and electrodiagnostic testing demonstrated advanced spondylosis with a combination of extensive intramedullary necrosis and bilateral multisegmental VNR compressions. This appears to be a more severe form of the classic syndrome, and represents the first report of a bilaterally symmetric picture with blurring of the proximal–distal distinction. The common underlying pathophysiology unites bilateral and unilateral, as well as proximal and distal, presentations. There is, however, a striking paucity of literature describing bilateral disease. A multiple database (PubMed, Scopus, Cochrane Database, Google Scholar) English language search of proximal CSA yields 72 cases, [2,5,8–12,14,15] excluding patients with concomitant myelopathy or sensory impairment,[16–18] post-operative dissociated motor loss, [19] antecedent post-polio syndrome,[20] or associated Hirayama's disease [21]. These cases include two reports covering a total of three patients with bilateral signs, all readily distinguished from our case [2,9]. First, Keegan's early post-mortem described one patient with left shoulder girdle weakness and atrophy developing 4 years after similar right sided symptoms [2]. This was not a bilateral presentation, but temporally discrete and isolated unilateral events. Our patient exhibited the insidious onset and progression of bilateral disease. Second, Kaneyama reported two cases of proximal CSA with bilateral features: one had an asymmetric weakness; the other had a two week progression of findings limited to the spinati and deltoid muscles, with completely normal triceps, forearms and hand musculature [9]. In contrast, our patient with insidiously progressive bilateral disease had symmetric atrophy and weakness, extending throughout the distal myotomes. This novel case presentation may reflect an unusual occurrence or rare variant; however, it is more likely that bilateral disease is simply under-recognized or misdiagnosed. It would be illogical to conclude that the myriad presentations including asymmetrical bilateral disease stop short of symmetrical bilateral disease. There are two reasons this syndrome may be overlooked. First, CSA has been labeled a unilateral disease since the original descriptions a half century ago. This makes it difficult to diagnosis the bilateral form until it progresses to include a myelopathy, leading to the label of cervical spondylotic myelopathy. Second, this bilaterally symmetric presentation may be misdiagnosed as the motor neuron disease variant termed Vulpian– Bernhardt syndrome, brachial amyotrophic diplegia, flail arm [FA], or man in the barrel syndrome [22]. The very early stages of FA may be
clinically indistinguishable from CSA; however, most patients with FA develop symptoms beyond the arms by 36 months [22]. In our patient, the total absence of bulbar or lower limb signs or symptoms after almost 7 years militated against FA. MR imaging bore all the earmarks of advanced spondylosis including pronounced stenosis with cord compression and intramedullary necrosis, as well as multilevel bilateral nerve root compressions. These features, in conjunction with the clinical picture, unequivocally substantiate the diagnosis of CSA. The total absence of acute denervation on electromyography excludes the extraordinarily remote possibility of a concomitant, atypical FA. Physicians must be aware of this bilaterally symmetric form of CSA in order to avoid diagnostic error or delay. Early diagnosis of CSA is crucial, underscored by reports of significant improvement with timely decompression, probably due to the presence of functionally reversible AH motor nuclei and nerve root fibers [10]. This finding is not negated by the fact that specific treatment options remain controversial as some authors advocate anterior decompression, [8,10] and others recommend a posterior approach [11,15]. Early intervention is further supported by evidence that patients harboring VNR compression without AH necrosis have a superior outcome regardless of the surgical approach, [8,15] and even with cord compression surgery appears beneficial if performed before development of intramedullary pathology [10]. This comports with the postoperative outcome findings in patients with cervical spondylotic myelopathy [23]. Indeed, there appears to be a narrow window of opportunity for surgical management. We propose expanding the generally accepted definition of CSA to include this bilaterally symmetric form of disease, thereby limiting diagnostic error or delay. Additionally, based on our case and a review of the literature, strict adherence to the proximal–distal distinction should be avoided since it is commonly blurred. 4. Conclusion Bilaterally symmetric CSA with blurring of the proximal–distal distinction is probably under-recognized or misdiagnosed due to a misperception that the disease is unilateral, and limited to either proximal or distal musculature. This novel presentation warrants expanding the traditionally accepted definition of CSA. Acknowledgement We thank the patient for cooperating and providing personal medical information in our preparation of this report. References [1] Brain WR, Northfield D, Wilkinson M. The neurological manifestations of cervical spondylosis. Brain 1952;75:187–225. [2] Keegan JJ. The cause of dissociated motor loss in the upper extremities with cervical spondylosis. J Neurosurg 1965;23:528–36. [3] Crandall PH, Batzdorf U. Cervical spondylotic myelopathy. J Neurosurg 1966;25: 57–66. [4] Yanagi T, Kato H, Sobue I. Clinical characteristics of cervical spondylotic amyotrophy. Clin Neurol (Rinsho Shinkeigaku) 1976;16:520–8. [5] Tsuboi Y, Tokumaru Y, Hirayama K. Clinical difference between “proximal” and “distal” type of cervical spondylotic amyotrophy. Clin Neurol (Rinsho Shinkeigaku) 1995;35:147–52. [6] Tamura M, Shinbo S, Ogawa K, Tamiya T, Takasu T. The clinical features of cervical spondylosis with boule musculaire. Clin Neurol (Rinsho Shinkeigaku) 1999;39 (11):1097–103. [7] Taguchi Y, Takashima S, Tanaka K. Boule musculaire associated with cervical spondylosis. Int Med 2007;46(6):329. [8] Shinomiya K, Komori H, Matsuoka T, Mutoh N, Furuya K. Neuroradiologic and electrophysiologic assessment of cervical spondylotic amyotrophy. Spine 1994;19 (1):21–5. [9] Kameyama T, Tetsuo A, Yanagi T, Keizo Y, Sobue G. Cervical spondylotic amyotrophy: magnetic resonance imaging demonstration of intrinsic cord pathology. Spine 1998;23(4):448–52.
S.G. Gebere-Michael et al. / Journal of the Neurological Sciences 290 (2010) 142–145 [10] Mori K, Yamamoto T, Nakao Y, Maeda M. Cervical spondylotic amyotrophy treated by anterior decompression. Neurol Med Chir (Tokyo) 2006;46:366–70. [11] Matsunaga S, Sakou T, Imamura T, Morimoto N. Dissociated motor loss in the upper extremities. Spine 1993;18(14):1964–7. [12] Asaka T, Satake R, Takamori M, Matsushima A. Dissociated motor loss syndrome with cavities in the anterior horns. Intern Med 1995;34:1027–9. [13] Fujiwara K. Cervical spondylotic amyotrophy with intramedullary cavity formation. Spine 2001;26(10):E220–2. [14] Shibuya R, Yonenobu K, Yamamoto K, Kuratsu S, Onoue K, Yoshikawa H. Acute arm paresis with cervical spondylosis: three case reports. Surg Neurol 2005;63 (3):220–8. [15] Fujiwara Y, Tanaka N, Fujimoto Y, Nakanishi K, Kamei N, Ochi M. Surgical outcomes of posterior decompression for cervical spondylosis with unilateral upper extremity amyotrophy. Spine 2006;31(20):E728–32. [16] Sasai K, Umeda M, Saito T, Ohnari H, Wakabayashi E, Iida H. Microsurgical posterior foraminotomy and laminoplasty for cervical spondylotic radiculomyelopathy including cervical spondylotic amyotrophy. J Neurosurg Spine 2006;5: 126–32.
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[17] Mizuno J, Nakagawa H, Hashizume Y. Cervical amyotrophy caused by hypertrophy of the posterior longitudinal ligament. Spinal Cord 2002;40:484–8. [18] Subramaniam P, Kumar R, Biswas A. Cervical spondylotic myelopathy mimicking ALS. IJPMR 2008;19(2):64–5. [19] O'Toole J, Olson T, Kaiser M. Surgical management of dissociated motor loss following complex cervical spine reconstruction. Spine 2004;29(3):E56–60. [20] Isobe T, Yaguchi H, Matsui K, Inoue K. A case of cervical spondylotic amyotrophy resembling post-polio syndrome. Clin Neurol (Rinsho Shinkeigaku) 2006;46(1): 59–61. [21] Hashiguchi S, Ogasawara N, Watanabe A, Kawachi Y, Miki N. Cervical spondylotic amyotrophy associated with Hirayama's disease. Intern Med 1997;36:647–50. [22] Wijesekera L, Mathers S, Talman P, Galtrey C, Parkinson M, Ganesalingam J, et al. Natural history and clinical features of the flail arm and flail leg ALS variants. Neurology 2009;72:1087–94. [23] Papadopoulos CA, Katonis P, Papagelopoulos PJ, Karampekios S, Hadjipavlou AG. Surgical decompression for cervical spondylotic myelopathy: correlation between operative outcomes and MRI of the spinal cord. Orthopedics 2004;27(10): 1087–91.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Clinical Short Communication
Bilaterally symmetric cervical spondylotic amyotrophy: A novel presentation and review of the literature Sisay Gizaw Gebere-Michael a, James C. Johnston a,b,⁎, Guta Zenebe Metaferia a, Mehila Zebenigus Wuhib a, Hubert Henery Fernandez c a b c
Department of Neurology, Medical Faculty, Addis Ababa University, Addis Ababa, Ethiopia Neurology Services, Legal Medicine Consultants, Seattle, Washington, USA Department of Neurology, College of Medicine, University of Florida, Gainesville, Florida, USA
a r t i c l e
i n f o
Article history: Received 8 September 2009 Received in revised form 25 November 2009 Accepted 8 December 2009 Available online December 31 2009 Keywords: Cervical spondylosis Cervical spondylotic amyotrophy Cervical spondylotic myelopathy Motor dissociation syndrome Vulpian–Bernhardt syndrome Flail arm syndrome
a b s t r a c t Background: Cervical spondylotic amyotrophy (CSA) is considered a syndrome of (1) unilateral upper extremity weakness and atrophy, (2) affecting either the proximal or distal musculature, (3) without sensory impairment or lower extremity dysfunction. Aims of study: The authors report a novel case of bilaterally symmetric CSA with blurring of the proximal– distal distinction, discuss the pathophysiology, and review the literature. Methods: A 45 year old man presented with a several year history of insidiously progressive bilaterally symmetric upper extremity weakness and wasting, profound in the proximal musculature and moderate to severe in the distal muscle groups. Results: Based on the clinical, neuroimaging and electrodiagnostic features, this patient harbors a more severe phenotype of the classical syndrome. Conclusion: The authors propose expanding the generally accepted definition of CSA to include this bilaterally symmetric form of disease, thereby minimizing diagnostic error or delay. Additionally, based on this case and a review of the literature, adherence to the proximal–distal distinction should be avoided since it is commonly blurred. Accurate diagnosis is crucial since this presentation mimics the motor neuron disease variant Vulpian–Bernhardt syndrome. The importance of early diagnosis is underscored by reports of significant improvement with timely surgical decompression. © 2009 Elsevier B.V. All rights reserved.
1. Introduction
2. Case report
Brain et al. first described cervical spondylosis presenting with upper extremity muscle atrophy and weakness in the absence of sensory impairment or myelopathy [1]. Keegan labeled the condition “dissociated motor loss syndrome,” Crandall and Batzdorf suggested the term “motor system syndrome,” and ensuing reports settled on the phrase “cervical spondylotic amyotrophy” (CSA) [2–4]. This condition is rare, characteristically described as unilateral, and classified according to the most predominantly affected muscle groups as either proximal (scapular, deltoid and biceps) or distal (triceps, forearm and hand) [5]. We present a novel case of bilaterally symmetric proximal CSA with spillover into the distal myotomes, and discuss the pathophysiological implications of this unusual syndrome.
A 45 year old male without significant past medical history or trauma presented to the Tikur Anbessa Hospital Neurology Department in Addis Ababa, Ethiopia with insidiously progressive bilaterally symmetric upper extremity weakness and wasting over the past 6 years. Additionally, he described a two year history of fasciculations in the involved musculature and diffuse intermittent aching of the left upper arm. Family history is negative for neurological disease. He is a government employee, married with seven children, and has no history of alcohol, tobacco or illicit drug use or abuse. Cognitive functions and cranial nerves were normal. Motor examination demonstrated severe atrophy throughout both shoulder girdles, as well as the bicep and tricep muscles, all being flaccid with spontaneous fasciculations. [Fig. 1] The bilateral forearm and hand muscles demonstrated moderate weakness with atrophy, and there were spontaneous fasciculations throughout the intrinsic hand musculature. Lower extremity motor examination revealed normal tone, bulk and strength. Sensory examination was normal to all primary modalities throughout the upper and lower extremities. Autonomic functions were preserved. Muscle stretch reflexes were
⁎ Corresponding author. Neurology Services, Legal Medicine Consultants, 321 High School Road NE, Suite D3-750, Bainbridge Island, Seattle, WA, USA 98110. Tel.: +1 206 2013618; fax: +1 206 2013619. E-mail address: [email protected] (J.C. Johnston). 0022-510X/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2009.12.009
S.G. Gebere-Michael et al. / Journal of the Neurological Sciences 290 (2010) 142–145
143
in the bilateral forearms and hand. The trapezius and lower extremity muscles had normal insertional activity, normal motor unit potentials and full recruitment. Magnetic resonance (MR) imaging of the cervical spine with and without gadolinium demonstrates loss of the normal lordosis with multi-segmental degenerative arthritis and degenerative disc disease, pronounced C3–C7 stenosis, and multi-segmental bilateral foraminal encroachment at C4–C5 and C5–C6, as well as left C3–C4 and right C6–C7 foraminal narrowing. There are multiple levels of marked extradural compression (anteroposterior canal diameters of 10 mm or less at C3–C4, C4–C5, and C5–C6), resulting in significant flattening of the cord with a compression ratio of 0.4. [Fig. 2-A] These findings are pathognomonic for spondylogenic compression of the spinal cord. T2-imaging demonstrates linear, circumscribed non-enhancing high signal intensity (HSI) lesions in the anterior horn (AH) regions consistent with spondylotic myelomalacia. [Fig. 2-B] 3. Discussion
Fig. 1. Severe wasting of the bilateral shoulder girdle musculature and biceps, and moderate wasting of forearms and hands.
hyporeflexic but symmetric in the upper extremities, and normoreflexic in the lower extremities with flexor plantar responses. Stance and posture demonstrated an adducted, hanging position of the arms. Gait including tandem walking was normal except for the absence of armswing. Routine hematologic studies, CPK and sedimentation rate were normal. HIV testing (ELISA) was negative. Salient features of the nerve conduction studies included mild right ulnar conduction slowing across the olecranon, and bilateral absence of ulnar F-waves. Electromyography of the bilateral deltoid, supraspinatus and infraspinatus demonstrated no spontaneous activity and an absence of motor units. Chronic neurogenic motor unit potentials were evident
CSA is considered a syndrome with unilateral upper extremity weakness and atrophy of either the proximal or distal musculature, without sensory impairment or lower extremity dysfunction. The proximal variant encompasses a broad phenotypic spectrum including boule musculaire in prodromal or mild stages;[6,7] unilateral wasting of a single muscle;[8] unilateral shoulder girdle wasting, which may occur with distal electromyographic denervation and, in more severe cases, distal weakness;[5,9] unilateral features with electromyographic denervation in the contralateral limb;[10] and unilateral shoulder girdle wasting with mild contralateral weakness [9]. Sporadic case reports have focused on the pathophysiology in order to unravel this clinically heterogeneous disorder [2,8–15]. Keegan, reporting the first autopsy of CSA, demonstrated a normal AH appearance and attributed the pathophysiology to selective intradural ventral nerve root (VNR) compression by posterolateral osteophytes [2]. Matsunaga et al. supported this view by correlating
Fig. 2. A. Axial MR images at C3–C4 (top) and C4–C5 (bottom) demonstrating marked extradural compression with a maximal anteroposterior canal diameter of 10 mm, and flattening of the cord with a compression ratio of 0.4. B. T2-weighted sagittal MR image demonstrating severe multi-segmental degenerative spondylotic disease with C3–C7 canal stenosis and circumscribed non-enhancing intramedullary HSI lesions.
144
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11 cases of proximal dissociated motor loss with isolated selective spondylotic compression of preforaminal anterior nerve roots [11]. However, subsequent reports based on delayed enhanced computed tomographic myelography (CTM) and MR imaging provided convincing evidence that AH compression or vascular insufficiency caused CSA. Asaka et al. suggested an ischemic etiology after describing one case of proximal dissociated motor loss with CTM and MR imaging evidence of AH cavities indicating cystic necrosis [12]. Fujiwara refined this view, albeit in a case of predominantly distal CSA, through CTM and MR imaging localization of AH cystic necrosis ipsilateral to the symptomatic arm [13]. Kameyama et al. and Shibuya et al. each described three proximal CSA patients with multi-segmental AH HSI lesions on T2-weighted MR imaging consistent with vascular insufficiency [9,14]. However, intramedullary lesions are not ubiquitous in proximal CSA. Mori et al. reported three proximal CSA patients, two with VNR compression and one with spinal cord compression, without evidence of intramedullary pathology, and based on significant improvement after anterior decompression suggested they had not developed irreversible cystic necrosis [10]. Shinomiya et al. and Fujiwara et al., with the advent of invasive electrodiagnostic testing during surgical intervention, corroborated both VNR compression and multi-segmental AH necrosis, independently or jointly, as etiopathogenetic mechanisms of CSA [8,15]. It is the widely variable location, extent and severity of the underlying pathology that accounts for the clinical heterogeneity of CSA. In the instant case, the clinical features, neuroimaging studies and electrodiagnostic testing demonstrated advanced spondylosis with a combination of extensive intramedullary necrosis and bilateral multisegmental VNR compressions. This appears to be a more severe form of the classic syndrome, and represents the first report of a bilaterally symmetric picture with blurring of the proximal–distal distinction. The common underlying pathophysiology unites bilateral and unilateral, as well as proximal and distal, presentations. There is, however, a striking paucity of literature describing bilateral disease. A multiple database (PubMed, Scopus, Cochrane Database, Google Scholar) English language search of proximal CSA yields 72 cases, [2,5,8–12,14,15] excluding patients with concomitant myelopathy or sensory impairment,[16–18] post-operative dissociated motor loss, [19] antecedent post-polio syndrome,[20] or associated Hirayama's disease [21]. These cases include two reports covering a total of three patients with bilateral signs, all readily distinguished from our case [2,9]. First, Keegan's early post-mortem described one patient with left shoulder girdle weakness and atrophy developing 4 years after similar right sided symptoms [2]. This was not a bilateral presentation, but temporally discrete and isolated unilateral events. Our patient exhibited the insidious onset and progression of bilateral disease. Second, Kaneyama reported two cases of proximal CSA with bilateral features: one had an asymmetric weakness; the other had a two week progression of findings limited to the spinati and deltoid muscles, with completely normal triceps, forearms and hand musculature [9]. In contrast, our patient with insidiously progressive bilateral disease had symmetric atrophy and weakness, extending throughout the distal myotomes. This novel case presentation may reflect an unusual occurrence or rare variant; however, it is more likely that bilateral disease is simply under-recognized or misdiagnosed. It would be illogical to conclude that the myriad presentations including asymmetrical bilateral disease stop short of symmetrical bilateral disease. There are two reasons this syndrome may be overlooked. First, CSA has been labeled a unilateral disease since the original descriptions a half century ago. This makes it difficult to diagnosis the bilateral form until it progresses to include a myelopathy, leading to the label of cervical spondylotic myelopathy. Second, this bilaterally symmetric presentation may be misdiagnosed as the motor neuron disease variant termed Vulpian– Bernhardt syndrome, brachial amyotrophic diplegia, flail arm [FA], or man in the barrel syndrome [22]. The very early stages of FA may be
clinically indistinguishable from CSA; however, most patients with FA develop symptoms beyond the arms by 36 months [22]. In our patient, the total absence of bulbar or lower limb signs or symptoms after almost 7 years militated against FA. MR imaging bore all the earmarks of advanced spondylosis including pronounced stenosis with cord compression and intramedullary necrosis, as well as multilevel bilateral nerve root compressions. These features, in conjunction with the clinical picture, unequivocally substantiate the diagnosis of CSA. The total absence of acute denervation on electromyography excludes the extraordinarily remote possibility of a concomitant, atypical FA. Physicians must be aware of this bilaterally symmetric form of CSA in order to avoid diagnostic error or delay. Early diagnosis of CSA is crucial, underscored by reports of significant improvement with timely decompression, probably due to the presence of functionally reversible AH motor nuclei and nerve root fibers [10]. This finding is not negated by the fact that specific treatment options remain controversial as some authors advocate anterior decompression, [8,10] and others recommend a posterior approach [11,15]. Early intervention is further supported by evidence that patients harboring VNR compression without AH necrosis have a superior outcome regardless of the surgical approach, [8,15] and even with cord compression surgery appears beneficial if performed before development of intramedullary pathology [10]. This comports with the postoperative outcome findings in patients with cervical spondylotic myelopathy [23]. Indeed, there appears to be a narrow window of opportunity for surgical management. We propose expanding the generally accepted definition of CSA to include this bilaterally symmetric form of disease, thereby limiting diagnostic error or delay. Additionally, based on our case and a review of the literature, strict adherence to the proximal–distal distinction should be avoided since it is commonly blurred. 4. Conclusion Bilaterally symmetric CSA with blurring of the proximal–distal distinction is probably under-recognized or misdiagnosed due to a misperception that the disease is unilateral, and limited to either proximal or distal musculature. This novel presentation warrants expanding the traditionally accepted definition of CSA. Acknowledgement We thank the patient for cooperating and providing personal medical information in our preparation of this report. References [1] Brain WR, Northfield D, Wilkinson M. The neurological manifestations of cervical spondylosis. Brain 1952;75:187–225. [2] Keegan JJ. The cause of dissociated motor loss in the upper extremities with cervical spondylosis. J Neurosurg 1965;23:528–36. [3] Crandall PH, Batzdorf U. Cervical spondylotic myelopathy. J Neurosurg 1966;25: 57–66. [4] Yanagi T, Kato H, Sobue I. Clinical characteristics of cervical spondylotic amyotrophy. Clin Neurol (Rinsho Shinkeigaku) 1976;16:520–8. [5] Tsuboi Y, Tokumaru Y, Hirayama K. Clinical difference between “proximal” and “distal” type of cervical spondylotic amyotrophy. Clin Neurol (Rinsho Shinkeigaku) 1995;35:147–52. [6] Tamura M, Shinbo S, Ogawa K, Tamiya T, Takasu T. The clinical features of cervical spondylosis with boule musculaire. Clin Neurol (Rinsho Shinkeigaku) 1999;39 (11):1097–103. [7] Taguchi Y, Takashima S, Tanaka K. Boule musculaire associated with cervical spondylosis. Int Med 2007;46(6):329. [8] Shinomiya K, Komori H, Matsuoka T, Mutoh N, Furuya K. Neuroradiologic and electrophysiologic assessment of cervical spondylotic amyotrophy. Spine 1994;19 (1):21–5. [9] Kameyama T, Tetsuo A, Yanagi T, Keizo Y, Sobue G. Cervical spondylotic amyotrophy: magnetic resonance imaging demonstration of intrinsic cord pathology. Spine 1998;23(4):448–52.
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