J Neurosurg Spine 20:191–195, 2014 ©AANS, 2014
A severe case of Hirayama disease successfully treated by anterior cervical fusion Case report Igor Paredes, M.D.,1 Jesus Esteban, Ph.D., 2 Ana Ramos, Ph.D., 3 Pedro Gonzalez, M.D.,1 and Juan José Rivas, Ph.D.1 1 Neurosurgery Service, 2Neurology Service, and 3Neuroradiology Service, 12 de Octubre University Hospital, Madrid, Spain
Hirayama disease, or juvenile amyotrophy of distal upper extremity, is a benign, self-limiting cervical myelopathy consisting of selective unilateral weakness of the hand and forearm. The weakness slowly progresses until spontaneous arrest occurs within 5 years of onset. The condition predominantly affects Asian males and is thought to be secondary to spinal cord compression during neck flexion, because of a forward displacement of the posterior dural sac. The authors present what is to their knowledge the first reported case of a Caucasian male with a severe form of Hirayama disease, suffering from weakness of the leg as well as the forearm. An abnormal range of cervical flexion was observed at the C5–6 level. The patient was successfully treated by anterior cervical discectomy and fusion. (http://thejns.org/doi/abs/10.3171/2013.10.SPINE13508)
Key Words • Hirayama • juvenile amyotrophy of distal upper extremity • cervical flexion myelopathy • cervical flexion MRI • discectomy and fusion • abnormal range of cervical flexion
J
amyotrophy of distal upper extremity, also known as Hirayama disease, is a benign, self-limiting cervical myelopathy first brought to attention by Hirayama11 in 1959. Over the past 50 years, with the advent of MRI, several researchers have established this illness as a different entity from the motor neuron diseases.6–10,13,17,25,26 It has been characterized not as a primary disease of motor neurons, but as a myelopathy secondary to spinal cord compression during cervical flexion. The clinical features of Hirayama disease are: 1) asymmetrical weakness of the distal upper extremities, with atrophy of the thenar and hypothenar eminence and relative sparing of the brachioradialis muscle (oblique amyotrophy); 2) cold paresis (worsening of the weakness and distal tremor with cold); 3) lack of sensory, autonomic, or cranial nerve signs or symptoms; 4) insidious onset at the second to third decades of life (15–25 years), predominantly in males, with slow worsening over a variable period of time (mean 5 years)31 and subsequent spontaneous arrest of progression; and 5) usually sporadic occurrence (although familial cases have been reported).1,3,14,23 Radiological findings are essential for the diagnosis of Hirayama disease. Neutral and flexion cervical MRI uvenile
Abbreviation used in this paper: EMG = electromyography.
J Neurosurg: Spine / Volume 20 / February 2014
shows asymmetrical atrophy of the spinal cord, forward displacement of the posterior dural sac with neck flexion, and thus, secondary cord compression against the posterior wall of the vertebral body.6,15,16,21,27,30 Since neck flexion was recognized as a possible cause of the disease, several therapies have proved their utility, shortening the progression period and even improving the patient’s strength. Wearing a cervical collar is the most common conservative therapy. For cases in which the disease progresses despite conservative treatment, several surgical options have been used: posterior decompression with dural sac augmentation,2 with and without fusion, anterior decompression and fusion, and combinations of these methods. Which is the most effective is still a matter of debate. We are presenting a case of Hirayama disease with lower-extremity signs and symptoms, which was successfully treated with anterior discectomy and fusion alone.
Case Report
A previously healthy 19-year-old Caucasian male presented with a 2-year history of insidious progressive This article contains some figures that are displayed in color online but in black-and-white in the print edition.
191
I. Paredes et al. weakness of the right distal upper limb. The weakness was already stable, and it had not progressed over the last several months. He reported a slow progressive weakness of the proximal lower ipsilateral limb, and this was what had brought him to consult a neurologist. He also reported that his condition worsened with the cold. There was no family history of neuromuscular disease. At physical examination, oblique atrophy was obvious (atrophy of the thenar and hypothenar eminences and of the cubital border of the forearm, with relative sparing of the brachioradialis muscle), and the patient had severe weakness of the intrinsic musculature of the hand (0/5). His wrist flexion and extension and his elbow extension were also affected. He had mild weakness of hip flexion and knee extension in the right lower limb but was still able to walk. The patient’s deep tendon reflexes were normal in the upper limb and the left foot, but were brisk in the affected lower limb. He had a positive Babinski sign on the right. No sensory alterations were present, and the cranial nerves were unaffected. No other abnormalities were found on physical examination. Complete blood counts, blood chemistry analysis, and urinalysis revealed nothing unusual. Electromyography (EMG) showed acute over chronic denervation of the right interossei dorsalis manus muscles and chronic reinnervative changes in the left abductor pollicis brevis, flexor pollicis longus, and flexor digitorum profundus. The ulnar and median nerve conduction velocities were within normal limits. EMG over the tibialis anterior muscle showed mild acute denervation changes, such as spontaneous potentials, without conduction velocity abnormalities. Cervical MRI in a neutral neck position depicted a normal-size spinal canal, with a loss of normal cervical lordosis. The spinal cord showed atrophic changes at the C5–6 level, with signal hyperintensity on T2-weighted images extending 1 level above and below (Fig. 1). Loss of attachment of the posterior dura was not seen on any image. Images obtained with the neck flexed showed forward displacement of the posterior dural sac and excessive angulation of the spine at C5–6 level, causing compression of the cord (Fig. 2). The forward displacement of the dural sac created a crescent-shaped space between the dura and the laminae, with a large flow void. This space enhanced strongly after gadolinium contrast administration. After considering the findings, a severe form of Hirayama disease was diagnosed. Considering the clinical course of the disease and that a conservative treatment had been tried unsuccessfully at the referring hospital, the decision was made to treat the patient surgically. Based on the excessive angulation observed at the C5–6 level (Fig. 2), an anterior C5–6 discectomy was performed, a polyetheretherketone (PEEK) cage was placed, and a plate was screwed to the vertebral bodies, completing an anterior fusion procedure. The total surgical time was less than 50 minutes, and the blood loss was insignificant. The patient’s postoperative course was uneventful. The neurological examination findings were unchanged, and the patient was discharged 48 hours after surgery. The disc was sent to the pathology laboratory, and no abnormality was found. 192
Fig. 1. Preoperative MR images. Left: Neutral-position sagittal T2-weighted image showing spinal cord atrophy at the C5–6 level. Normal spinal canal size is appreciated. No loss of attachment of the posterior dura is evident. Right: Sagittal T2-weighted image obtained in flexion showing forward displacement of the posterior dura, with abnormal flexion of the C5–6 segment and spinal cord compression. A large flow void can be seen in the crescent-shaped space created between the dura and the laminae.
Two months after the procedure the patient presented with subjective improvement of his lower leg strength. A cervical MRI with the neck flexed and extended was performed 1 month after the procedure (Fig. 3). The posterior dural sac no longer moved forward with neck flexion, and
Fig. 2. Midsagittal T2-weighted cervical MR image obtained with the neck in flexion. Segmental angles have been calculated by drawing a line linking the middle height of the posterior and anterior wall of the vertebral bodies and extending them until they cross. The C5–6 angle is almost double that of the 2 other measured levels.
J Neurosurg: Spine / Volume 20 / February 2014
Severe Hirayama disease treated by discectomy and fusion
Fig. 3. Postoperative MR images (obtained 1 month after the procedure). Left: Sagittal T2-weighted image obtained in extension showing no change from the preoperative findings. Right: Sagittal T2-weighted image obtained in flexion. No abnormal flexion, no forward displacement, and no contact between the spinal cord and the posterior wall of the vertebral bodies is evident. Spinal cord compression is no longer present.
there was no contact between the spinal cord and posterior wall of the vertebral bodies; thus, no compression was observed. Six months after the surgery a CT scan was performed, showing bone bridge formation at the surgically treated level (Fig. 4). As of this writing, a year after the surgery, the patient’s leg has regained its full strength, gait is normal, and upper limb is unchanged. EMG shows no abnormalities in the lower extremities, but does show chronic denervation changes in the upper limb.
Discussion
Hirayama disease was initially described in 1959 by K. Hirayama.11 The author described it as a monomyelic disease, affecting only one limb, without impairment of sensory pathways or cranial nerve or brain function. However, the largest series reported in the English literature31 describes electrophysiological studies depicting a bilateral impairment (although asymmetrical) in up to 95% of the cases, and a lower limb impairment in 3 of 195 cases. Nevertheless, patients presenting with bilateral paresis are rare, and patients presenting with lower ipsilateral limb paresis are even rarer.24 In fact, to the best of our knowledge, this is the first report of a Caucasian male with this severe form of Hirayama disease. The first autopsy of a patient with Hirayama disease was performed in 1982 by Hirayama,8 and the findings suggested chronic ischemic injury to the anterior horn of the cord. He described the condition as a flexion myelopathy and proposed a misbalance between the growth of the spinal cord and the spine as the cause. The anterior horn is the area most vulnerable to ischemic insults; thus it was proposed that chronic repetitive compressions of the cord J Neurosurg: Spine / Volume 20 / February 2014
Fig. 4. Midsagittal CT scan of the cervical spine obtained 6 months after the procedure. New bone bridging the C5–6 space can be appreciated.
due to the forward displacement of the posterior dural sac during neck flexion caused perfusion impairment and permanent injury. The male predominance would support the idea of a misbalance in growth, because the growth spurt is usually more marked in males than in females, and the typical age at onset of Hirayama disease is 2 years after the beginning of the growth spurt. The observation that in older patients, once the progression is arrested, the forward shifting of the dura is no longer appreciated supports it as a causative factor. Evidence from EMG studies helps to differentiate Hirayama disease from other motor neuron diseases. EMG typically shows the presence of neurogenic lesions in all affected muscles with spontaneous potentials, a prolonged duration or augmentation of amplitude in motor unit potentials, or an incomplete pattern of recruitment.5,18–20,28 Electrophysiological studies performed during neck flexion failed to prove abnormalities related to 193
I. Paredes et al. neck posture,20 although those studies were performed at the plateau phase of the disease, and there was no mention of how long flexion was maintained. The diagnosis of the disease is strongly based on MRI findings in the flexed position of the neck. There are some subtle changes in the neutral MRI that should raise the suspicion of the condition, as described by Huang and Chen:13 asymmetrical atrophy of the cord and loss of attachment of the posterior sac to the lamina. It is also important to note that the changes in the flexed position vary with the degree of flexion, and they might not be remarkable with the neck flexed less than 25°.12 Even though the forward shift of the dura in the flexed position is the most striking finding, it might be found in up to 40% of healthy young males,15 so the diagnosis cannot be made exclusively on this basis. It is also common to find large flow voids in the crescent-shaped space created due to the forward shifting of the dura. Those flow voids correspond to an engorged venous epidural plexus. Patel et al.22 reported a case in which venography was performed and the epidural pressure was monitored. The lack of pressure change with neck flexion suggested that the engorgement of the plexus was a passive event rather than a causative factor. Xu et al.29 have recently shown that there is a marked abnormality in the range of motion of the cervical spine in patients with Hirayama disease, both globally and by segment. They compared findings in 31 patients with Hirayama disease with findings in 40 healthy subjects of the same age. They found that the angle of flexion was greater in the patients with Hirayama disease than in the controls, especially at the C5–6 level, where they found a mean angulation of 11.95° compared with the 5.36° that was the mean value obtained in the healthy subjects. (To measure the angle an imaginary line is formed by linking the middle point of the posterior and anterior walls of the vertebral body. The angle is measured where the extended lines of adjacent levels cross.) Our patient had an angulation of 11.78° at C5–6, 6.1° at C4–5, and 5.8° at C3–4 (Fig. 2). This finding drove us to operate on the C5–6 segment, and the good result obtained suggests that an excessive range of motion of the cervical spine could be a causative factor in the disease. Treatment of Hirayama disease is a controversial issue. Because the progression will arrest spontaneously within 5 years of symptom onset in the majority of cases31 and the use of a cervical collar has been shown to shorten that period, some authors advocate conservative treatment.26 In some cases, however, the patient’s condition worsens despite the use of the cervical collar. Moreover, the use of a cervical collar has only proven effective in stabilizing the patient’s condition, not improving it. Therefore, an increasing number of physicians advocate surgical treatment.2,4,17,22 Anterior and posterior decompressive procedures—with or without duraplasty and with or without fusion—have been used, 2,17 producing arrest of the progression and even improvement of patients’ previous symptoms. However, a randomized controlled trial is lacking, and no recommendations about the type of surgery, its timing, or even its adequacy can be made. The good result obtained in our case suggests that an exces194
sive range of flexion of the cervical spine might play a key role in the pathophysiology of the disease. Thus, a simple and safe anterior fusion procedure could be the best choice.
Conclusions
We present what is to our knowledge the first case of a Caucasian male with a severe form of Hirayama disease. The disease presented as stabilized paresis of the right upper limb and progressive paresis of the right lower limb. The patient was treated with anterior discectomy and fusion. His lower limb function improved, with resolution of symptoms in that limb, and his upper limb function stabilized. Therefore we believe that anterior fusion might be the best choice of treatment. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Paredes. Acquisition of data: Paredes, Esteban, Ramos. Analysis and interpretation of data: Paredes, Rivas. Drafting the article: Paredes. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Paredes. References 1. Andreadou E, Christodoulou K, Manta P, Karandreas N, Loukaidis P, Sfagos C, et al: Familial asymmetric distal upper limb amyotrophy (Hirayama disease): report of a Greek family. Neurologist 15:156–160, 2009 2. Arrese I, Rivas JJ, Esteban J, Ramos A, Lobato RD: A case of Hirayama disease treated with laminectomy and duraplasty without spinal fusion. Neurocirugia (Astur) 20:555–558, 2009 3. Atchayaram N, Vasudev MK, Goel G: Familial monomelic amyotrophy (Hirayama disease): two brothers with classical flexion induced dynamic changes of the cervical dural sac. Neurol India 57:810–812, 2009 4. Chiba S, Yonekura K, Nonaka M, Imai T, Matumoto H, Wada T: Advanced Hirayama disease with successful improvement of activities of daily living by operative reconstruction. Intern Med 43:79–81, 2004 5. Guo XM, Qin XY, Huang C: Neuroelectrophysiological characteristics of Hirayama disease: report of 14 cases. Chin Med J (Engl) 125:2440–2443, 2012 6. Hassan KM, Sahni H, Jha A: Clinical and radiological profile of Hirayama disease: a flexion myelopathy due to tight cervical dural canal amenable to collar therapy. Ann Indian Acad Neurol 15:106–112, 2012 7. Hirayama K: Juvenile muscular atrophy of distal upper extremity (Hirayama disease). Intern Med 39:283–290, 2000 8. Hirayama K: Juvenile muscular atrophy of distal upper extremity (Hirayama disease): focal cervical ischemic poliomyelopathy. Neuropathology 20 (Suppl):S91–S94, 2000 9. Hirayama K: [Juvenile muscular atrophy of unilateral upper extremity (Hirayama disease)—half-century progress and establishment since its discovery.] Brain Nerve 60:17–29, 2008 (Jpn) 10. Hirayama K, Tokumaru Y: Cervical dural sac and spinal cord in juvenile muscular atrophy of distal upper extremity. Neurology 54:1922–1926, 2000 11. Hirayama K, Toyokura Y, Tsubaki T: [Juvenile muscular atro-
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Severe Hirayama disease treated by discectomy and fusion phy of unilateral upper extremity: a new clinical entity.] Psychiatr Neurol Jpn 61:2190–2198, 1959 (Jpn) 12. Hou C, Han H, Yang X, Xu X, Gao H, Fan D, et al: How does the neck flexion affect the cervical MRI features of Hirayama disease? Neurol Sci 33:1101–1105, 2012 13. Huang YL, Chen CJ: Hirayama disease. Neuroimaging Clin N Am 21:939–950, ix–x, 2011 14. Kajikawa H, Kokubo Y, Taniguchi A, Naito Y, Kuzuhara S: Juvenile muscular atrophy of the distal upper extremity (Hirayama disease) in two lanky look-alike brothers. Neurologist 15:220–222, 2009 15. Lai V, Wong YC, Poon WL, Yuen MK, Fu YP, Wong OW: Forward shifting of posterior dural sac during flexion cervical magnetic resonance imaging in Hirayama disease: an initial study on normal subjects compared to patients with Hirayama disease. Eur J Radiol 80:724–728, 2011 16. Lehman VT, Luetmer PH, Sorenson EJ, Carter RE, Gupta V, Fletcher GP, et al: Cervical spine MR imaging findings of patients with Hirayama disease in North America: a multisite study. AJNR Am J Neuroradiol 34:451–456, 2013 17. Lin MS, Kung WM, Chiu WT, Lyu RK, Chen CJ, Chen TY: Hirayama disease. Clinical article. J Neurosurg Spine 12: 629–634, 2010 18. Lyu RK, Huang YC, Wu YR, Kuo HC, Ro LS, Chen CM, et al: Electrophysiological features of Hirayama disease. Muscle Nerve 44:185–190, 2011 19. Misra UK, Kalita J: Central motor conduction in Hirayama disease. Electroencephalogr Clin Neurophysiol 97:73–76, 1995 20. Misra UK, Kalita J, Mishra VN, Phadke RV, Hadique A: Effect of neck flexion on F wave, somatosensory evoked potentials, and magnetic resonance imaging in Hirayama disease. J Neurol Neurosurg Psychiatry 77:695–698, 2006 21. Parihar A, Khurana N, Aga P, Singh R, Garg RK: Role of dynamic MRI study in Hirayama disease. Ann Indian Acad Neurol 14:138–139, 2011 22. Patel TR, Chiocca EA, Freimer ML, Christoforidis GA: Lack of epidural pressure change with neck flexion in a patient with Hirayama disease: case report. Neurosurgery 64:E1196–E1197, 2009
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23. Robberecht W, Aguirre T, Van den Bosch L, Theys P, Nees H, Cassiman JJ, et al: Familial juvenile focal amyotrophy of the upper extremity (Hirayama disease). Superoxide dismutase 1 genotype and activity. Arch Neurol 54:46–50, 1997 24. Sakai K, Ono K, Okamoto Y, Murakami H, Yamada M: Cervical flexion myelopathy in a patient showing apparent long tract signs: a severe form of Hirayama disease. Joint Bone Spine 78:316–318, 2011 25. Tashiro K, Kikuchi S, Itoyama Y, Tokumaru Y, Sobue G, Mukai E, et al: Nationwide survey of juvenile muscular atrophy of distal upper extremity (Hirayama disease) in Japan. Amyotroph Lateral Scler 7:38–45, 2006 26. Tokumaru Y, Hirayama K: [Cervical collar therapy for juvenile muscular atrophy of distal upper extremity (Hirayama disease): results from 38 cases.] Rinsho Shinkeigaku 41:173– 178, 2001 (Jpn) 27. Vargas MC, Castillo M: Magnetic resonance imaging in Hirayama disease. J Radiol Case Rep 5:17–23, 2011 28. Wang XN, Cui LY, Liu MS, Guan YZ, Li BH, Du H: A clinical neurophysiology study of Hirayama disease. Chin Med J (Engl) 125:1115–1120, 2012 29. Xu X, Han H, Gao H, Hou C, Fan D, Fu Y, et al: The increased range of cervical flexed motion detected by radiographs in Hirayama disease. Eur J Radiol 78:82–86, 2011 30. Yin B, Liu L, Geng DY: Features of Hirayama disease on fully flexed position cervical MRI. J Int Med Res 39:222–228, 2011 31. Zhou B, Chen L, Fan D, Zhou D: Clinical features of Hirayama disease in mainland China. Amyotroph Lateral Scler 11: 133–139, 2010
Manuscript submitted June 3, 2013. Accepted October 29, 2013. Please include this information when citing this paper: published online November 29, 2013; DOI: 10.3171/2013.10.SPINE13508. Address correspondence to: Igor Paredes, M.D., Hospital 12 de Octubre, Avenida de Córdoba s/n, Madrid 28041, Spain. email: [email protected].
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A severe case of Hirayama disease successfully treated by anterior cervical fusion Case report Igor Paredes, M.D.,1 Jesus Esteban, Ph.D., 2 Ana Ramos, Ph.D., 3 Pedro Gonzalez, M.D.,1 and Juan José Rivas, Ph.D.1 1 Neurosurgery Service, 2Neurology Service, and 3Neuroradiology Service, 12 de Octubre University Hospital, Madrid, Spain
Hirayama disease, or juvenile amyotrophy of distal upper extremity, is a benign, self-limiting cervical myelopathy consisting of selective unilateral weakness of the hand and forearm. The weakness slowly progresses until spontaneous arrest occurs within 5 years of onset. The condition predominantly affects Asian males and is thought to be secondary to spinal cord compression during neck flexion, because of a forward displacement of the posterior dural sac. The authors present what is to their knowledge the first reported case of a Caucasian male with a severe form of Hirayama disease, suffering from weakness of the leg as well as the forearm. An abnormal range of cervical flexion was observed at the C5–6 level. The patient was successfully treated by anterior cervical discectomy and fusion. (http://thejns.org/doi/abs/10.3171/2013.10.SPINE13508)
Key Words • Hirayama • juvenile amyotrophy of distal upper extremity • cervical flexion myelopathy • cervical flexion MRI • discectomy and fusion • abnormal range of cervical flexion
J
amyotrophy of distal upper extremity, also known as Hirayama disease, is a benign, self-limiting cervical myelopathy first brought to attention by Hirayama11 in 1959. Over the past 50 years, with the advent of MRI, several researchers have established this illness as a different entity from the motor neuron diseases.6–10,13,17,25,26 It has been characterized not as a primary disease of motor neurons, but as a myelopathy secondary to spinal cord compression during cervical flexion. The clinical features of Hirayama disease are: 1) asymmetrical weakness of the distal upper extremities, with atrophy of the thenar and hypothenar eminence and relative sparing of the brachioradialis muscle (oblique amyotrophy); 2) cold paresis (worsening of the weakness and distal tremor with cold); 3) lack of sensory, autonomic, or cranial nerve signs or symptoms; 4) insidious onset at the second to third decades of life (15–25 years), predominantly in males, with slow worsening over a variable period of time (mean 5 years)31 and subsequent spontaneous arrest of progression; and 5) usually sporadic occurrence (although familial cases have been reported).1,3,14,23 Radiological findings are essential for the diagnosis of Hirayama disease. Neutral and flexion cervical MRI uvenile
Abbreviation used in this paper: EMG = electromyography.
J Neurosurg: Spine / Volume 20 / February 2014
shows asymmetrical atrophy of the spinal cord, forward displacement of the posterior dural sac with neck flexion, and thus, secondary cord compression against the posterior wall of the vertebral body.6,15,16,21,27,30 Since neck flexion was recognized as a possible cause of the disease, several therapies have proved their utility, shortening the progression period and even improving the patient’s strength. Wearing a cervical collar is the most common conservative therapy. For cases in which the disease progresses despite conservative treatment, several surgical options have been used: posterior decompression with dural sac augmentation,2 with and without fusion, anterior decompression and fusion, and combinations of these methods. Which is the most effective is still a matter of debate. We are presenting a case of Hirayama disease with lower-extremity signs and symptoms, which was successfully treated with anterior discectomy and fusion alone.
Case Report
A previously healthy 19-year-old Caucasian male presented with a 2-year history of insidious progressive This article contains some figures that are displayed in color online but in black-and-white in the print edition.
191
I. Paredes et al. weakness of the right distal upper limb. The weakness was already stable, and it had not progressed over the last several months. He reported a slow progressive weakness of the proximal lower ipsilateral limb, and this was what had brought him to consult a neurologist. He also reported that his condition worsened with the cold. There was no family history of neuromuscular disease. At physical examination, oblique atrophy was obvious (atrophy of the thenar and hypothenar eminences and of the cubital border of the forearm, with relative sparing of the brachioradialis muscle), and the patient had severe weakness of the intrinsic musculature of the hand (0/5). His wrist flexion and extension and his elbow extension were also affected. He had mild weakness of hip flexion and knee extension in the right lower limb but was still able to walk. The patient’s deep tendon reflexes were normal in the upper limb and the left foot, but were brisk in the affected lower limb. He had a positive Babinski sign on the right. No sensory alterations were present, and the cranial nerves were unaffected. No other abnormalities were found on physical examination. Complete blood counts, blood chemistry analysis, and urinalysis revealed nothing unusual. Electromyography (EMG) showed acute over chronic denervation of the right interossei dorsalis manus muscles and chronic reinnervative changes in the left abductor pollicis brevis, flexor pollicis longus, and flexor digitorum profundus. The ulnar and median nerve conduction velocities were within normal limits. EMG over the tibialis anterior muscle showed mild acute denervation changes, such as spontaneous potentials, without conduction velocity abnormalities. Cervical MRI in a neutral neck position depicted a normal-size spinal canal, with a loss of normal cervical lordosis. The spinal cord showed atrophic changes at the C5–6 level, with signal hyperintensity on T2-weighted images extending 1 level above and below (Fig. 1). Loss of attachment of the posterior dura was not seen on any image. Images obtained with the neck flexed showed forward displacement of the posterior dural sac and excessive angulation of the spine at C5–6 level, causing compression of the cord (Fig. 2). The forward displacement of the dural sac created a crescent-shaped space between the dura and the laminae, with a large flow void. This space enhanced strongly after gadolinium contrast administration. After considering the findings, a severe form of Hirayama disease was diagnosed. Considering the clinical course of the disease and that a conservative treatment had been tried unsuccessfully at the referring hospital, the decision was made to treat the patient surgically. Based on the excessive angulation observed at the C5–6 level (Fig. 2), an anterior C5–6 discectomy was performed, a polyetheretherketone (PEEK) cage was placed, and a plate was screwed to the vertebral bodies, completing an anterior fusion procedure. The total surgical time was less than 50 minutes, and the blood loss was insignificant. The patient’s postoperative course was uneventful. The neurological examination findings were unchanged, and the patient was discharged 48 hours after surgery. The disc was sent to the pathology laboratory, and no abnormality was found. 192
Fig. 1. Preoperative MR images. Left: Neutral-position sagittal T2-weighted image showing spinal cord atrophy at the C5–6 level. Normal spinal canal size is appreciated. No loss of attachment of the posterior dura is evident. Right: Sagittal T2-weighted image obtained in flexion showing forward displacement of the posterior dura, with abnormal flexion of the C5–6 segment and spinal cord compression. A large flow void can be seen in the crescent-shaped space created between the dura and the laminae.
Two months after the procedure the patient presented with subjective improvement of his lower leg strength. A cervical MRI with the neck flexed and extended was performed 1 month after the procedure (Fig. 3). The posterior dural sac no longer moved forward with neck flexion, and
Fig. 2. Midsagittal T2-weighted cervical MR image obtained with the neck in flexion. Segmental angles have been calculated by drawing a line linking the middle height of the posterior and anterior wall of the vertebral bodies and extending them until they cross. The C5–6 angle is almost double that of the 2 other measured levels.
J Neurosurg: Spine / Volume 20 / February 2014
Severe Hirayama disease treated by discectomy and fusion
Fig. 3. Postoperative MR images (obtained 1 month after the procedure). Left: Sagittal T2-weighted image obtained in extension showing no change from the preoperative findings. Right: Sagittal T2-weighted image obtained in flexion. No abnormal flexion, no forward displacement, and no contact between the spinal cord and the posterior wall of the vertebral bodies is evident. Spinal cord compression is no longer present.
there was no contact between the spinal cord and posterior wall of the vertebral bodies; thus, no compression was observed. Six months after the surgery a CT scan was performed, showing bone bridge formation at the surgically treated level (Fig. 4). As of this writing, a year after the surgery, the patient’s leg has regained its full strength, gait is normal, and upper limb is unchanged. EMG shows no abnormalities in the lower extremities, but does show chronic denervation changes in the upper limb.
Discussion
Hirayama disease was initially described in 1959 by K. Hirayama.11 The author described it as a monomyelic disease, affecting only one limb, without impairment of sensory pathways or cranial nerve or brain function. However, the largest series reported in the English literature31 describes electrophysiological studies depicting a bilateral impairment (although asymmetrical) in up to 95% of the cases, and a lower limb impairment in 3 of 195 cases. Nevertheless, patients presenting with bilateral paresis are rare, and patients presenting with lower ipsilateral limb paresis are even rarer.24 In fact, to the best of our knowledge, this is the first report of a Caucasian male with this severe form of Hirayama disease. The first autopsy of a patient with Hirayama disease was performed in 1982 by Hirayama,8 and the findings suggested chronic ischemic injury to the anterior horn of the cord. He described the condition as a flexion myelopathy and proposed a misbalance between the growth of the spinal cord and the spine as the cause. The anterior horn is the area most vulnerable to ischemic insults; thus it was proposed that chronic repetitive compressions of the cord J Neurosurg: Spine / Volume 20 / February 2014
Fig. 4. Midsagittal CT scan of the cervical spine obtained 6 months after the procedure. New bone bridging the C5–6 space can be appreciated.
due to the forward displacement of the posterior dural sac during neck flexion caused perfusion impairment and permanent injury. The male predominance would support the idea of a misbalance in growth, because the growth spurt is usually more marked in males than in females, and the typical age at onset of Hirayama disease is 2 years after the beginning of the growth spurt. The observation that in older patients, once the progression is arrested, the forward shifting of the dura is no longer appreciated supports it as a causative factor. Evidence from EMG studies helps to differentiate Hirayama disease from other motor neuron diseases. EMG typically shows the presence of neurogenic lesions in all affected muscles with spontaneous potentials, a prolonged duration or augmentation of amplitude in motor unit potentials, or an incomplete pattern of recruitment.5,18–20,28 Electrophysiological studies performed during neck flexion failed to prove abnormalities related to 193
I. Paredes et al. neck posture,20 although those studies were performed at the plateau phase of the disease, and there was no mention of how long flexion was maintained. The diagnosis of the disease is strongly based on MRI findings in the flexed position of the neck. There are some subtle changes in the neutral MRI that should raise the suspicion of the condition, as described by Huang and Chen:13 asymmetrical atrophy of the cord and loss of attachment of the posterior sac to the lamina. It is also important to note that the changes in the flexed position vary with the degree of flexion, and they might not be remarkable with the neck flexed less than 25°.12 Even though the forward shift of the dura in the flexed position is the most striking finding, it might be found in up to 40% of healthy young males,15 so the diagnosis cannot be made exclusively on this basis. It is also common to find large flow voids in the crescent-shaped space created due to the forward shifting of the dura. Those flow voids correspond to an engorged venous epidural plexus. Patel et al.22 reported a case in which venography was performed and the epidural pressure was monitored. The lack of pressure change with neck flexion suggested that the engorgement of the plexus was a passive event rather than a causative factor. Xu et al.29 have recently shown that there is a marked abnormality in the range of motion of the cervical spine in patients with Hirayama disease, both globally and by segment. They compared findings in 31 patients with Hirayama disease with findings in 40 healthy subjects of the same age. They found that the angle of flexion was greater in the patients with Hirayama disease than in the controls, especially at the C5–6 level, where they found a mean angulation of 11.95° compared with the 5.36° that was the mean value obtained in the healthy subjects. (To measure the angle an imaginary line is formed by linking the middle point of the posterior and anterior walls of the vertebral body. The angle is measured where the extended lines of adjacent levels cross.) Our patient had an angulation of 11.78° at C5–6, 6.1° at C4–5, and 5.8° at C3–4 (Fig. 2). This finding drove us to operate on the C5–6 segment, and the good result obtained suggests that an excessive range of motion of the cervical spine could be a causative factor in the disease. Treatment of Hirayama disease is a controversial issue. Because the progression will arrest spontaneously within 5 years of symptom onset in the majority of cases31 and the use of a cervical collar has been shown to shorten that period, some authors advocate conservative treatment.26 In some cases, however, the patient’s condition worsens despite the use of the cervical collar. Moreover, the use of a cervical collar has only proven effective in stabilizing the patient’s condition, not improving it. Therefore, an increasing number of physicians advocate surgical treatment.2,4,17,22 Anterior and posterior decompressive procedures—with or without duraplasty and with or without fusion—have been used, 2,17 producing arrest of the progression and even improvement of patients’ previous symptoms. However, a randomized controlled trial is lacking, and no recommendations about the type of surgery, its timing, or even its adequacy can be made. The good result obtained in our case suggests that an exces194
sive range of flexion of the cervical spine might play a key role in the pathophysiology of the disease. Thus, a simple and safe anterior fusion procedure could be the best choice.
Conclusions
We present what is to our knowledge the first case of a Caucasian male with a severe form of Hirayama disease. The disease presented as stabilized paresis of the right upper limb and progressive paresis of the right lower limb. The patient was treated with anterior discectomy and fusion. His lower limb function improved, with resolution of symptoms in that limb, and his upper limb function stabilized. Therefore we believe that anterior fusion might be the best choice of treatment. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Paredes. Acquisition of data: Paredes, Esteban, Ramos. Analysis and interpretation of data: Paredes, Rivas. Drafting the article: Paredes. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Paredes. References 1. Andreadou E, Christodoulou K, Manta P, Karandreas N, Loukaidis P, Sfagos C, et al: Familial asymmetric distal upper limb amyotrophy (Hirayama disease): report of a Greek family. Neurologist 15:156–160, 2009 2. Arrese I, Rivas JJ, Esteban J, Ramos A, Lobato RD: A case of Hirayama disease treated with laminectomy and duraplasty without spinal fusion. Neurocirugia (Astur) 20:555–558, 2009 3. Atchayaram N, Vasudev MK, Goel G: Familial monomelic amyotrophy (Hirayama disease): two brothers with classical flexion induced dynamic changes of the cervical dural sac. Neurol India 57:810–812, 2009 4. Chiba S, Yonekura K, Nonaka M, Imai T, Matumoto H, Wada T: Advanced Hirayama disease with successful improvement of activities of daily living by operative reconstruction. Intern Med 43:79–81, 2004 5. Guo XM, Qin XY, Huang C: Neuroelectrophysiological characteristics of Hirayama disease: report of 14 cases. Chin Med J (Engl) 125:2440–2443, 2012 6. Hassan KM, Sahni H, Jha A: Clinical and radiological profile of Hirayama disease: a flexion myelopathy due to tight cervical dural canal amenable to collar therapy. Ann Indian Acad Neurol 15:106–112, 2012 7. Hirayama K: Juvenile muscular atrophy of distal upper extremity (Hirayama disease). Intern Med 39:283–290, 2000 8. Hirayama K: Juvenile muscular atrophy of distal upper extremity (Hirayama disease): focal cervical ischemic poliomyelopathy. Neuropathology 20 (Suppl):S91–S94, 2000 9. Hirayama K: [Juvenile muscular atrophy of unilateral upper extremity (Hirayama disease)—half-century progress and establishment since its discovery.] Brain Nerve 60:17–29, 2008 (Jpn) 10. Hirayama K, Tokumaru Y: Cervical dural sac and spinal cord in juvenile muscular atrophy of distal upper extremity. Neurology 54:1922–1926, 2000 11. Hirayama K, Toyokura Y, Tsubaki T: [Juvenile muscular atro-
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Severe Hirayama disease treated by discectomy and fusion phy of unilateral upper extremity: a new clinical entity.] Psychiatr Neurol Jpn 61:2190–2198, 1959 (Jpn) 12. Hou C, Han H, Yang X, Xu X, Gao H, Fan D, et al: How does the neck flexion affect the cervical MRI features of Hirayama disease? Neurol Sci 33:1101–1105, 2012 13. Huang YL, Chen CJ: Hirayama disease. Neuroimaging Clin N Am 21:939–950, ix–x, 2011 14. Kajikawa H, Kokubo Y, Taniguchi A, Naito Y, Kuzuhara S: Juvenile muscular atrophy of the distal upper extremity (Hirayama disease) in two lanky look-alike brothers. Neurologist 15:220–222, 2009 15. Lai V, Wong YC, Poon WL, Yuen MK, Fu YP, Wong OW: Forward shifting of posterior dural sac during flexion cervical magnetic resonance imaging in Hirayama disease: an initial study on normal subjects compared to patients with Hirayama disease. Eur J Radiol 80:724–728, 2011 16. Lehman VT, Luetmer PH, Sorenson EJ, Carter RE, Gupta V, Fletcher GP, et al: Cervical spine MR imaging findings of patients with Hirayama disease in North America: a multisite study. AJNR Am J Neuroradiol 34:451–456, 2013 17. Lin MS, Kung WM, Chiu WT, Lyu RK, Chen CJ, Chen TY: Hirayama disease. Clinical article. J Neurosurg Spine 12: 629–634, 2010 18. Lyu RK, Huang YC, Wu YR, Kuo HC, Ro LS, Chen CM, et al: Electrophysiological features of Hirayama disease. Muscle Nerve 44:185–190, 2011 19. Misra UK, Kalita J: Central motor conduction in Hirayama disease. Electroencephalogr Clin Neurophysiol 97:73–76, 1995 20. Misra UK, Kalita J, Mishra VN, Phadke RV, Hadique A: Effect of neck flexion on F wave, somatosensory evoked potentials, and magnetic resonance imaging in Hirayama disease. J Neurol Neurosurg Psychiatry 77:695–698, 2006 21. Parihar A, Khurana N, Aga P, Singh R, Garg RK: Role of dynamic MRI study in Hirayama disease. Ann Indian Acad Neurol 14:138–139, 2011 22. Patel TR, Chiocca EA, Freimer ML, Christoforidis GA: Lack of epidural pressure change with neck flexion in a patient with Hirayama disease: case report. Neurosurgery 64:E1196–E1197, 2009
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23. Robberecht W, Aguirre T, Van den Bosch L, Theys P, Nees H, Cassiman JJ, et al: Familial juvenile focal amyotrophy of the upper extremity (Hirayama disease). Superoxide dismutase 1 genotype and activity. Arch Neurol 54:46–50, 1997 24. Sakai K, Ono K, Okamoto Y, Murakami H, Yamada M: Cervical flexion myelopathy in a patient showing apparent long tract signs: a severe form of Hirayama disease. Joint Bone Spine 78:316–318, 2011 25. Tashiro K, Kikuchi S, Itoyama Y, Tokumaru Y, Sobue G, Mukai E, et al: Nationwide survey of juvenile muscular atrophy of distal upper extremity (Hirayama disease) in Japan. Amyotroph Lateral Scler 7:38–45, 2006 26. Tokumaru Y, Hirayama K: [Cervical collar therapy for juvenile muscular atrophy of distal upper extremity (Hirayama disease): results from 38 cases.] Rinsho Shinkeigaku 41:173– 178, 2001 (Jpn) 27. Vargas MC, Castillo M: Magnetic resonance imaging in Hirayama disease. J Radiol Case Rep 5:17–23, 2011 28. Wang XN, Cui LY, Liu MS, Guan YZ, Li BH, Du H: A clinical neurophysiology study of Hirayama disease. Chin Med J (Engl) 125:1115–1120, 2012 29. Xu X, Han H, Gao H, Hou C, Fan D, Fu Y, et al: The increased range of cervical flexed motion detected by radiographs in Hirayama disease. Eur J Radiol 78:82–86, 2011 30. Yin B, Liu L, Geng DY: Features of Hirayama disease on fully flexed position cervical MRI. J Int Med Res 39:222–228, 2011 31. Zhou B, Chen L, Fan D, Zhou D: Clinical features of Hirayama disease in mainland China. Amyotroph Lateral Scler 11: 133–139, 2010
Manuscript submitted June 3, 2013. Accepted October 29, 2013. Please include this information when citing this paper: published online November 29, 2013; DOI: 10.3171/2013.10.SPINE13508. Address correspondence to: Igor Paredes, M.D., Hospital 12 de Octubre, Avenida de Córdoba s/n, Madrid 28041, Spain. email: [email protected].
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