Journal http://jcn.sagepub.com/ of Child Neurology
Acute Motor-Sensory Axonal Neuropathy With Hyperreflexia in Guillain-Barré Syndrome Ayse Tosun, Siar Dursun, Utku Ogan Akyildiz, Seçil Oktay and Cengiz Tataroglu J Child Neurol published online 2 April 2014 DOI: 10.1177/0883073814528377 The online version of this article can be found at: http://jcn.sagepub.com/content/early/2014/04/01/0883073814528377
Published by: http://www.sagepublications.com
Additional services and information for Journal of Child Neurology can be found at: Email Alerts: http://jcn.sagepub.com/cgi/alerts Subscriptions: http://jcn.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - Apr 2, 2014 What is This?
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
Brief Communication
Acute Motor-Sensory Axonal Neuropathy With Hyperreflexia in Guillain-Barre´ Syndrome
Journal of Child Neurology 1-4 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0883073814528377 jcn.sagepub.com
Ays¸ e Tosun, MD2, S¸ iar Dursun, MD2, Utku Ogan Akyildiz, MD1, Sec¸il Oktay, MD2, and Cengiz Tatarog˘lu, MD1
Abstract Guillain-Barre´ syndrome is an acute inflammatory autoimmune polyradiculoneuritis. Progressive motor weakness and areflexia are essential for its diagnosis. Hyperreflexia has rarely been reported in the early healing period of Guillain-Barre´ syndrome following Campylobacter jejuni infection in patients with acute motor axonal neuropathy with antiganglioside antibody positivity. In this study, we report a 12-year-old girl presenting with complaints of inability to walk, numbness in hands and feet, and hyperactive deep tendon reflexes since the onset of the clinical picture, diagnosed with acute motor-sensory axonal neuropathy type of Guillain-Barre´ syndrome. Keywords Guillain-Barre´ syndrome, hyperreflexia Received December 29, 2013. Received revised February 25, 2014. Accepted for publication February 26, 2014.
Guillain-Barre´ syndrome is the most common cause of acquired polyneuropathies. The worldwide incidence has been reported to be 0.6 to 4 in 100 000.1 Guillain-Barre´ syndrome is an autoimmune clinical picture characterized with elevated protein levels without pleocytosis in cerebrospinal fluid; often ascending and symmetrical extremity paralysis; sensorial deficit of distal extremities; bulbar, facial, and ocular involvement of varying degrees; and loss of deep tendon reflexes following a viral upper respiratory tract infection, gastrointestinal infection, or vaccination.1,2 The term Guillain-Barre´ syndrome defines a heterogeneous group of diseases with different clinical features rather than a single disease. Guillain-Barre´ syndrome has 3 subtypes defined by electrophysiological and pathogenetic properties, including acute inflammatory demyelinating polyneuropathy, acute motor axonal neuropathy, and acute motor-sensory axonal neuropathy.3,4 Acute inflammatory demyelinating polyneuropathy is the prototype of GuillainBarre´ syndrome and is most frequently seen in northern America and Europe. This subtype constitutes 85% to 90% of all cases of Guillain-Barre´ syndrome. Acute motor axonal neuropathy is characterized with pure motor involvement with prominent axonal injury often seen in northern China, Japan, and southern America following Campylobacter jejuni infections. Sensorial symptoms are more distinctive in the acute motor-sensory axonal neuropathy subtype, a rare pediatric pathology, resulting from axonal injury of motor and sensorial fibers.5
Normoactive or hyperactive deep tendon reflexes is not usual in Guillain-Barre´ syndrome. The 12-year-old girl presenting with complaints of inability to walk, numbness in hands and feet, and diagnosed with Guillain-Barre´ syndrome is presented for bilateral absence of Achilles reflex and hyperactivity of the other upper and lower extremity deep tendon reflexes.
Case Summary A 12-year-old girl admitted with unsteady gait and numbness in hands and feet. History of the patient revealed that 10 days ago she had been hospitalized with a diagnosis of acute gastroenteritis at another center for a week, and developed numbness in hands and feet, weakness in lower extremities, and impairment of walking in 4 days. Neurologic examination showed bilateral lateral gaze palsy that was more prominent on the left. Uvula was deviated to the right and gag reflex was 1
Department of Neurology, Medical Faculty, Adnan Menderes University, Aydin, Turkey 2 Department of Child Neurology, Medical Faculty, Adnan Menderes University, Aydin, Turkey Corresponding Author: Utku Ogan Akyildiz, MD, Adnan Menderes University, Medical Faculty, Department of Neurology, 09100, Aydin, Turkey. Email: [email protected]
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
2
Journal of Child Neurology
lost. Muscle strength was 4/5 bilaterally in the upper extremity and proximal muscle groups of lower extremity, but 2/5 in distal muscle groups of lower extremity. Tendon reflexes were brisk except for an absent Achilles tendon reflex. Hoffmann and Babinski reflexes and superficial reflexes were also bilaterally positive. Hyperesthesia was determined in distal parts of the extremities. The other systems were normal. Analysis of complete blood count and routine biochemistry were normal. No pathologic findings were determined in cranial and spinal magnetic resonance imaging with contrast enhancement. Cerebrospinal fluid analysis showed no cells, despite a protein level of 126 mg/dL (N: 15-40 mg/dL). Sensorial nerve action potentials could not be obtained in the upper and lower extremity electromyography. There was no significant slowness in the motor conductions of upper and lower extremity nerves; however, loss of peak to peak amplitudes was determined in compound muscle action potentials observed more significantly in the lower extremities. Additionally, a reduced F wave persistence was seen in the lower extremity peripheral nerves. The patient was diagnosed with Guillain-Barre´ syndrome on clinical, laboratorial, and electromyographic grounds and 2 g/kg intravenous immunoglobulin therapy was administered. Negative results were obtained in serologic tests screening for cytomegalovirus, Epstein-Barr, Herpes Simplex, and Borrelia burgdorferi. The antibodies against gangliosides (GM1, GQ1B, GD1B, GT1B, GD1a, GM3, and GM2) were absent both in serum and cerebrospinal fluid. Serologic test for C jejuni could not be performed for financial reasons. Electromyography performed at day 15 of the clinical course demonstrated absence of sensorial nerve action potential in the upper and lower extremities. Significant loss of amplitude was observed in upper extremity motor conduction. No significant prolongation in the distal latencies or conduction slowness was detected. Persistency of F responses was reduced. Tibial H reflex was within normal ranges. Any electrophysiological findings reflecting demyelinating features was not observed in electrophysiological investigations during the patient follow-up. Detailed electrophysiological data have been given in Table 1. On clinical examination, muscle strength was 5/5 on all extremities and bilaterally Achilles reflex was hypoactive. Babinski reflexes were bilaterally positive. Although sensorial nerve action potentials could not be obtained in the electrophysiological investigation performed at 1 month into examination, tibial F response persistency was reduced and latency was moderately prolonged. Tibial nerve examination demonstrated no prolongation in distal latency or marked slowing of conduction rates. However, the amplitudes of compound muscle action potentials were significantly small. Sensorial nerve action potentials could still not be obtained in the electrophysiological examination of upper and lower extremities performed at 18 months into examination. Significant increase was determined in upper extremity compound muscle action potential amplitudes, whereas lower extremity compound muscle action potential amplitudes were still below the normal range despite a mild increase (Table 1). Electrophysiological examinations repeated in the control visit
Table 1. Electrophysiological Findings. Day 4 Day 15 Day 30 Month 18 Normal limit Motor NCS Median nerve DL (ms) CV (m/s) CMAP (mV) Tibial nerve DL (ms) CV (m/s) CMAP (mV) Sensorial NCS Median nerve DL (ms) SNAP (mV) Sural nerve DL (ms) SNAP (mV)
3.5 42.2 5.8
3.6 50 0.7
3.6 53.8 8.4
3.8 60.5 9.2
40 >2
8.9 39.6 0.5
6.2 47.9 0.8
4.8 36.0 0.3
6.0 37.0 1.2
40 >4
— —
— —
— —
— —
15
— —
— —
— —
— —
5
Abbreviations: CMAP, compound muscle action potential; CV, conduction velocity; DL, distal latency; ms, milliseconds; mV, millivolt; mV, microvolt; NCS, nerve conduction studies; SNAP, sensorial nerve action potential.
confirmed an acute polyneuropathy picture with prominent sensorial and motor axonal injury with more significant impairment of lower extremity motor conduction, and the case was therefore diagnosed with acute motor-sensory axonal neuropathy subtype of Guillain-Barre´ syndrome. Muscle strength was 5/5 on all 4 extremities at 8 months into examination; bilaterally Achilles reflex was hypoactive and the remaining deep tendon reflexes were brisk at 18 months into examination.
Discussion Guillain-Barre´ syndrome is characterized with acute progressive motor weakness and areflexia.6,7 Normoactive or hyperactive deep tendon reflexes is not a common finding in Guillain-Barre´ syndrome. Brisk or normal deep tendon reflexes has been reported often early in the disease course in acute motor axonal neuropathy subtype of Guillain-Barre´ syndrome cases developed following C jejuni infection, with antiganglioside antibody positivity.5,8,9 In a study of 54 Japanese Guillain-Barre´ syndrome patients of 3 to 78 years, hyperreflexia was determined early (4-6 weeks) in the disease course in 7 individuals (acute hyperreflexia in 1 patient), a diagnosis of acute motor axonal neuropathy was established in 6 of these 7 patients, anti-GM1 antibodies were detected in all, and C jejuni antibody positivity was observed in 2.8 Hyperreflexia was more frequent in the early recovery period of some Chinese and Japanese patients, and a better recovery process has been reported in 44% and 48% of various studies.10,11 Yuki et al12 have compared patients with intact deep tendon reflexes at the onset of the clinical picture and patients with decreased or absent deep tendon reflexes and found significantly higher rates of diarrhea in history, extremity weakness, antiganglioside antibody positivity in the
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
Tosun et al
3
acute motor axonal neuropathy subtype in the first group; on the other hand, there were higher rates of distal paresthesia, cranial nerve involvement, and acute inflammatory demyelinating polyneuropathy in the second group. Authors have reported that deep tendon reflex was normal or increased in 10% of Guillain-Barre´ syndrome patients; however, hyperreflexia was not observed in any of the patients diagnosed with acute motor-sensory axonal neuropathy. Additionally, some patients with Guillain-Barre´ syndrome and retained tendon reflexes and/or extensor plantar responses have been reported in the literature.13,14 Barisic´ and Grkovic´9 have reported 16 children aged 14 months to 13 years with Guillain-Barre´ syndrome with hyperreflexia. Hyperreflexia or brisk reflexes and/or positive extensor plantar response were observed in the first 2 weeks of the clinical picture in 7 individuals, in the recovery period in 9 cases (4-13 months after the onset of clinical improvement), and in the initial or recovery period only in 1 patient.9 Our patient had also an overt axonal involvement of sensorial fibers. No demyelinating feature in motor and sensorial nerve conductions was observed in this individual. Therefore, it seems that acute motor-sensory axonal neuropathy was appropriate diagnosis for our patient. Additionally, these features have not been observed in the cases presented by Barisic´ and Grkovic´.9 Patients with acute motor axonal neuropathy subtype of Guillain-Barre´ syndrome and hyperreflexia following C jejuni infection have been reported in the literature.4,6,8 Similarly, there is a literature report of acute motor axonal neuropathy subtype of Guillain-Barre´ syndrome with hyperreflexia following an episode of diarrhea, and C jejuni and antiganglioside antibody negativity.15 However, C jejuni serology could not be examined in our case because of financial reasons. Although the exact mechanism of hyperreflexia in the context of Guillain-Barre´ syndrome, has not been thoroughly clarified, central mechanisms have provided an explanation in certain patients. Hyperreflexia has been reported to be an associated finding of spinal inhibitor intermediate neuronal or upper motor neuronal dysfunction.6 Hyperreflexia is mostly reported in patients with anti-GM1 ganglioside antibody positivity in the literature, and anti-GM1 positive serum has been reported to cause injury in nerve roots and central axons of the spinal cord on injection into the subarachnoid space.8 Inflammation in the spinal nerve roots has also been suggested to damage blood–central nervous system barrier in patients with Guillain-Barre´ syndrome and allow antiganglioside antibodies to reach inhibitory intermediate neurons, neuronal structures close to the anterior horn cells of spinal cord.8,12 Although areflexia secondary to sensorial nervous involvement has been reported in acute inflammatory demyelinating polyneuropathy or acute motor axonal neuropathy patients, and intact or faster recovering deep tendon reflexes due to isolated motor axonal involvement has been reported in individuals with acute motor axonal neuropathy; hyperreflexia has not been explained.8 This patient has been diagnosed with acute motor-sensory axonal neuropathy subtype of Guillain-Barre´ syndrome because of lack of sensorial nervous action potential in repeated nerve
conduction studies, and prominent sensorial and motor axonal injury. The hyperreflexia observed in this patient could not be explained. There are no other literature reports of acute motorsensory axonal neuropathy subtype of Guillain-Barre´ syndrome with hyperreflexia.
Conclusion Normoactive or hyperactive deep tendon reflexes is not a common finding in Guillain-Barre´ syndrome. Hyperreflexia in Guillain-Barre´ syndrome has been reported in a limited number of acute motor axonal neuropathy patients with antiGM1 antibody positivity, mild forms of acute inflammatory demyelinating polyneuropathy. This case report emphasizes the rare possibility of hyperreflexia in acute motor-sensory axonal neuropathy in the absence of antiganglioside antibodies, in the pediatric age group. Author Contributions AT, S¸ D, and UOA wrote the first draft of the manuscript. CT, UOA, and SO cared for the patient.
Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
References 1. Vucic S, Kiernan MC, Cornblath DR. Guillain-Barre´ syndrome: an update. J Clin Neurosci. 2009;16:733-741. 2. Thomas NH. Diagnosis and management of Guillain-Barre´ syndrome. Curr Paediatr. 2005;15:287-291. 3. Gupta D, Nair M, Baheti NN, Sarma PS, Kuruvilla A. Electrodiagnostic and clinical aspects of Guillain-Barre´ syndrome: an analysis of 142 cases. J Clin Neuromuscul Dis. 2008;10:42-51. 4. Neuwirth C, Mojon D, Weber M. GD1a-associated pure motor Guillain-Barre´ syndrome with hyperreflexia and bilateral papillitis. J Clin Neuromuscul Dis. 2010;11:114-119. 5. Nagasawa K, Kuwabara S, Misawa S, Fujii K, Tanabe Y, Yuki N, Hattori T, Kohno Y. Electrophysiological subtypes and prognosis of childhood Guillain-Barre´ syndrome in Japan. Muscle Nerve. 2006;33:766-770. 6. Kuwabara S, Nakata M, Sung JY, Mori M, Kato N, Hattori T, Koga M, Yuki N. Hyperreflexia in axonal Guillain-Barre´ syndrome subsequent to Campylobacter jejuni enteritis. J Neurol Sci. 2002;199:89-92. 7. Ye Y, Zhu D, Wang K, Wu J, Feng J, Ma D, Xing Y, Jiang X. Clinical and electrophysiological features of the 2007 GuillainBarre´ syndrome epidemic in northeast China. Muscle Nerve. 2010;42:311-314. 8. Kuwabara S, Ogawara K, Koga M, Mori M, Hattori T, Yuki N. Hyperreflexia in Guillain-Barre´ syndrome: relation with acute
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
4
Journal of Child Neurology
motor axonal neuropathy and anti-GM1 antibody. J Neurol Neurosurg Psychiatry. 1999;67:180-184. 9. Barisic´ N, Grkovic´ L. Long term clinical and electrophysiological assessment of Croatian children with corticospinal tract involvement in Guillain-Barre´ syndrome (GBS). Eur J Paediatr Neurol. 2010;14:391-399. 10. Kuwabara S, Mori M, Ogawara K, Hattori T, Yuki N. Indicators of rapid clinical recovery in Guillain-Barre´ syndrome. J Neurol Neurosurg Psychiatry. 2001;70:560-562. 11. McKhann GM, Cornblath DR, et al. Acute motor axonal neuropathy: a frequent cause of acute flaccid paralysis in China. Ann Neurol. 1993;33:333-342.
12. Yuki N, Kokubun N, Kuwabara S, et al. Guillain-Barre´ syndrome associated with normal or exaggerated tendon reflexes. J Neurol. 2012;259:1181-1190. 13. Singhal V, Bhat KG. Guillain-Barre syndrome with hyperreflexia: a variant. J Pediatr Neurosci. 2011;6:144-145. 14. Ogawa G, Kaida K, Shiozaki Y, Araki M, Kimura F, Kamakura K. Case of pure motor Guillain-Barre´ syndrome with motor conduction block and anti-GM1/GalNAc-GD1a antibody [in Japanese]. Rinsho Shinkeigaku. 2009;49:488-492. 15. Baheti NN, Manuel D, Shinde PD, Radhakrishnan A, Nair M. Hyperreflexic Guillain-Barre´ syndrome. Ann Indian Acad Neurol. 2010;13:305-307.
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
Acute Motor-Sensory Axonal Neuropathy With Hyperreflexia in Guillain-Barré Syndrome Ayse Tosun, Siar Dursun, Utku Ogan Akyildiz, Seçil Oktay and Cengiz Tataroglu J Child Neurol published online 2 April 2014 DOI: 10.1177/0883073814528377 The online version of this article can be found at: http://jcn.sagepub.com/content/early/2014/04/01/0883073814528377
Published by: http://www.sagepublications.com
Additional services and information for Journal of Child Neurology can be found at: Email Alerts: http://jcn.sagepub.com/cgi/alerts Subscriptions: http://jcn.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - Apr 2, 2014 What is This?
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
Brief Communication
Acute Motor-Sensory Axonal Neuropathy With Hyperreflexia in Guillain-Barre´ Syndrome
Journal of Child Neurology 1-4 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0883073814528377 jcn.sagepub.com
Ays¸ e Tosun, MD2, S¸ iar Dursun, MD2, Utku Ogan Akyildiz, MD1, Sec¸il Oktay, MD2, and Cengiz Tatarog˘lu, MD1
Abstract Guillain-Barre´ syndrome is an acute inflammatory autoimmune polyradiculoneuritis. Progressive motor weakness and areflexia are essential for its diagnosis. Hyperreflexia has rarely been reported in the early healing period of Guillain-Barre´ syndrome following Campylobacter jejuni infection in patients with acute motor axonal neuropathy with antiganglioside antibody positivity. In this study, we report a 12-year-old girl presenting with complaints of inability to walk, numbness in hands and feet, and hyperactive deep tendon reflexes since the onset of the clinical picture, diagnosed with acute motor-sensory axonal neuropathy type of Guillain-Barre´ syndrome. Keywords Guillain-Barre´ syndrome, hyperreflexia Received December 29, 2013. Received revised February 25, 2014. Accepted for publication February 26, 2014.
Guillain-Barre´ syndrome is the most common cause of acquired polyneuropathies. The worldwide incidence has been reported to be 0.6 to 4 in 100 000.1 Guillain-Barre´ syndrome is an autoimmune clinical picture characterized with elevated protein levels without pleocytosis in cerebrospinal fluid; often ascending and symmetrical extremity paralysis; sensorial deficit of distal extremities; bulbar, facial, and ocular involvement of varying degrees; and loss of deep tendon reflexes following a viral upper respiratory tract infection, gastrointestinal infection, or vaccination.1,2 The term Guillain-Barre´ syndrome defines a heterogeneous group of diseases with different clinical features rather than a single disease. Guillain-Barre´ syndrome has 3 subtypes defined by electrophysiological and pathogenetic properties, including acute inflammatory demyelinating polyneuropathy, acute motor axonal neuropathy, and acute motor-sensory axonal neuropathy.3,4 Acute inflammatory demyelinating polyneuropathy is the prototype of GuillainBarre´ syndrome and is most frequently seen in northern America and Europe. This subtype constitutes 85% to 90% of all cases of Guillain-Barre´ syndrome. Acute motor axonal neuropathy is characterized with pure motor involvement with prominent axonal injury often seen in northern China, Japan, and southern America following Campylobacter jejuni infections. Sensorial symptoms are more distinctive in the acute motor-sensory axonal neuropathy subtype, a rare pediatric pathology, resulting from axonal injury of motor and sensorial fibers.5
Normoactive or hyperactive deep tendon reflexes is not usual in Guillain-Barre´ syndrome. The 12-year-old girl presenting with complaints of inability to walk, numbness in hands and feet, and diagnosed with Guillain-Barre´ syndrome is presented for bilateral absence of Achilles reflex and hyperactivity of the other upper and lower extremity deep tendon reflexes.
Case Summary A 12-year-old girl admitted with unsteady gait and numbness in hands and feet. History of the patient revealed that 10 days ago she had been hospitalized with a diagnosis of acute gastroenteritis at another center for a week, and developed numbness in hands and feet, weakness in lower extremities, and impairment of walking in 4 days. Neurologic examination showed bilateral lateral gaze palsy that was more prominent on the left. Uvula was deviated to the right and gag reflex was 1
Department of Neurology, Medical Faculty, Adnan Menderes University, Aydin, Turkey 2 Department of Child Neurology, Medical Faculty, Adnan Menderes University, Aydin, Turkey Corresponding Author: Utku Ogan Akyildiz, MD, Adnan Menderes University, Medical Faculty, Department of Neurology, 09100, Aydin, Turkey. Email: [email protected]
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
2
Journal of Child Neurology
lost. Muscle strength was 4/5 bilaterally in the upper extremity and proximal muscle groups of lower extremity, but 2/5 in distal muscle groups of lower extremity. Tendon reflexes were brisk except for an absent Achilles tendon reflex. Hoffmann and Babinski reflexes and superficial reflexes were also bilaterally positive. Hyperesthesia was determined in distal parts of the extremities. The other systems were normal. Analysis of complete blood count and routine biochemistry were normal. No pathologic findings were determined in cranial and spinal magnetic resonance imaging with contrast enhancement. Cerebrospinal fluid analysis showed no cells, despite a protein level of 126 mg/dL (N: 15-40 mg/dL). Sensorial nerve action potentials could not be obtained in the upper and lower extremity electromyography. There was no significant slowness in the motor conductions of upper and lower extremity nerves; however, loss of peak to peak amplitudes was determined in compound muscle action potentials observed more significantly in the lower extremities. Additionally, a reduced F wave persistence was seen in the lower extremity peripheral nerves. The patient was diagnosed with Guillain-Barre´ syndrome on clinical, laboratorial, and electromyographic grounds and 2 g/kg intravenous immunoglobulin therapy was administered. Negative results were obtained in serologic tests screening for cytomegalovirus, Epstein-Barr, Herpes Simplex, and Borrelia burgdorferi. The antibodies against gangliosides (GM1, GQ1B, GD1B, GT1B, GD1a, GM3, and GM2) were absent both in serum and cerebrospinal fluid. Serologic test for C jejuni could not be performed for financial reasons. Electromyography performed at day 15 of the clinical course demonstrated absence of sensorial nerve action potential in the upper and lower extremities. Significant loss of amplitude was observed in upper extremity motor conduction. No significant prolongation in the distal latencies or conduction slowness was detected. Persistency of F responses was reduced. Tibial H reflex was within normal ranges. Any electrophysiological findings reflecting demyelinating features was not observed in electrophysiological investigations during the patient follow-up. Detailed electrophysiological data have been given in Table 1. On clinical examination, muscle strength was 5/5 on all extremities and bilaterally Achilles reflex was hypoactive. Babinski reflexes were bilaterally positive. Although sensorial nerve action potentials could not be obtained in the electrophysiological investigation performed at 1 month into examination, tibial F response persistency was reduced and latency was moderately prolonged. Tibial nerve examination demonstrated no prolongation in distal latency or marked slowing of conduction rates. However, the amplitudes of compound muscle action potentials were significantly small. Sensorial nerve action potentials could still not be obtained in the electrophysiological examination of upper and lower extremities performed at 18 months into examination. Significant increase was determined in upper extremity compound muscle action potential amplitudes, whereas lower extremity compound muscle action potential amplitudes were still below the normal range despite a mild increase (Table 1). Electrophysiological examinations repeated in the control visit
Table 1. Electrophysiological Findings. Day 4 Day 15 Day 30 Month 18 Normal limit Motor NCS Median nerve DL (ms) CV (m/s) CMAP (mV) Tibial nerve DL (ms) CV (m/s) CMAP (mV) Sensorial NCS Median nerve DL (ms) SNAP (mV) Sural nerve DL (ms) SNAP (mV)
3.5 42.2 5.8
3.6 50 0.7
3.6 53.8 8.4
3.8 60.5 9.2
40 >2
8.9 39.6 0.5
6.2 47.9 0.8
4.8 36.0 0.3
6.0 37.0 1.2
40 >4
— —
— —
— —
— —
15
— —
— —
— —
— —
5
Abbreviations: CMAP, compound muscle action potential; CV, conduction velocity; DL, distal latency; ms, milliseconds; mV, millivolt; mV, microvolt; NCS, nerve conduction studies; SNAP, sensorial nerve action potential.
confirmed an acute polyneuropathy picture with prominent sensorial and motor axonal injury with more significant impairment of lower extremity motor conduction, and the case was therefore diagnosed with acute motor-sensory axonal neuropathy subtype of Guillain-Barre´ syndrome. Muscle strength was 5/5 on all 4 extremities at 8 months into examination; bilaterally Achilles reflex was hypoactive and the remaining deep tendon reflexes were brisk at 18 months into examination.
Discussion Guillain-Barre´ syndrome is characterized with acute progressive motor weakness and areflexia.6,7 Normoactive or hyperactive deep tendon reflexes is not a common finding in Guillain-Barre´ syndrome. Brisk or normal deep tendon reflexes has been reported often early in the disease course in acute motor axonal neuropathy subtype of Guillain-Barre´ syndrome cases developed following C jejuni infection, with antiganglioside antibody positivity.5,8,9 In a study of 54 Japanese Guillain-Barre´ syndrome patients of 3 to 78 years, hyperreflexia was determined early (4-6 weeks) in the disease course in 7 individuals (acute hyperreflexia in 1 patient), a diagnosis of acute motor axonal neuropathy was established in 6 of these 7 patients, anti-GM1 antibodies were detected in all, and C jejuni antibody positivity was observed in 2.8 Hyperreflexia was more frequent in the early recovery period of some Chinese and Japanese patients, and a better recovery process has been reported in 44% and 48% of various studies.10,11 Yuki et al12 have compared patients with intact deep tendon reflexes at the onset of the clinical picture and patients with decreased or absent deep tendon reflexes and found significantly higher rates of diarrhea in history, extremity weakness, antiganglioside antibody positivity in the
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
Tosun et al
3
acute motor axonal neuropathy subtype in the first group; on the other hand, there were higher rates of distal paresthesia, cranial nerve involvement, and acute inflammatory demyelinating polyneuropathy in the second group. Authors have reported that deep tendon reflex was normal or increased in 10% of Guillain-Barre´ syndrome patients; however, hyperreflexia was not observed in any of the patients diagnosed with acute motor-sensory axonal neuropathy. Additionally, some patients with Guillain-Barre´ syndrome and retained tendon reflexes and/or extensor plantar responses have been reported in the literature.13,14 Barisic´ and Grkovic´9 have reported 16 children aged 14 months to 13 years with Guillain-Barre´ syndrome with hyperreflexia. Hyperreflexia or brisk reflexes and/or positive extensor plantar response were observed in the first 2 weeks of the clinical picture in 7 individuals, in the recovery period in 9 cases (4-13 months after the onset of clinical improvement), and in the initial or recovery period only in 1 patient.9 Our patient had also an overt axonal involvement of sensorial fibers. No demyelinating feature in motor and sensorial nerve conductions was observed in this individual. Therefore, it seems that acute motor-sensory axonal neuropathy was appropriate diagnosis for our patient. Additionally, these features have not been observed in the cases presented by Barisic´ and Grkovic´.9 Patients with acute motor axonal neuropathy subtype of Guillain-Barre´ syndrome and hyperreflexia following C jejuni infection have been reported in the literature.4,6,8 Similarly, there is a literature report of acute motor axonal neuropathy subtype of Guillain-Barre´ syndrome with hyperreflexia following an episode of diarrhea, and C jejuni and antiganglioside antibody negativity.15 However, C jejuni serology could not be examined in our case because of financial reasons. Although the exact mechanism of hyperreflexia in the context of Guillain-Barre´ syndrome, has not been thoroughly clarified, central mechanisms have provided an explanation in certain patients. Hyperreflexia has been reported to be an associated finding of spinal inhibitor intermediate neuronal or upper motor neuronal dysfunction.6 Hyperreflexia is mostly reported in patients with anti-GM1 ganglioside antibody positivity in the literature, and anti-GM1 positive serum has been reported to cause injury in nerve roots and central axons of the spinal cord on injection into the subarachnoid space.8 Inflammation in the spinal nerve roots has also been suggested to damage blood–central nervous system barrier in patients with Guillain-Barre´ syndrome and allow antiganglioside antibodies to reach inhibitory intermediate neurons, neuronal structures close to the anterior horn cells of spinal cord.8,12 Although areflexia secondary to sensorial nervous involvement has been reported in acute inflammatory demyelinating polyneuropathy or acute motor axonal neuropathy patients, and intact or faster recovering deep tendon reflexes due to isolated motor axonal involvement has been reported in individuals with acute motor axonal neuropathy; hyperreflexia has not been explained.8 This patient has been diagnosed with acute motor-sensory axonal neuropathy subtype of Guillain-Barre´ syndrome because of lack of sensorial nervous action potential in repeated nerve
conduction studies, and prominent sensorial and motor axonal injury. The hyperreflexia observed in this patient could not be explained. There are no other literature reports of acute motorsensory axonal neuropathy subtype of Guillain-Barre´ syndrome with hyperreflexia.
Conclusion Normoactive or hyperactive deep tendon reflexes is not a common finding in Guillain-Barre´ syndrome. Hyperreflexia in Guillain-Barre´ syndrome has been reported in a limited number of acute motor axonal neuropathy patients with antiGM1 antibody positivity, mild forms of acute inflammatory demyelinating polyneuropathy. This case report emphasizes the rare possibility of hyperreflexia in acute motor-sensory axonal neuropathy in the absence of antiganglioside antibodies, in the pediatric age group. Author Contributions AT, S¸ D, and UOA wrote the first draft of the manuscript. CT, UOA, and SO cared for the patient.
Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
References 1. Vucic S, Kiernan MC, Cornblath DR. Guillain-Barre´ syndrome: an update. J Clin Neurosci. 2009;16:733-741. 2. Thomas NH. Diagnosis and management of Guillain-Barre´ syndrome. Curr Paediatr. 2005;15:287-291. 3. Gupta D, Nair M, Baheti NN, Sarma PS, Kuruvilla A. Electrodiagnostic and clinical aspects of Guillain-Barre´ syndrome: an analysis of 142 cases. J Clin Neuromuscul Dis. 2008;10:42-51. 4. Neuwirth C, Mojon D, Weber M. GD1a-associated pure motor Guillain-Barre´ syndrome with hyperreflexia and bilateral papillitis. J Clin Neuromuscul Dis. 2010;11:114-119. 5. Nagasawa K, Kuwabara S, Misawa S, Fujii K, Tanabe Y, Yuki N, Hattori T, Kohno Y. Electrophysiological subtypes and prognosis of childhood Guillain-Barre´ syndrome in Japan. Muscle Nerve. 2006;33:766-770. 6. Kuwabara S, Nakata M, Sung JY, Mori M, Kato N, Hattori T, Koga M, Yuki N. Hyperreflexia in axonal Guillain-Barre´ syndrome subsequent to Campylobacter jejuni enteritis. J Neurol Sci. 2002;199:89-92. 7. Ye Y, Zhu D, Wang K, Wu J, Feng J, Ma D, Xing Y, Jiang X. Clinical and electrophysiological features of the 2007 GuillainBarre´ syndrome epidemic in northeast China. Muscle Nerve. 2010;42:311-314. 8. Kuwabara S, Ogawara K, Koga M, Mori M, Hattori T, Yuki N. Hyperreflexia in Guillain-Barre´ syndrome: relation with acute
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
4
Journal of Child Neurology
motor axonal neuropathy and anti-GM1 antibody. J Neurol Neurosurg Psychiatry. 1999;67:180-184. 9. Barisic´ N, Grkovic´ L. Long term clinical and electrophysiological assessment of Croatian children with corticospinal tract involvement in Guillain-Barre´ syndrome (GBS). Eur J Paediatr Neurol. 2010;14:391-399. 10. Kuwabara S, Mori M, Ogawara K, Hattori T, Yuki N. Indicators of rapid clinical recovery in Guillain-Barre´ syndrome. J Neurol Neurosurg Psychiatry. 2001;70:560-562. 11. McKhann GM, Cornblath DR, et al. Acute motor axonal neuropathy: a frequent cause of acute flaccid paralysis in China. Ann Neurol. 1993;33:333-342.
12. Yuki N, Kokubun N, Kuwabara S, et al. Guillain-Barre´ syndrome associated with normal or exaggerated tendon reflexes. J Neurol. 2012;259:1181-1190. 13. Singhal V, Bhat KG. Guillain-Barre syndrome with hyperreflexia: a variant. J Pediatr Neurosci. 2011;6:144-145. 14. Ogawa G, Kaida K, Shiozaki Y, Araki M, Kimura F, Kamakura K. Case of pure motor Guillain-Barre´ syndrome with motor conduction block and anti-GM1/GalNAc-GD1a antibody [in Japanese]. Rinsho Shinkeigaku. 2009;49:488-492. 15. Baheti NN, Manuel D, Shinde PD, Radhakrishnan A, Nair M. Hyperreflexic Guillain-Barre´ syndrome. Ann Indian Acad Neurol. 2010;13:305-307.
Downloaded from jcn.sagepub.com at National Dong Hwa University on April 7, 2014
![[Acute sensory-motor axonal neuropathy (Guillain-Barre syndrome) following vertebroplasty].](/assets/img/hold.png)
