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Double spinal cord lesions and pelvic floor electrophysiology
Clinical Neurophysiology 127 (2016) 2317–2318
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
Double spinal cord lesions and pelvic floor electrophysiology See Article, pages 2319–2324
In most patients with cervical or thoracic spinal cord injury (SCI) the average clinician might expect the sacral spinal cord (and the sacral nerve roots and related nerves) to be preserved (unless there was obvious polytrauma). This may not be so as Tankisi et al. report in this issue of Clinical Neurophysiologu (Tankisi et al., 2016). They are not the first to demonstrate this: sphincter EMG abnormalities (indicating a lower motor neuron lesion) in SCI patients with supraconal lesions have been reported before (Blank and Magora, 1975), and the concept of a ‘‘double lesion” has been introduced by Beric et al., who have demonstrated unexpected lesions of the lumbosacral segments – as demonstrated by findings of clinical, neurophysiological and urodynamic examinations – in 18 out of 130 patients with cervical or thoracic spinal cord injuries. The pathophysiology of this ‘‘lower” nervous system lesion was proposed to be directly or indirectly linked to the processes accompanying the original trauma causing the higher spinal cord lesion (Beric et al., 1987). Thus, an ‘‘additional” pathology in the sacral segments in a patient with a ‘‘primary” cervical or thoracic spinal cord lesion should not be quite unexpected; it has now been confirmed by using a different set of clinical neurophysiological tests as Beric et al. (1987): tests assessing particularly the elements of the peripheral reflex arc of lower sacral segments (EMG of the external anal sphincter, pudendal terminal motor latency /PNTML/, bulbocavernosus reflex and pudendal somatosensory evoked potentials (/pSEP/) (Tankisi et al., 2016). As Tankisi et al. found sphincter EMG abnormalities (Tankisi et al., 2016), clearly the lesion in the lower sacral segments was of the ‘‘lower motor neuron type”; but more precise localization was not possible; one of the reasons being the questionable usefulness of PNTML (cf. Tubaro et al., 2013), the other technical issues related to the root and spinal cord potentials of the pudendal SEP. Thus, the demonstrated abnormalities can derive from anywhere in the reflex arc – from conus to the periphery. The site of the lesion was better defined by Beric et al., who meticulously recorded lumbosacral SEP and reported abnormalities of the R wave (the cauda equina root potential) in the majority of their patients with lumbosacral abnormalities, thus pointing to the nerve roots as the site of the lesion. (In some, only the S wave – spinogram – was abnormal, pointing to myelopathy). (Beric et al., 1987). As Tankisi et al. have demonstrated – in the same patient group as reported in (Tankisi et al., 2016) – also peripheral nervous system involvement in lower limbs (Tankisi et al., 2015), both lumbal and sacral segments were involved (but this has also been claimed by Beric et al. in their larger group of SCI patients (Beric et al.,
1987)). The real question is: are these abnormalities present in all segments below the «primary lesion» (in affected patients), or is there a predilection for the lumbo-sacral segments? Similarly uncertain is the pathophysiology of the reported additional «lower motor neuron type/peripheral nervous system lesions». In previous literature, ‘‘transsynaptic degeneration” was the most often proposed hypothesis to account for peripheral denervation in patients with primary upper motor neuron lesions (Kirshblum et al., 2001). Newly developed compression neuropathies in wheelchair/ bedbound SCI patients might explain abnormalities in lower limbs, but could this also be true for the pudendal nerve? In this respect it is important to point out that Beric et al. have demonstrated urodynamic abnormalities compatible with a ‘‘lower motor neuron type” lesion, as well, thus pointing to a lesion of the autonomic fibers, and necessarily a more widespread involvement of the sacral nervous system than pudendal nerve alone. Such a widespread involvement is most readily explained by a proximal – conus or cauda equina – lesion (Beric et al., 1987). Whatever the cause, the presence of the potential abnormalities below the «obvious» spinal cord lesion in SCI patients has clear practical implications. Whenever in any individual patient the extent or nature of the neurological lesion is uncertain, and especially if irreversible treatment is contemplated, it seems logical to gather quantitative knowledge of the nervous system dysfunction in order to make a rational treatment choice. Of course most patients with cervical or thoracic spinal cord lesions may not require a sophisticated definition of the ‘‘overall” lesion if conservative treatment and rehabilitation produce the expected results. But in selected patients – for instance those undergoing invasive therapeutic interventions related to nervous system function – clinical neurophysiological testing will clarify issues related to the lesion(s) of the spinal cord (and the peripheral nervous system innervating any defined myotomes and dermatomes, also the sacral). Experience with testing patient groups with suspected lesions within the nervous reflex arcs of sacral segments 2–5 has generated the recommendation that the information gained by clinical examination may be enhanced particularly by concentric needle EMG (to diagnose denervation and reinervation of pelvic floor and perineal muscles), and sacral reflex testing (to assess the continuity of the sacral reflex arc) (Tubaro et al., 2013). In summary, further studies should clarify the prevalence and grades of severity of involvement of nervous system segments lower to the primary or «obvious» spinal cord lesion in SCI patients; define the potentially different locations (and causes) of such
http://dx.doi.org/10.1016/j.clinph.2016.01.007 1388-2457/Ó 2016 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
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Editorial / Clinical Neurophysiology 127 (2016) 2317–2318
lesions; their clinical relevance, and the place of particular clinical neurophysiological tests in defining these lesions in individual patients. Conflict of interest The author has no conflict of interest. References Beric A, Dimitrijevic MR, Light JK. A clinical syndrome of rostral and caudal spinal injury: neurological, neurophysiological and urodynamic evidence for occult sacral lesion. J Neurol Neurosurg Psychiatry 1987;50:600–6. Blank A, Magora A. Electromyographic investigation of the superficial sphincter ani muscle (SSAM) in spinal cord injury. Electromyogr Clin Neurophysiol 1975;15:261–8. Kirshblum S, Lim S, Garstang S, Millis S. Electrodiagnostic changes in the lower limbs in subjects with chronic complete cervical spinal cord injury. Arch Phys Med Rehabil 2001;82:604–7.
Tankisi H, Pugdahl K, Rasmussen MM, Clemmensen D, Rawashdeh YF, Christensen P, et al. Peripheral nervous system involvement in chronic spinal cord injury. Muscle Nerve 2015;52:1022–62. Tankisi H, Pugdahl K, Rasmussen MM, Clemmensen D, Rawashdeh YF, Christensen P, et al. Pelvic floor electrophysiology in spinal cord injury. Clin Neurophysiol 2016;127(5):2319–24. Tubaro A, Vodušek DB, Amarenco G, Doumouchtsis SK, DeLancey JOL, Fernando R, et al. Imaging, neurophysiological testing and other tests. In: Abrams P, Cardozo L, Khoury S, Wein A, editors. Incontinence. 5th ed. Paris: ICUD – EAU; 2013. p. 507–622.
David B. Vodušek Medical Faculty, University of Ljubljana, Ljubljana, Slovenia E-mail address: [email protected] Available online 23 January 2016
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
Double spinal cord lesions and pelvic floor electrophysiology See Article, pages 2319–2324
In most patients with cervical or thoracic spinal cord injury (SCI) the average clinician might expect the sacral spinal cord (and the sacral nerve roots and related nerves) to be preserved (unless there was obvious polytrauma). This may not be so as Tankisi et al. report in this issue of Clinical Neurophysiologu (Tankisi et al., 2016). They are not the first to demonstrate this: sphincter EMG abnormalities (indicating a lower motor neuron lesion) in SCI patients with supraconal lesions have been reported before (Blank and Magora, 1975), and the concept of a ‘‘double lesion” has been introduced by Beric et al., who have demonstrated unexpected lesions of the lumbosacral segments – as demonstrated by findings of clinical, neurophysiological and urodynamic examinations – in 18 out of 130 patients with cervical or thoracic spinal cord injuries. The pathophysiology of this ‘‘lower” nervous system lesion was proposed to be directly or indirectly linked to the processes accompanying the original trauma causing the higher spinal cord lesion (Beric et al., 1987). Thus, an ‘‘additional” pathology in the sacral segments in a patient with a ‘‘primary” cervical or thoracic spinal cord lesion should not be quite unexpected; it has now been confirmed by using a different set of clinical neurophysiological tests as Beric et al. (1987): tests assessing particularly the elements of the peripheral reflex arc of lower sacral segments (EMG of the external anal sphincter, pudendal terminal motor latency /PNTML/, bulbocavernosus reflex and pudendal somatosensory evoked potentials (/pSEP/) (Tankisi et al., 2016). As Tankisi et al. found sphincter EMG abnormalities (Tankisi et al., 2016), clearly the lesion in the lower sacral segments was of the ‘‘lower motor neuron type”; but more precise localization was not possible; one of the reasons being the questionable usefulness of PNTML (cf. Tubaro et al., 2013), the other technical issues related to the root and spinal cord potentials of the pudendal SEP. Thus, the demonstrated abnormalities can derive from anywhere in the reflex arc – from conus to the periphery. The site of the lesion was better defined by Beric et al., who meticulously recorded lumbosacral SEP and reported abnormalities of the R wave (the cauda equina root potential) in the majority of their patients with lumbosacral abnormalities, thus pointing to the nerve roots as the site of the lesion. (In some, only the S wave – spinogram – was abnormal, pointing to myelopathy). (Beric et al., 1987). As Tankisi et al. have demonstrated – in the same patient group as reported in (Tankisi et al., 2016) – also peripheral nervous system involvement in lower limbs (Tankisi et al., 2015), both lumbal and sacral segments were involved (but this has also been claimed by Beric et al. in their larger group of SCI patients (Beric et al.,
1987)). The real question is: are these abnormalities present in all segments below the «primary lesion» (in affected patients), or is there a predilection for the lumbo-sacral segments? Similarly uncertain is the pathophysiology of the reported additional «lower motor neuron type/peripheral nervous system lesions». In previous literature, ‘‘transsynaptic degeneration” was the most often proposed hypothesis to account for peripheral denervation in patients with primary upper motor neuron lesions (Kirshblum et al., 2001). Newly developed compression neuropathies in wheelchair/ bedbound SCI patients might explain abnormalities in lower limbs, but could this also be true for the pudendal nerve? In this respect it is important to point out that Beric et al. have demonstrated urodynamic abnormalities compatible with a ‘‘lower motor neuron type” lesion, as well, thus pointing to a lesion of the autonomic fibers, and necessarily a more widespread involvement of the sacral nervous system than pudendal nerve alone. Such a widespread involvement is most readily explained by a proximal – conus or cauda equina – lesion (Beric et al., 1987). Whatever the cause, the presence of the potential abnormalities below the «obvious» spinal cord lesion in SCI patients has clear practical implications. Whenever in any individual patient the extent or nature of the neurological lesion is uncertain, and especially if irreversible treatment is contemplated, it seems logical to gather quantitative knowledge of the nervous system dysfunction in order to make a rational treatment choice. Of course most patients with cervical or thoracic spinal cord lesions may not require a sophisticated definition of the ‘‘overall” lesion if conservative treatment and rehabilitation produce the expected results. But in selected patients – for instance those undergoing invasive therapeutic interventions related to nervous system function – clinical neurophysiological testing will clarify issues related to the lesion(s) of the spinal cord (and the peripheral nervous system innervating any defined myotomes and dermatomes, also the sacral). Experience with testing patient groups with suspected lesions within the nervous reflex arcs of sacral segments 2–5 has generated the recommendation that the information gained by clinical examination may be enhanced particularly by concentric needle EMG (to diagnose denervation and reinervation of pelvic floor and perineal muscles), and sacral reflex testing (to assess the continuity of the sacral reflex arc) (Tubaro et al., 2013). In summary, further studies should clarify the prevalence and grades of severity of involvement of nervous system segments lower to the primary or «obvious» spinal cord lesion in SCI patients; define the potentially different locations (and causes) of such
http://dx.doi.org/10.1016/j.clinph.2016.01.007 1388-2457/Ó 2016 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
2318
Editorial / Clinical Neurophysiology 127 (2016) 2317–2318
lesions; their clinical relevance, and the place of particular clinical neurophysiological tests in defining these lesions in individual patients. Conflict of interest The author has no conflict of interest. References Beric A, Dimitrijevic MR, Light JK. A clinical syndrome of rostral and caudal spinal injury: neurological, neurophysiological and urodynamic evidence for occult sacral lesion. J Neurol Neurosurg Psychiatry 1987;50:600–6. Blank A, Magora A. Electromyographic investigation of the superficial sphincter ani muscle (SSAM) in spinal cord injury. Electromyogr Clin Neurophysiol 1975;15:261–8. Kirshblum S, Lim S, Garstang S, Millis S. Electrodiagnostic changes in the lower limbs in subjects with chronic complete cervical spinal cord injury. Arch Phys Med Rehabil 2001;82:604–7.
Tankisi H, Pugdahl K, Rasmussen MM, Clemmensen D, Rawashdeh YF, Christensen P, et al. Peripheral nervous system involvement in chronic spinal cord injury. Muscle Nerve 2015;52:1022–62. Tankisi H, Pugdahl K, Rasmussen MM, Clemmensen D, Rawashdeh YF, Christensen P, et al. Pelvic floor electrophysiology in spinal cord injury. Clin Neurophysiol 2016;127(5):2319–24. Tubaro A, Vodušek DB, Amarenco G, Doumouchtsis SK, DeLancey JOL, Fernando R, et al. Imaging, neurophysiological testing and other tests. In: Abrams P, Cardozo L, Khoury S, Wein A, editors. Incontinence. 5th ed. Paris: ICUD – EAU; 2013. p. 507–622.
David B. Vodušek Medical Faculty, University of Ljubljana, Ljubljana, Slovenia E-mail address: [email protected] Available online 23 January 2016