Perspectives Commentary on: Clinical Correlates of High Cervical Fractional Anisotropy in Acute Cervical Spinal Cord Injury by Vedantam et al. World Neurosurg 2014 http://dx.doi.org/10.1016/j.wneu.2013.09.017
David J. Hart, M.D. Assistant Professor, Department of Neurological Surgery Case Western Reserve University University Hospitals Case Medical Center
Advanced Imaging Techniques in Cervical Spinal Cord Trauma Fernando Alonso and David J. Hart
T
his issue of WORLD NEUROSURGERY contains a very important article by Vedantam et al. that expands on the use of fractional anisotropy (FA) and diffusion tensor imaging (DTI) in spinal cord injury (SCI). Acute SCI is a condition that carries potentially grave consequences for the patient, the health care system, and society in general. Successful treatment of acute SCI begins with rapid identification and characterization of the injury, and initiation of treatment. Although diagnosis by physical examination remains of the utmost importance, imaging has become a critical and ubiquitous component of assessing patients with acute SCI. Often in the acute trauma setting, computed tomography is the initial imaging of choice due to its low cost, detailed evaluation of bony anatomy, and rapid image acquisition. With a negative computed tomography scan and high clinical suspicion, physicians often rely on magnetic resonance imaging for further delineation of a possible spinal injury. However, recent literature suggests that T2-weighted imaging alone has a low sensitivity for identification of acute myelopathy (2, 5). Furthermore, high signal intensity on T2-weighted images appears in late clinical stages of compression. DTI images of the spinal cord white matter tracts reveal well-organized pathways traveling in different directions, with those oriented in the craniocaudal direction having a higher apparent diffusion coefficient compared with those extending primarily in a transverse direction (12).
Rehabilitation after SCI is of great importance to the functional outcome of patients with such injuries. One vital component of neurological assessment and monitoring in patients with recent acute traumatic myelopathy is assessment of the extent of SCI. Injury in areas below the neurological level of injury are difficult to
Key words Diffusion tensor imaging - Fractional anisotropy - Spinal cord - Spinal cord injury -
Abbreviations and Acronyms DTI: Diffusion tensor imaging FA: Fractional anisotropy SCI: Spinal cord injury
WORLD NEUROSURGERY - [-]: ---, MONTH 2014
assess by physical or electric stimulation given the overriding impairment in sensory and motor function often present in these patients. Patients can also develop ascending neurological deficits as a result of an evolving SCI, therefore making a noninvasive method of spinal cord assessment of the utmost importance (3, 4). Spinal cord trauma in humans often results in spinal cord contusion, and as such DTI and FA measured at the site of injury may not provide reliable data. This is hypothesized to be due to varying combinations of hemorrhage, vascular congestion, impaired perfusion, and ischemic changes to the spinal cord (1, 9). The different SCI patterns between the more chronic process of cervical myelopathy and acute SCI will affect the ability to measure areas of injury with these imaging techniques. The use of DTI and FA is more complex as many of the studies for myelopathy have measured FA at the site of maximal compression, an area that may not be well-suited to measurement in the setting of acute traumatic injury. Permeability, and most notably hemorrhage, within the cord during the acute setting affect the apparent diffusion coefficient and FA, making measurements of spinal cord microstructure rostral to the injury site an interesting proposition. It is reasonable to suspect that such a tactic might allow us to better understand retrograde degeneration and its effect on clinical functional outcome. DTI may assist in the estimation of white matter integrity when an injury produces retrograde degeneration of motor pathways, and thus could aid in prediction of recovery potential for upper limb motor function after injury. DTI in spine imaging has further applications in addition to trauma and has been used to characterize spondylosis, intervertebral
Department of Neurological Surgery, Case Western Reserve University, University Hospitals Case Medical Center, Cleveland, Ohio, USA To whom correspondence should be addressed: David J. Hart, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.10.059
www.WORLDNEUROSURGERY.org
1
PERSPECTIVES
disc herniation, hypertrophy of the ligamentum flavum, facet hypertrophy, and osteophytosis leading to canal stenosis (7, 10). However, in cases of severe compression one must take into consideration different FA values for spinal cord, bone, and cerebrospinal fluid and the difficulty in delineating the area for data calculation (11). Nakamura et al. (8) published a study on diffusion tensor tractography in cervical compressive myelopathy and used a fiber tract ratio, defined as the number of fibers at the site of compression divided by the number of fibers at C2. They found that a fiber tract ratio less than 60% was correlated with a poor recovery rate after laminoplasty. Wen et al. (13) found that FA values in spinal cord compression were a predictor of surgical outcome in patients with spondylotic cervical myelopathy. Freund et al. (6) found that in cervical SCIs with bilateral motor and sensory impairment, FA was significantly lower in both corticospinal tracts when compared with controls (6). Interestingly, this also correlated with a lower FA of the cranial corticospinal tract at the internal capsule level, thus showing that spinal cord degeneration after traumatic injury can parallel brain corticospinal
REFERENCES 1. Cheran S, Shanmuganathan K, Zhuo J, Mirvis SE, Aarabi B, Alexander MT, Gullapalli RP: Correlation of MR diffusion tensor imaging parameters with ASIA motor scores in hemorrhagic and nonhemorrhagic acute spinal cord injury. J Neurotrauma 28:1881-1892, 2011. 2. Demir A, Ries M, Noonen CT, Vital JM, Dehais J, Arne P, Caille JM, Dousset V: Diffusion-weighted MRI imaging with apparent diffusion coefficient and apparent diffusion tensor maps in cervical spondylotic myelopathy. Radiology 229:37-43, 2003. 3. Ellingson BM, Salamon N, Holly LT: Imaging techniques in spinal cord injury. World Neurosurg Dec 12, 2012 [Epub ahead of print]. 4. Ellingson BM, Ulmer JL, Kurpad SN, Schmit BD: Diffusion tensor MR imaging in chronic spinal cord injury. Am J Neuroradiol 29:1976-1982, 2008. 5. Facon D, Ozanne A, Fillard P, Lepeintre JF, Tournoux-Facon C, Ducreux D: MR diffusion tensor imaging and fiber tracking in spinal cord compression. Am J Neuroradiol 26:1587-1594, 2005.
2
www.SCIENCEDIRECT.com
tract degeneration. This is vital in understanding the direction of further studies in elucidating the changes that occur along the neuroaxis during and after acute traumatic central nervous system injury. The fact that in this issue’s article by Vedantam et al. there was variability in timing of American Spinal Injury Association (ASIA) neurological examination may have affected the results. However, rather than judging this simply as a weakness of the study, it should be viewed as an opportunity for the development of further protocols and imaging techniques for victims of polytrauma where a full neurological examination cannot be performed due to a patient’s clinical condition. We believe that the work of Vedantam et al. is a strong step forward in bringing this type of imaging out of the imaging research laboratory and into clinical practice. We look forward to seeing their group and other investigators continue to advance our understanding of the limits and the potential associated with FA and DTI in a variety of clinical situations, whether that be trauma, degenerative conditions, or even demyelination, infection, and/or inflammation.
6. Freund P, Schneider T: Degeneration of the injured cervical cord is associated with remote changes in corticospinal tract integrity and upper limb impairment. PLOS 7:1-7, 2012. 7. Mamata H, Jolesz FA, Maier SE: Apparent diffusion coefficient and fractional anisotropy in spinal cord: age and cervical spondylosis-related changes. J Magn Reson Imaging 22:38-43, 2005. 8. Nakamura M, Fujiyoshi K, Tsuji O, Konomi T, Hosogane N, Watanabe K, Tsuji T, Ishii K, Momoshima S, Toyama Y, Chiba K, Matsumoto M: Clinical significance of diffusion tensor tractography as a predictor of functional recovery after laminoplasty in patients with cervical compressive myelopathy. J Neurosurg Spine 17:147-152, 2012. 9. Shanmuganathan K, Gullapalli RP: Diffusion tensor MR imaging in cervical spine trauma. Am J Neuroradiol 29:655-659, 2008. 10. Song T, Chen WJ, Yang B, Zhao HP, Huang JW, Cai MJ, Dong TF, Li TS: Diffusion tensor imaging in the cervical spinal cord. Eur Spine J 20:422-428, 2011.
diffusion tensor magnetic resonance imaging parameter at 3.0 tesla. Spine 38:407-414, 2013. 12. Virta A, Barnett A, Pierpaoli C: Visualizing and characterizing white matter fiber structure and architecture in the human pyramidal tract using diffusion tensor MRI. Magn Reson Imaging 17: 1121-1133, 1999. 13. Wen CY, Cui JL, Liu HS, Mak KC, Cheung WY, Luk KD, Hu Y: Is diffusion anisotropy a biomarker for disease severity and surgical prognosis of cervical spondylotic myelopathy? Radiology 2013 Aug 13 [Epub ahead of print].
Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.10.059 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
11. Uda T, Takami T, Tsuyuguchi N, Sakamoto S, Yamagata T, Ikeda H, Nagata T, Ohata K: Assessment of cervical spondylotic myelopathy using
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2013.10.059
David J. Hart, M.D. Assistant Professor, Department of Neurological Surgery Case Western Reserve University University Hospitals Case Medical Center
Advanced Imaging Techniques in Cervical Spinal Cord Trauma Fernando Alonso and David J. Hart
T
his issue of WORLD NEUROSURGERY contains a very important article by Vedantam et al. that expands on the use of fractional anisotropy (FA) and diffusion tensor imaging (DTI) in spinal cord injury (SCI). Acute SCI is a condition that carries potentially grave consequences for the patient, the health care system, and society in general. Successful treatment of acute SCI begins with rapid identification and characterization of the injury, and initiation of treatment. Although diagnosis by physical examination remains of the utmost importance, imaging has become a critical and ubiquitous component of assessing patients with acute SCI. Often in the acute trauma setting, computed tomography is the initial imaging of choice due to its low cost, detailed evaluation of bony anatomy, and rapid image acquisition. With a negative computed tomography scan and high clinical suspicion, physicians often rely on magnetic resonance imaging for further delineation of a possible spinal injury. However, recent literature suggests that T2-weighted imaging alone has a low sensitivity for identification of acute myelopathy (2, 5). Furthermore, high signal intensity on T2-weighted images appears in late clinical stages of compression. DTI images of the spinal cord white matter tracts reveal well-organized pathways traveling in different directions, with those oriented in the craniocaudal direction having a higher apparent diffusion coefficient compared with those extending primarily in a transverse direction (12).
Rehabilitation after SCI is of great importance to the functional outcome of patients with such injuries. One vital component of neurological assessment and monitoring in patients with recent acute traumatic myelopathy is assessment of the extent of SCI. Injury in areas below the neurological level of injury are difficult to
Key words Diffusion tensor imaging - Fractional anisotropy - Spinal cord - Spinal cord injury -
Abbreviations and Acronyms DTI: Diffusion tensor imaging FA: Fractional anisotropy SCI: Spinal cord injury
WORLD NEUROSURGERY - [-]: ---, MONTH 2014
assess by physical or electric stimulation given the overriding impairment in sensory and motor function often present in these patients. Patients can also develop ascending neurological deficits as a result of an evolving SCI, therefore making a noninvasive method of spinal cord assessment of the utmost importance (3, 4). Spinal cord trauma in humans often results in spinal cord contusion, and as such DTI and FA measured at the site of injury may not provide reliable data. This is hypothesized to be due to varying combinations of hemorrhage, vascular congestion, impaired perfusion, and ischemic changes to the spinal cord (1, 9). The different SCI patterns between the more chronic process of cervical myelopathy and acute SCI will affect the ability to measure areas of injury with these imaging techniques. The use of DTI and FA is more complex as many of the studies for myelopathy have measured FA at the site of maximal compression, an area that may not be well-suited to measurement in the setting of acute traumatic injury. Permeability, and most notably hemorrhage, within the cord during the acute setting affect the apparent diffusion coefficient and FA, making measurements of spinal cord microstructure rostral to the injury site an interesting proposition. It is reasonable to suspect that such a tactic might allow us to better understand retrograde degeneration and its effect on clinical functional outcome. DTI may assist in the estimation of white matter integrity when an injury produces retrograde degeneration of motor pathways, and thus could aid in prediction of recovery potential for upper limb motor function after injury. DTI in spine imaging has further applications in addition to trauma and has been used to characterize spondylosis, intervertebral
Department of Neurological Surgery, Case Western Reserve University, University Hospitals Case Medical Center, Cleveland, Ohio, USA To whom correspondence should be addressed: David J. Hart, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.10.059
www.WORLDNEUROSURGERY.org
1
PERSPECTIVES
disc herniation, hypertrophy of the ligamentum flavum, facet hypertrophy, and osteophytosis leading to canal stenosis (7, 10). However, in cases of severe compression one must take into consideration different FA values for spinal cord, bone, and cerebrospinal fluid and the difficulty in delineating the area for data calculation (11). Nakamura et al. (8) published a study on diffusion tensor tractography in cervical compressive myelopathy and used a fiber tract ratio, defined as the number of fibers at the site of compression divided by the number of fibers at C2. They found that a fiber tract ratio less than 60% was correlated with a poor recovery rate after laminoplasty. Wen et al. (13) found that FA values in spinal cord compression were a predictor of surgical outcome in patients with spondylotic cervical myelopathy. Freund et al. (6) found that in cervical SCIs with bilateral motor and sensory impairment, FA was significantly lower in both corticospinal tracts when compared with controls (6). Interestingly, this also correlated with a lower FA of the cranial corticospinal tract at the internal capsule level, thus showing that spinal cord degeneration after traumatic injury can parallel brain corticospinal
REFERENCES 1. Cheran S, Shanmuganathan K, Zhuo J, Mirvis SE, Aarabi B, Alexander MT, Gullapalli RP: Correlation of MR diffusion tensor imaging parameters with ASIA motor scores in hemorrhagic and nonhemorrhagic acute spinal cord injury. J Neurotrauma 28:1881-1892, 2011. 2. Demir A, Ries M, Noonen CT, Vital JM, Dehais J, Arne P, Caille JM, Dousset V: Diffusion-weighted MRI imaging with apparent diffusion coefficient and apparent diffusion tensor maps in cervical spondylotic myelopathy. Radiology 229:37-43, 2003. 3. Ellingson BM, Salamon N, Holly LT: Imaging techniques in spinal cord injury. World Neurosurg Dec 12, 2012 [Epub ahead of print]. 4. Ellingson BM, Ulmer JL, Kurpad SN, Schmit BD: Diffusion tensor MR imaging in chronic spinal cord injury. Am J Neuroradiol 29:1976-1982, 2008. 5. Facon D, Ozanne A, Fillard P, Lepeintre JF, Tournoux-Facon C, Ducreux D: MR diffusion tensor imaging and fiber tracking in spinal cord compression. Am J Neuroradiol 26:1587-1594, 2005.
2
www.SCIENCEDIRECT.com
tract degeneration. This is vital in understanding the direction of further studies in elucidating the changes that occur along the neuroaxis during and after acute traumatic central nervous system injury. The fact that in this issue’s article by Vedantam et al. there was variability in timing of American Spinal Injury Association (ASIA) neurological examination may have affected the results. However, rather than judging this simply as a weakness of the study, it should be viewed as an opportunity for the development of further protocols and imaging techniques for victims of polytrauma where a full neurological examination cannot be performed due to a patient’s clinical condition. We believe that the work of Vedantam et al. is a strong step forward in bringing this type of imaging out of the imaging research laboratory and into clinical practice. We look forward to seeing their group and other investigators continue to advance our understanding of the limits and the potential associated with FA and DTI in a variety of clinical situations, whether that be trauma, degenerative conditions, or even demyelination, infection, and/or inflammation.
6. Freund P, Schneider T: Degeneration of the injured cervical cord is associated with remote changes in corticospinal tract integrity and upper limb impairment. PLOS 7:1-7, 2012. 7. Mamata H, Jolesz FA, Maier SE: Apparent diffusion coefficient and fractional anisotropy in spinal cord: age and cervical spondylosis-related changes. J Magn Reson Imaging 22:38-43, 2005. 8. Nakamura M, Fujiyoshi K, Tsuji O, Konomi T, Hosogane N, Watanabe K, Tsuji T, Ishii K, Momoshima S, Toyama Y, Chiba K, Matsumoto M: Clinical significance of diffusion tensor tractography as a predictor of functional recovery after laminoplasty in patients with cervical compressive myelopathy. J Neurosurg Spine 17:147-152, 2012. 9. Shanmuganathan K, Gullapalli RP: Diffusion tensor MR imaging in cervical spine trauma. Am J Neuroradiol 29:655-659, 2008. 10. Song T, Chen WJ, Yang B, Zhao HP, Huang JW, Cai MJ, Dong TF, Li TS: Diffusion tensor imaging in the cervical spinal cord. Eur Spine J 20:422-428, 2011.
diffusion tensor magnetic resonance imaging parameter at 3.0 tesla. Spine 38:407-414, 2013. 12. Virta A, Barnett A, Pierpaoli C: Visualizing and characterizing white matter fiber structure and architecture in the human pyramidal tract using diffusion tensor MRI. Magn Reson Imaging 17: 1121-1133, 1999. 13. Wen CY, Cui JL, Liu HS, Mak KC, Cheung WY, Luk KD, Hu Y: Is diffusion anisotropy a biomarker for disease severity and surgical prognosis of cervical spondylotic myelopathy? Radiology 2013 Aug 13 [Epub ahead of print].
Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.10.059 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
11. Uda T, Takami T, Tsuyuguchi N, Sakamoto S, Yamagata T, Ikeda H, Nagata T, Ohata K: Assessment of cervical spondylotic myelopathy using
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2013.10.059
