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International Journal of Neuroscience Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ines20
Neural injury by frontal approach of external ventricular drainage in stroke patients a
Yong Min Kwon & Sung Ho Jang
b
a
Department of Physical Medicine, Neurosurgery, and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea b
Chair professor, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea Accepted author version posted online: 22 May 2015.Published online: 27 May 2015.
Click for updates To cite this article: Yong Min Kwon & Sung Ho Jang (2015) Neural injury by frontal approach of external ventricular drainage in stroke patients, International Journal of Neuroscience, 125:10, 742-746, DOI: 10.3109/00207454.2015.1012665 To link to this article: http://dx.doi.org/10.3109/00207454.2015.1012665
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
International Journal of Neuroscience, 2015; 125(10): 742–746 Copyright © 2015 Taylor and Francis ISSN: 0020-7454 print / 1543-5245 online DOI: 10.3109/00207454.2015.1012665
RESEARCH ARTICLE
Neural injury by frontal approach of external ventricular drainage in stroke patients Yong Min Kwon1 and Sung Ho Jang2,∗ 1
Downloaded by [Stockholm University Library] at 22:29 04 September 2015
Department of Physical Medicine, Neurosurgery, and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea; 2 Chair professor, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea Objectives: No study on the characteristics of injury of neural tracts following external ventricular drainage (EVD) in a large number of consecutive patients following EVD has been reported. In this study, using diffusion tensor tractography (DTT), we attempted to investigate the characteristics of injury of neural tracts associated with EVD using a frontal approach in stroke patients. Methods: We recruited 43 consecutive hemorrhagic stroke patients with a history of EVD using a frontal approach. Five neural tracts were reconstructed [corticospinal-tract (CST), corticoreticular-pathway (CRP), arcuate-fasciculus (AF), cingulum, and superior-longitudinal-fasciculus (SLF)]. Results: Among five neural tracts, neural injury by EVD was observed on only two neural tracts (the CRP and the cingulum): CRP—seven (16.3%, five patients—partial tearing and two patients—complete discontinuation) of 43 patients and cingulum—eight (18.6%, eight patients—complete discontinuation of the anterior portion of the cingulum) of 43 patients. Conclusions: It appears that neural injury occurred in a considerable number of patients who underwent EVD; therefore, conduct of further studies on measures to prevent or minimize neural injury by EVD should be encouraged. KEYWORDS: external ventricular drainage, neural tract injury, diffusion tensor tractography, stroke
Introduction External ventricular drainage (EVD), one of the most commonly used neurosurgical procedures, along with shunt operation [1–5], is a freehand procedure for monitoring and managing intracerebral pressure or hemorrhage in patients with intracerebral hemorrhage, intraventricular hemorrhage, and subarachnoid hemorrhage [1, 2, 6, 7]. However, it can cause injury of neural tracts located adjacent to the passage of the catheter of EVD [8]. Yet, little is known about neural injury by EVD. Therefore, accurate performance of EVD could prevent
Received 05 November 2014; revised 23 January 2015; accepted 24 January 2015 Study approval: The study protocol was approved by the Institutional Review Board of Yeungnam University hospital. Correspondence: Sung Ho Jang, MD, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University 317-1, Daemyungdong, Namku, Taegu, 705-717, Republic of Korea. Tel: 82-53-620-3269, Fax: 82-53-620-3269. E-mail: [email protected]
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additional cortical injury, improve neurological status, or save the patient’s life by preventing neural herniation [9–11]. Diffusion tensor tractography (DTT), derived from diffusion tensor imaging (DTI), enables visualization and estimation of neural tracts in three dimensions [12]. A few case studies have reported on injury of neural tracts by invasive neurosurgical procedures such as EVD or shunt operation [11, 13,14]. In addition, a recent DTT study reported on the anterior safe area by analyzing the anatomical location of five neural tracts located in the anterior area of the brain [corticospinal tract (CST), corticoreticular pathway (CRP), cingulum, arcuate fasciculus (AF), and superior longitudinal fasciculus (SLF)] [15]. However, no study on the characteristics of injury of neural tracts following EVD in a large number of consecutive stroke patients has been reported. In the current study, using DTT, we attempted to investigate the characteristics of injury of neural tracts associated with EVD using a frontal approach in stroke patients.
Neural injury by frontal approach of external ventricular drainage
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Subjects and Methods
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Subjects Among 599 stroke patients admitted to the rehabilitation department of a university hospital for rehabilitation during a period of 2.5 years, we recruited 51 patients (28 males, 23 females; mean age 56.1 years, range 30–81) according to the following criteria: (1) history of EVD using a frontal approach, (2) DTI scanning was performed after EVD (mean duration 34 ± 12.8 days; 8–72 days after EVD), and (3) first-ever hemorrhagic stroke, confirmed by a neuro-radiologist, and no history of a neurological or psychiatric disorder. Patients who showed hemorrhage along the catheter passage were excluded. Eight patients with neural injury between the stroke lesion and EVD procedure in whom the etiology of neural injury could not be determined were excluded. Therefore, 43 patients were finally included in our study. Among the 43 patients, 34 patients underwent EVD using a unilateral approach and nine patients underwent EVD using a bilateral approach through their frontal area. All patients underwent surgery in the operating room, which was performed by neurosurgeons; surgery was performed by freehand in 32 patients and with stereotactic guidance in 11 patients. Twenty two age- and sex-matched normal healthy control subjects (14 males, eight females, mean age: 50.1 ± 16.1 years, range: 35–77 years) with no history of a neurological or psychiatric disorder were recruited for this study. This study was conducted retrospectively and the study protocol was approved by the Institutional Review Board of a university hospital.
Diffusion tensor tractography A 6-channel head coil on a 1.5 T Philips Gyroscan Intera (Philips, Best, and Netherlands) with single-shot echo-planar imaging was used for acquisition of DTI data. For each of the 32 noncollinear diffusion sensitizing gradients, we acquired 60 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters were as follows: acquisition matrix = 96 × 96; reconstructed to matrix = 128 × 128; field of view = 221 × 221 mm2 ; TE = 76 ms; TR = 10,726 ms parallel imaging reduction factor (SENSE factor) = 2; NEX = 1; EPI factor = 49; b-value = 1000 s/mm2 ; and a slice thickness of 2.3 mm (acquired voxel size 1.73 × 1.73 × 2.3 mm3 ). Removal of eddy currentinduced image distortions was performed at the Oxford Centre for functional magnetic resonance imaging of brain software library (FSL; www.fmrib.ox.ac.uk/fsl) using affine multi-scale two-dimensional registration [16]. We reconstructed five neural tracts (CST, CRP, cingulum, AF, and SLF) using DTI-Studio software C
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Figure 1.
Schematic overview of patient grouping protocol.
(CMRM, Johns Hopkins Medical Institute, Baltimore, MD, USA). Placement of the two following regions of interest (ROIs) for fiber tracking was based on the fiber assignment continuous tracking algorithm: [17] CST; ROI 1—anterior portion of the upper pons on the axial image, and ROI 2—anterior portion of the lower pons on the axial image [18], CRP: ROI 1—reticular formation of the medulla on the axial image, and ROI 2-tegmentum of the midbrain on the axial image, cingulum: ROI 1—anterior portion of the cingulum area on the coronal image, and ROI 2—posterior portion of the cingulum area on the coronal image [19,20]: AF, ROI 1 the deep white matter of the posterior parietal portion of the SLF on the axial image, and ROI 2—the posterior temporal lobe on the axial image [21], and the SLF, ROI 1 0—a triangular shape just lateral to the CST near the anterior horn of the lateral ventricle on the coronal image, ROI 2—a triangular shape near the posterior horn of the lateral ventricle where the tracts ran from posterior to anterior on the coronal image [22]. Fiber tracking was started at any seed voxel with a fractional anisotropy (FA) > 0.2 and ended at a voxel with a FA of < 0.2 and a tract turning-angle of < 60 degrees. We defined a neural injury when definite injury (complete discontinuation or partial tearing along the passage of EVD) was observed on DTT. Classification was based on the presence of a neural injury by the EVD procedure on DTT: Injured patient subgroup—patients whose neural tract was definitely injured by the EVD procedure, 29 patients with definite neural injury by the stroke lesion only or absence of neural injury were excluded. The FA value and fiber number of each neural tract were measured in the affected hemisphere of the injured patient subgroup and the control group (Fig. 1).
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Table 1. Demographic and diffusion tensor imaging data of the patient and control group.
Age Sex (Male/Female) EVD approach (Unilateral/Bilateral) Diagnosis ICH+IVH+Hydro SAH+IVH+Hydro SAH+IVH ICH+IVH ICH+Hydro Other Incidence of neural injury CST CRP Cingulum AF SLF Duration to DTI after EVD (days) Number of EVD;(one:two:three)
Patient group (n = 43)
Injured group (n = 15)
Control group (n = 22)
56.1 ± 9.7 28/24 40/12
58.4 ± 7.2 6/9 13/2
50.1 ± 16.1 14/8
5 16 2 13 4 3
0 8 0 5 0 2
24 (55.8%) 14(32.6%) 12 (27.9%) 2(4.7%) 2(4.7%) 34 ± 12.8
0 (0.0%) 7 (16.3%) 8 (18.6%) 0 (0.0%) 0 (0.0%) 30 ± 15.9
25:12:6
10:4:1
EVD: external ventricular drainage, IVH: Intraventricularhemorrhage, ICH: Intracerebral hemorrhage, Hydro: Hydrocephalus, SAH: subarachnoid hemorrhage, CST: corticospinal tract, CRP: corticoreticular pathway, AF: arcuate fasciculus, SLF: superior longitudinal fasciculus, DTI: diffusion tensor imaging. Neural injury incidence in Subgroup A: injury by EVD. Neural injury incidence in Subgroup B: injury by stroke lesion or EVD. Values represent mean (±standard deviation).
Statistical analysis Statistical analysis was performed using SPSS 17.0 for Windows (SPSS Inc., Chicago, Ill., USA). The Mann–Whitney U test was used to determine the significances of FA value and fiber number between the injured patient subgroup and the control group. Statistical significance was accepted for p < 0.05.
Results A summary of demographic and DTI data of the patient and control groups is shown in Table 1. As a result, for the CRP, seven (16.3%) of 43 patients belonged to the injured patient subgroup. By contrast, regarding the cingulum, eight patients (18.6%) belonged to the injured patient subgroup. Regarding the configuration of the injury of the CRP, among seven patients with
injury by EVD, five patients (9.6%) showed partial tearing by EVD and two patients (3.8%) showed complete discontinuation. By contrast, all patients (eight patients: 18.6%) who showed cingulum injury showed definite discontinuation of anterior portions of the cingulum on DTT. As a result, among five neural tracts, neural injury by EVD was observed on only two neural tracts (the CRP and the cingulum): CRP—eight (18.6%) of 43 patients and cingulum—seven (16.3%) of 43 patients. We found no infarct in or around the injury site except for the passage of EVD. Detailed injury characteristics of injured patients are shown in Figure 2. The FA value of patients who showed CRP injury in the injured patient subgroup did not differ significantly from that of the control group (p > 0.05), however, the fiber number was significantly lower than in the control group (p < 0.05). By contrast, regarding the cingulum, the FA value was significantly lower than in the control group (p < 0.05). However, no significant difference in the fiber number was observed between patients with injury of the cingulum and those in the control group (Table 2).
Discussion In the current study, using DTT, we investigated the characteristics of injury of neural tracts in consecutive stroke patients who underwent EVD insertion using a frontal approach; our results were as follows: (1) among five neural tracts, neural injury by EVD was observed in only two neural tracts (the CRP and the cingulum): CRP—seven (16.3%, five patients—partial tearing and two patients—complete discontinuation) of 43 patients and cingulum—eight (18.6%, seven patients—complete discontinuation of the anterior portion of the cingulum) of 43 patients, (2) The fiber number of the CRP in patients who showed CRP injury by EVD and the FA value of the cingulum in patients who showed cingulum injury by EVD were lower than in the control group. The FA value indicates the degree of directionality of water diffusion and represents the white matter organization: in detail, the degree of directionality and integrity of white matter microstructures such as axon, myelin, and microtubule [23]. The fiber number reflects the total number of fibers in a neural tract [24]. Therefore, the decreased FA value or fiber numbers suggest injury of a neural tract. As a result, we confirmed neural injury of the CRP and cingulum by EVD in terms of DTI parameters (FA and fiber number) as well as the configuration of the neural tracts. The CRP innervates the proximal muscles of the trunk and leg; therefore, it is mainly involved in gait function [19, 25]. By contrast, the cingulum, the neural fiber bundle extending between the orbitofrontal, parietal, and medial temporal lobe is known International Journal of Neuroscience
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Neural injury by frontal approach of external ventricular drainage
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Injured patient subgroup showed a neural injury by external ventricular drainage (EVD) (red arrows) on brain CT images (left), brain MR images (right), and confirmed by diffusion tensor tractography: the corticoreticular pathway (CRP) and cingulum showed discontinuations (green arrows) in the hemisphere with EVD insertion. Control group showed normal integrity on diffusion tensor tractography for five neural tracts [CST, red; corticoreticular pathway (CRP, sky-blue); cingulum (blue); arcuate fasciculus (AF, green) and superior longitudinal fasciculus (SLF, yellow)].
Figure 2.
to play an important role in diverse cognitive function, such as attention, memory, learning, and motivation [26]. Therefore, patients with neural injury of the CRP and cingulum can show problems in the function of gait and cognition. However, these functions could not be compared due to the various stroke pathologies of patients who underwent EVD procedures. Conduct of further controlled studies on this topic would be necessary. Although many studies have reported on the complications of invasive procedures such as EVD or shunt operation, injuries of neural tracts in the brain caused by these procedures have rarely been reported [11, 13, 14, 27, 28]. Since introduction of DTI, a few case studies have reported on neural injury caused by invasive proTable 2. Comparison of diffusion tensor image parameters of the corticoreticular pathway and cingulum
Subgroup A CRP injury (n = 7) Cingulum injury (n = 8) Control group CRP (n = 22) Cingulum (n = 22)
FA
Fiber number
0.49 ± 0.04 0.42 ± 0.02∗
37.57 ± 34.63∗ 412.62 ± 114.40
0.52 ± 0.03 0.46 ± 0.04
127.52 ± 45.77 474 ± 0.03
CRP: Corticoreticular pathway, FA: fractional anisotrophy. Values represent mean (±standard deviation). ∗ p < 0.05. C
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cedures, including EVD or ventriculo-peritoneal shunt [11, 13, 14]. In 2008, Gold et al. reported on a patient who presented with direct injury to the corticospinal tract and limbic system during revision of a ventriculoperitoneal shunt [14]. In 2012, Kwon and Jang reported on a patient who showed an injury of the cingulum (discontinuation of the left cingulum above the body of the corpus callosum) by ventriculo-peritoneal shunt operation for hydrocephalus following subarachnoid hemorrhage due to rupture of a posterior communicating cerebral artery aneurysm [13]. In a recent study, Kwon and Jang (2013) reported on a patient with bilateral cingulum injury by EVDs, which were performed for subarachnoid and intraventricular-hemorrhage [11]. Therefore, to the best of our knowledge, this study is the first DTI study to evaluate different neural tracts in a large number of consecutive stroke patients. On the other hand, Kwon and Jang (2013) recently reported on the anterior safe area by analyzing the location of five neural tracts (corticospinal tract, corticoreticular pathway, arcuate fasciculus, cingulum, and superior longitudinal fasciculus) [15]. It was found that the common relative safe areas were located at 13.44 mm laterally from the midline and 9.35 mm anteriorly from the anterior commissural line. In conclusion, we investigated neural injury by EVD using an anterior approach; according to our findings, neural injuries by EVD were observed on two neural tracts (the CRP and the cingulum) among five neural
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tracts: CRP—seven (16.3%) and cingulum—eight (18.6%) of 43 patients. Based on our findings, it appears that a significant number of patients who underwent EVD sustained neural injury; therefore, conduct of further studies on measures to prevent or minimize neural injury by EVD should be encouraged. However, limitations of DTI should be considered in interpretation of the results [23]. DTI is a powerful anatomic imaging tool, which can demonstrate gross fiber architecture; however, due to crossing fiber or partial volume effect, DTI can produce both false positive and negative results throughout the white matter of the brain. Therefore, conduct of further studies to overcome these limitations will also be necessary.
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Acknowledgement This work was supported by the 2013 Yeungnam University Research Grant.
Funding statement
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Name of funder: Yeungnam University Research Grant number: 2013.
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Declaration of Interest
17.
The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.
18.
Contributor ship statement Sung Ho Jang: Conceiving and designing the study, funding, data acquisition, manuscript development and manuscript writing. Yong Min Kwon: Manuscript development, data acquisition, manuscript writing and manuscript authorization.
References 1. Dey M, Jaffe J, Stadnik A, et al. External ventricular drainage for intraventricular hemorrhage. Curr Neurol Neurosci Rep 2012;12:24–33. 2. Greenberg MS, Greenberg MS. Handbook of neurosurgery. 7th ed. Tampa, Fla.: Greenberg Graphics; 2010. 3. Wong FW. Cerebrospinal fluid collection: a comparison of different collection sites on the external ventricular drain. Dynamics 2011;22:19–24. 4. Muirhead WR, Basu S. Trajectories for frontal external ventricular drain placement: virtual cannulation of adults with acute hydrocephalus. Br J Neurosurg 2012;26:710–6. 5. Srinivasan VM, O’Neill BR, Jho D, et al. The history of external ventricular drainage. J Neurosurg 2013. 6. Toma AK, Camp S, Watkins LD, et al. External ventricular drain insertion accuracy: is there a need for change
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International Journal of Neuroscience
International Journal of Neuroscience Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ines20
Neural injury by frontal approach of external ventricular drainage in stroke patients a
Yong Min Kwon & Sung Ho Jang
b
a
Department of Physical Medicine, Neurosurgery, and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea b
Chair professor, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea Accepted author version posted online: 22 May 2015.Published online: 27 May 2015.
Click for updates To cite this article: Yong Min Kwon & Sung Ho Jang (2015) Neural injury by frontal approach of external ventricular drainage in stroke patients, International Journal of Neuroscience, 125:10, 742-746, DOI: 10.3109/00207454.2015.1012665 To link to this article: http://dx.doi.org/10.3109/00207454.2015.1012665
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
International Journal of Neuroscience, 2015; 125(10): 742–746 Copyright © 2015 Taylor and Francis ISSN: 0020-7454 print / 1543-5245 online DOI: 10.3109/00207454.2015.1012665
RESEARCH ARTICLE
Neural injury by frontal approach of external ventricular drainage in stroke patients Yong Min Kwon1 and Sung Ho Jang2,∗ 1
Downloaded by [Stockholm University Library] at 22:29 04 September 2015
Department of Physical Medicine, Neurosurgery, and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea; 2 Chair professor, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea Objectives: No study on the characteristics of injury of neural tracts following external ventricular drainage (EVD) in a large number of consecutive patients following EVD has been reported. In this study, using diffusion tensor tractography (DTT), we attempted to investigate the characteristics of injury of neural tracts associated with EVD using a frontal approach in stroke patients. Methods: We recruited 43 consecutive hemorrhagic stroke patients with a history of EVD using a frontal approach. Five neural tracts were reconstructed [corticospinal-tract (CST), corticoreticular-pathway (CRP), arcuate-fasciculus (AF), cingulum, and superior-longitudinal-fasciculus (SLF)]. Results: Among five neural tracts, neural injury by EVD was observed on only two neural tracts (the CRP and the cingulum): CRP—seven (16.3%, five patients—partial tearing and two patients—complete discontinuation) of 43 patients and cingulum—eight (18.6%, eight patients—complete discontinuation of the anterior portion of the cingulum) of 43 patients. Conclusions: It appears that neural injury occurred in a considerable number of patients who underwent EVD; therefore, conduct of further studies on measures to prevent or minimize neural injury by EVD should be encouraged. KEYWORDS: external ventricular drainage, neural tract injury, diffusion tensor tractography, stroke
Introduction External ventricular drainage (EVD), one of the most commonly used neurosurgical procedures, along with shunt operation [1–5], is a freehand procedure for monitoring and managing intracerebral pressure or hemorrhage in patients with intracerebral hemorrhage, intraventricular hemorrhage, and subarachnoid hemorrhage [1, 2, 6, 7]. However, it can cause injury of neural tracts located adjacent to the passage of the catheter of EVD [8]. Yet, little is known about neural injury by EVD. Therefore, accurate performance of EVD could prevent
Received 05 November 2014; revised 23 January 2015; accepted 24 January 2015 Study approval: The study protocol was approved by the Institutional Review Board of Yeungnam University hospital. Correspondence: Sung Ho Jang, MD, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University 317-1, Daemyungdong, Namku, Taegu, 705-717, Republic of Korea. Tel: 82-53-620-3269, Fax: 82-53-620-3269. E-mail: [email protected]
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additional cortical injury, improve neurological status, or save the patient’s life by preventing neural herniation [9–11]. Diffusion tensor tractography (DTT), derived from diffusion tensor imaging (DTI), enables visualization and estimation of neural tracts in three dimensions [12]. A few case studies have reported on injury of neural tracts by invasive neurosurgical procedures such as EVD or shunt operation [11, 13,14]. In addition, a recent DTT study reported on the anterior safe area by analyzing the anatomical location of five neural tracts located in the anterior area of the brain [corticospinal tract (CST), corticoreticular pathway (CRP), cingulum, arcuate fasciculus (AF), and superior longitudinal fasciculus (SLF)] [15]. However, no study on the characteristics of injury of neural tracts following EVD in a large number of consecutive stroke patients has been reported. In the current study, using DTT, we attempted to investigate the characteristics of injury of neural tracts associated with EVD using a frontal approach in stroke patients.
Neural injury by frontal approach of external ventricular drainage
743
Subjects and Methods
Downloaded by [Stockholm University Library] at 22:29 04 September 2015
Subjects Among 599 stroke patients admitted to the rehabilitation department of a university hospital for rehabilitation during a period of 2.5 years, we recruited 51 patients (28 males, 23 females; mean age 56.1 years, range 30–81) according to the following criteria: (1) history of EVD using a frontal approach, (2) DTI scanning was performed after EVD (mean duration 34 ± 12.8 days; 8–72 days after EVD), and (3) first-ever hemorrhagic stroke, confirmed by a neuro-radiologist, and no history of a neurological or psychiatric disorder. Patients who showed hemorrhage along the catheter passage were excluded. Eight patients with neural injury between the stroke lesion and EVD procedure in whom the etiology of neural injury could not be determined were excluded. Therefore, 43 patients were finally included in our study. Among the 43 patients, 34 patients underwent EVD using a unilateral approach and nine patients underwent EVD using a bilateral approach through their frontal area. All patients underwent surgery in the operating room, which was performed by neurosurgeons; surgery was performed by freehand in 32 patients and with stereotactic guidance in 11 patients. Twenty two age- and sex-matched normal healthy control subjects (14 males, eight females, mean age: 50.1 ± 16.1 years, range: 35–77 years) with no history of a neurological or psychiatric disorder were recruited for this study. This study was conducted retrospectively and the study protocol was approved by the Institutional Review Board of a university hospital.
Diffusion tensor tractography A 6-channel head coil on a 1.5 T Philips Gyroscan Intera (Philips, Best, and Netherlands) with single-shot echo-planar imaging was used for acquisition of DTI data. For each of the 32 noncollinear diffusion sensitizing gradients, we acquired 60 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters were as follows: acquisition matrix = 96 × 96; reconstructed to matrix = 128 × 128; field of view = 221 × 221 mm2 ; TE = 76 ms; TR = 10,726 ms parallel imaging reduction factor (SENSE factor) = 2; NEX = 1; EPI factor = 49; b-value = 1000 s/mm2 ; and a slice thickness of 2.3 mm (acquired voxel size 1.73 × 1.73 × 2.3 mm3 ). Removal of eddy currentinduced image distortions was performed at the Oxford Centre for functional magnetic resonance imaging of brain software library (FSL; www.fmrib.ox.ac.uk/fsl) using affine multi-scale two-dimensional registration [16]. We reconstructed five neural tracts (CST, CRP, cingulum, AF, and SLF) using DTI-Studio software C
2015 Taylor and Francis
Figure 1.
Schematic overview of patient grouping protocol.
(CMRM, Johns Hopkins Medical Institute, Baltimore, MD, USA). Placement of the two following regions of interest (ROIs) for fiber tracking was based on the fiber assignment continuous tracking algorithm: [17] CST; ROI 1—anterior portion of the upper pons on the axial image, and ROI 2—anterior portion of the lower pons on the axial image [18], CRP: ROI 1—reticular formation of the medulla on the axial image, and ROI 2-tegmentum of the midbrain on the axial image, cingulum: ROI 1—anterior portion of the cingulum area on the coronal image, and ROI 2—posterior portion of the cingulum area on the coronal image [19,20]: AF, ROI 1 the deep white matter of the posterior parietal portion of the SLF on the axial image, and ROI 2—the posterior temporal lobe on the axial image [21], and the SLF, ROI 1 0—a triangular shape just lateral to the CST near the anterior horn of the lateral ventricle on the coronal image, ROI 2—a triangular shape near the posterior horn of the lateral ventricle where the tracts ran from posterior to anterior on the coronal image [22]. Fiber tracking was started at any seed voxel with a fractional anisotropy (FA) > 0.2 and ended at a voxel with a FA of < 0.2 and a tract turning-angle of < 60 degrees. We defined a neural injury when definite injury (complete discontinuation or partial tearing along the passage of EVD) was observed on DTT. Classification was based on the presence of a neural injury by the EVD procedure on DTT: Injured patient subgroup—patients whose neural tract was definitely injured by the EVD procedure, 29 patients with definite neural injury by the stroke lesion only or absence of neural injury were excluded. The FA value and fiber number of each neural tract were measured in the affected hemisphere of the injured patient subgroup and the control group (Fig. 1).
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Table 1. Demographic and diffusion tensor imaging data of the patient and control group.
Age Sex (Male/Female) EVD approach (Unilateral/Bilateral) Diagnosis ICH+IVH+Hydro SAH+IVH+Hydro SAH+IVH ICH+IVH ICH+Hydro Other Incidence of neural injury CST CRP Cingulum AF SLF Duration to DTI after EVD (days) Number of EVD;(one:two:three)
Patient group (n = 43)
Injured group (n = 15)
Control group (n = 22)
56.1 ± 9.7 28/24 40/12
58.4 ± 7.2 6/9 13/2
50.1 ± 16.1 14/8
5 16 2 13 4 3
0 8 0 5 0 2
24 (55.8%) 14(32.6%) 12 (27.9%) 2(4.7%) 2(4.7%) 34 ± 12.8
0 (0.0%) 7 (16.3%) 8 (18.6%) 0 (0.0%) 0 (0.0%) 30 ± 15.9
25:12:6
10:4:1
EVD: external ventricular drainage, IVH: Intraventricularhemorrhage, ICH: Intracerebral hemorrhage, Hydro: Hydrocephalus, SAH: subarachnoid hemorrhage, CST: corticospinal tract, CRP: corticoreticular pathway, AF: arcuate fasciculus, SLF: superior longitudinal fasciculus, DTI: diffusion tensor imaging. Neural injury incidence in Subgroup A: injury by EVD. Neural injury incidence in Subgroup B: injury by stroke lesion or EVD. Values represent mean (±standard deviation).
Statistical analysis Statistical analysis was performed using SPSS 17.0 for Windows (SPSS Inc., Chicago, Ill., USA). The Mann–Whitney U test was used to determine the significances of FA value and fiber number between the injured patient subgroup and the control group. Statistical significance was accepted for p < 0.05.
Results A summary of demographic and DTI data of the patient and control groups is shown in Table 1. As a result, for the CRP, seven (16.3%) of 43 patients belonged to the injured patient subgroup. By contrast, regarding the cingulum, eight patients (18.6%) belonged to the injured patient subgroup. Regarding the configuration of the injury of the CRP, among seven patients with
injury by EVD, five patients (9.6%) showed partial tearing by EVD and two patients (3.8%) showed complete discontinuation. By contrast, all patients (eight patients: 18.6%) who showed cingulum injury showed definite discontinuation of anterior portions of the cingulum on DTT. As a result, among five neural tracts, neural injury by EVD was observed on only two neural tracts (the CRP and the cingulum): CRP—eight (18.6%) of 43 patients and cingulum—seven (16.3%) of 43 patients. We found no infarct in or around the injury site except for the passage of EVD. Detailed injury characteristics of injured patients are shown in Figure 2. The FA value of patients who showed CRP injury in the injured patient subgroup did not differ significantly from that of the control group (p > 0.05), however, the fiber number was significantly lower than in the control group (p < 0.05). By contrast, regarding the cingulum, the FA value was significantly lower than in the control group (p < 0.05). However, no significant difference in the fiber number was observed between patients with injury of the cingulum and those in the control group (Table 2).
Discussion In the current study, using DTT, we investigated the characteristics of injury of neural tracts in consecutive stroke patients who underwent EVD insertion using a frontal approach; our results were as follows: (1) among five neural tracts, neural injury by EVD was observed in only two neural tracts (the CRP and the cingulum): CRP—seven (16.3%, five patients—partial tearing and two patients—complete discontinuation) of 43 patients and cingulum—eight (18.6%, seven patients—complete discontinuation of the anterior portion of the cingulum) of 43 patients, (2) The fiber number of the CRP in patients who showed CRP injury by EVD and the FA value of the cingulum in patients who showed cingulum injury by EVD were lower than in the control group. The FA value indicates the degree of directionality of water diffusion and represents the white matter organization: in detail, the degree of directionality and integrity of white matter microstructures such as axon, myelin, and microtubule [23]. The fiber number reflects the total number of fibers in a neural tract [24]. Therefore, the decreased FA value or fiber numbers suggest injury of a neural tract. As a result, we confirmed neural injury of the CRP and cingulum by EVD in terms of DTI parameters (FA and fiber number) as well as the configuration of the neural tracts. The CRP innervates the proximal muscles of the trunk and leg; therefore, it is mainly involved in gait function [19, 25]. By contrast, the cingulum, the neural fiber bundle extending between the orbitofrontal, parietal, and medial temporal lobe is known International Journal of Neuroscience
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Neural injury by frontal approach of external ventricular drainage
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Injured patient subgroup showed a neural injury by external ventricular drainage (EVD) (red arrows) on brain CT images (left), brain MR images (right), and confirmed by diffusion tensor tractography: the corticoreticular pathway (CRP) and cingulum showed discontinuations (green arrows) in the hemisphere with EVD insertion. Control group showed normal integrity on diffusion tensor tractography for five neural tracts [CST, red; corticoreticular pathway (CRP, sky-blue); cingulum (blue); arcuate fasciculus (AF, green) and superior longitudinal fasciculus (SLF, yellow)].
Figure 2.
to play an important role in diverse cognitive function, such as attention, memory, learning, and motivation [26]. Therefore, patients with neural injury of the CRP and cingulum can show problems in the function of gait and cognition. However, these functions could not be compared due to the various stroke pathologies of patients who underwent EVD procedures. Conduct of further controlled studies on this topic would be necessary. Although many studies have reported on the complications of invasive procedures such as EVD or shunt operation, injuries of neural tracts in the brain caused by these procedures have rarely been reported [11, 13, 14, 27, 28]. Since introduction of DTI, a few case studies have reported on neural injury caused by invasive proTable 2. Comparison of diffusion tensor image parameters of the corticoreticular pathway and cingulum
Subgroup A CRP injury (n = 7) Cingulum injury (n = 8) Control group CRP (n = 22) Cingulum (n = 22)
FA
Fiber number
0.49 ± 0.04 0.42 ± 0.02∗
37.57 ± 34.63∗ 412.62 ± 114.40
0.52 ± 0.03 0.46 ± 0.04
127.52 ± 45.77 474 ± 0.03
CRP: Corticoreticular pathway, FA: fractional anisotrophy. Values represent mean (±standard deviation). ∗ p < 0.05. C
2015 Taylor and Francis
cedures, including EVD or ventriculo-peritoneal shunt [11, 13, 14]. In 2008, Gold et al. reported on a patient who presented with direct injury to the corticospinal tract and limbic system during revision of a ventriculoperitoneal shunt [14]. In 2012, Kwon and Jang reported on a patient who showed an injury of the cingulum (discontinuation of the left cingulum above the body of the corpus callosum) by ventriculo-peritoneal shunt operation for hydrocephalus following subarachnoid hemorrhage due to rupture of a posterior communicating cerebral artery aneurysm [13]. In a recent study, Kwon and Jang (2013) reported on a patient with bilateral cingulum injury by EVDs, which were performed for subarachnoid and intraventricular-hemorrhage [11]. Therefore, to the best of our knowledge, this study is the first DTI study to evaluate different neural tracts in a large number of consecutive stroke patients. On the other hand, Kwon and Jang (2013) recently reported on the anterior safe area by analyzing the location of five neural tracts (corticospinal tract, corticoreticular pathway, arcuate fasciculus, cingulum, and superior longitudinal fasciculus) [15]. It was found that the common relative safe areas were located at 13.44 mm laterally from the midline and 9.35 mm anteriorly from the anterior commissural line. In conclusion, we investigated neural injury by EVD using an anterior approach; according to our findings, neural injuries by EVD were observed on two neural tracts (the CRP and the cingulum) among five neural
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tracts: CRP—seven (16.3%) and cingulum—eight (18.6%) of 43 patients. Based on our findings, it appears that a significant number of patients who underwent EVD sustained neural injury; therefore, conduct of further studies on measures to prevent or minimize neural injury by EVD should be encouraged. However, limitations of DTI should be considered in interpretation of the results [23]. DTI is a powerful anatomic imaging tool, which can demonstrate gross fiber architecture; however, due to crossing fiber or partial volume effect, DTI can produce both false positive and negative results throughout the white matter of the brain. Therefore, conduct of further studies to overcome these limitations will also be necessary.
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Acknowledgement This work was supported by the 2013 Yeungnam University Research Grant.
Funding statement
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Name of funder: Yeungnam University Research Grant number: 2013.
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Declaration of Interest
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The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.
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Contributor ship statement Sung Ho Jang: Conceiving and designing the study, funding, data acquisition, manuscript development and manuscript writing. Yong Min Kwon: Manuscript development, data acquisition, manuscript writing and manuscript authorization.
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