Intraoperative measurement of spinal cord blood flow in syringomyelia

Clinical Neurology and Neurosurgery 102 (2000) 119 – 123 www.elsevier.com/locate/clineuro

Intraoperative measurement of spinal cord blood flow in syringomyelia William F. Young a,*, Ronald Tuma b, Timothy O’Grady c a

Department of Neurosurgery, Temple Uni6ersity School of Medicine, 3401 North Broad Street, Philadelphia, PA 19140, USA Department of Physiology, Temple Uni6ersity School of Medicine, 3401 North Broad Street, Philadelphia, PA 19140, USA c Department of Anesthesiology, Temple Uni6ersity School of Medicine, 3401 North Broad Street, Philadelphia, PA 19140, USA b

Received 12 April 2000; accepted 27 April 2000

Abstract The role of spinal cord ischemia in the pathophysiology of syringomyelia remains undetermined. Previous reports in the literature suggest that shunting of syringes can improve spinal cord blood flow. In order to determine the effects of syrinx decompression on spinal cord blood flow in patients with syringomyelia, we prospectively measured regional spinal cord blood flow (RSCBF) intraoperatively pre and post shunting in patients with symptomatic syringomyelia using laser doppler flowmetry. Six patients with MRI documented syringomyelia were studied (three with Arnold Chiari I malformation and associated syrinx and three with post-traumatic syringomyelia). Surgery was performed on all patients with either a syringopleural or syringoperitoneal shunt. Laser doppler blood flow and somatosensory evoked potentials were monitored prior to myelotomy and after shunt insertion. Results indicate that there was a significant increase in RSCBF after decompression of the syrinx. This study supports the hypothesis that spinal cord ischemia is important in the pathophysiology of syringomyelia and confirms previous reports in the literature regarding RSCBF in syringomyelia. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Syringomyelia; Laser doppler; Flowmetry

1. Introduction The pathophysiology of syringomyelia remains enigmatic particularly as it relates to its association with hind brain anomalies (e.g. Chiari I malformation) [22,30,36,39,40]. Neurologic deficits are thought to result from syrinx cavity distention and intramedullary pressure on the spinal cord [39,41]. The observation that reduction of cavity size by direct syrinx drainage or restoration of CSF circulation can often result in neurologic improvement serves as evidence that cavity distention is an important pathophysiological factor [4,13,14,20,21,26,28,29,33]. However, few reports have studied the role of other factors such as spinal cord ischemia in the pathophysiology of syringomyelia [24,25]. In this study, we report our findings utilizing laser doppler flowmetry (LDF) to * Corresponding author. Tel.: +1-215-7072225; fax: + 1-2157073831. E-mail address: [email protected] (W.F. Young).

measure regional spinal cord blood flow (RSCB) pre and post syrinx cavity drainage in patients with syringomyelia. This is the third report in the literature to utilize (LDF) in this setting [24,25]. 2. Patients and methods Six patients with symptomatic syringomyelia served as the study group. There were four females and two males. The age range was 22–45 years. The etiology of syringomyelia was Arnold Chiari I (A.C.1) in three patients and post-traumatic in three patients. All patients presented with progressive neurologic deficits: motor weakness (four patients), sensory dysesthesias (three patients), sensory loss (two patients), bladder dysfunction (two patients). Syringomyelia was diagnosed on the basis of magnetic resonance imaging (MRI) in all cases. A distended syrinx was identified on MRI in all cases. Syringes were located in the cervical region in three patients, cervicothoracic in two patients and thoracic in one patient.

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3. Operative technique All patients were operated upon in the prone position. Blood pressure was monitored in all cases using an intraarterial catheter. Mean arterial pressure was maintained at a constant level during somatosensory evoked potential (SSEP) recordings and laser doppler measurements. Blood pressure was maintained at a level no greater than 10 – 20 mmHg above or below the patient’s preoperative baseline.

3.1. Blood flow in syringomyelia Arterial PCO2 was maintained at between 30 and 35 mmHg. The depth of general anesthesia was kept at a constant level during SSEP and LDF recordings. Moreover, core body temperature was monitored with an esophageal probe and kept at a constant level (98.0– 98.9°F). Patients with (A.C.1) malformations underwent a suboccipital craniectomy for decompression of the cerebellar tonsils. A laminectomy was also performed based on the level of the cerebellar tonsils. A duraplasty was performed in all cases of (A.C.1) using a fascia lata graft. A one-to-two level laminectomy was performed to expose all syringes. The area of largest cavity distention was evaluated by MRI, which served as the basis for choosing the level for laminectomy and ultimately the site for catheter insertion. Syrinx drainage was performed by placing the proximal end of a Spetzler lumbar peritoneal catheter (Codman) in to the cavity through a midline myelotomy after opening the dura. The distal end of the catheter was placed either into the pleural space (cervical syrinx) or peritoneal cavity (thoracic syrinx). A zero-pressure (non-valved) shunt system was utilized.

after shunting. SSEP data was analyzed using the paired t-test.

5. Laser Doppler recordings RSCBF was monitored both pre and post shunting using the TSI laser flow blood perfusion monitor (model BPM 403A, St. Paul, MN). A 0.84 mm diameter probe was fixed  1 mm above the widest area of the syrinx and just above the site for planned myelotomy for syrinx drainage. The probe was secured using a clamp attached to the operating room table. Care was taken to avoid areas with large dorsal vessels in order to prevent falsely elevated recordings. The probe was adjusted after placement of the shunt and syrinx decompression to ensure that it remained 1 mm above the spinal cord. Recordings were taken for 5 min prior to shunting and for 5 min after shunting. This duration of measurement has been found to be reliable by other authors [15,24]. Blood flow was recorded and expressed as laser doppler units (LDU), because the laser doppler technique is not a true measure of absolute flow, but a measure of changes in flow. We have extensive experience using laser doppler in experimental models and found it reliable in detecting changes in flow [37,42]. The average of the five RSCBF readings prior to shunting was used as the pre-shunting control value for each patient. Readings from each of the five 1-min post shunting periods were compared to the pre-shunting control value. The Friedman two-way analysis of variance by Rank test was used for comparing pre and post shunting RSCBF values.

6. Postoperative follow-up 4. SSEP monitoring Upper extremity somatosensory evoked potentials (SSEP) were monitored while stimulating the right and left median nerves at the wrists with percutaneous needle electrodes [1]. Lower extremity SSEP’s were recorded using the same montages and percutaneous stimulating needle electrodes in the right and left posterior tibial nerves at the ankles. Recording needle electrodes were placed in the scalp at Fpz-C11, C31 –C41 and Fpz-C7. A biologic explorer system was used for nerve stimulation and recording of SSEP’s. Stimulus intensity ranged from 20 to 40 mA with an average frequency of 4.5 Hz. The recorded signals were amplified and filtered at 30 – 1000 Hz. Acquisition time was a minimum of 50 s, and 250 – 750 stimuli were averaged. SSEP data was acquired continually at 15 – 30-mine intervals at least 2 h prior to shunting and at least 1 h

All patients underwent a postoperative MRI to confirm decompression of the syrinx. Moreover, serial neurological examinations were performed at 1, 3, 6 months and 1 year after surgery.

7. Results Only one patient exhibited improvement in SSEP latency and amplitude (patient 2). SSEP latency and amplitude data was taken at 15, 30 and 60 min prior to shunting and was compared to values 15, 30 and 60 min after syrinx decompression. Therefore, there was not a significant improvement in SSEP’s after syrinx decompression in our study. Table 1 summarizes the blood flow results in the 6 study patients. There was a significant increase in

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RSCBF over the baseline values after decompression of the syrinx (PB 0.001). All 6 patients showed an increase in RSCBF after syrinx drainage. There was evidence of a slight hyperemic response in RSCBF after syrinx drainage. This hyperemic response was exhibited by the fact that the highest RSCBF recording was seen during the first minute after decompression. The increase in RSCBF remained relatively consistent after the initial one minute of recordings. All patients exhibited improvement on subsequent neurological follow-up. In addition, reduction in syrinx size was confirmed on postoperative MRI.

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Post-traumatic syringomyelia is believed to result from an intramedullary hematoma or hematomyelia at the site of a spinal cord injury [2,5,17,19,34]. Arachnoid adhesions at the site of trauma may result in complete subarachnoid block [15,16,32]. The pathophysiology of neurologic damage in syringomyelia is incompletely understood [24,25]. Traditionally, it is thought that pressure effects on spinal cord parenchyma secondary to syringomyelia cavity expansion is an important factor. The importance of other factors such as a spinal cord ischemia has not been studied extensively. LDF is an excellent way of providing real-time regional measurements of blood flow and characterization of microcirculatory events. Most studies have used LDF to evaluate the cerebral microcirculation [3,6,10–12,18,27,31,32,35,38]. Laser doppler flowmetry utilizes infrared light which is emitted through an optical filter [42]. The light is directed through tissue and reflected by moving red blood cells. Blood flow is determined by calculating the product of blood volume and blood velocity. Red blood cells in motion cause a doppler shift proportional to their velocity. The scattered light is reflected back through the probe to a photo detector. This signal is converted to frequency and power information. Frequency correlates with blood velocity and power information to blood volume. Laser doppler flowmetry is not a measure of absolute flow, but is reflective of changes in flow. Thus, values are expressed in arbitrary or laser doppler units (L.D.U.). LDF has been used extensively to study the human cerebral microcirculation. It compares favorably with other techniques including: quantitative autoradiography, radiolabelled microspheres and hydrogen clearance [24]. An important advantage of LDF over other techniques is that it provides realtime continuous measurements. Our study is the third report in the literature to provide information regarding the use of LDF in patients with syringomyelia.

8. Discussion A number of theories have been proposed regarding the pathophysiology of syringomyelia in patients with Chiari malformations [7 – 9,23]. The two theories which are most discussed are those of Williams and Gardner’s hydrodynamic theory, which proposes that intracranial arterial pulsations are transmitted through the central canal producing a ‘water hammer’ effect that enlarges the syrinx. In addition, there is obstruction of the outlets of the fourth ventricle resulting in transmission of the arterial pulse from the choroid plexus down the central canal. Williams’ modifications of the Gardner theory proposes that increases in subarachnoid fluid pressure from increased venous pressure during coughing results in increased CSF pressure. This increase, coupled with the hind brain anomalies, results in a pressure differential between the cistern magna and spinal subarachnoid space. The spinal subarachnoid space experiences a drop in pressure. This results in herniation of the posterior fossa malformation, which acts as a ball valve to trap fluid intracranially. This pressure differential ‘sucks’ CSF into the central canal resulting in syringomyelia.

Table 1 Regional spinal cord blood flow measurements using laser Doppler flowmetry Patient

1 2 3 4 5 6

Age/sex

22 34 28 30 45 35 a

F F M F F M

Diagnosis

AC-1b AC-1 AC-1 PTc PT PT

Pre-shunt (L.D.U.)a 1 min

2 min

3 min

4 min

5 min

1 min

2 min

3 min

4 min

5 min

13.6 20.8 10.2 12.0 12.4 9.6

13.7 18.3 13.4 14.3 10.6 9.8

15.0 18.2 13.4 15.2 8.7 10.0

14.3 18.9 10.9 12.1 8.8 9.8

13.9 19.1 10.8 15.6 8.4 9.8

48.2 52.3 44.5 43.5 43.9 50.7

46.0 50.1 42.7 40.9 40.6 48.6

45.1 49.6 43.4 41.1 42.8 47.2

45.3 49.5 43.3 40.2 42.7 47.2

45.1 48.2 41.7 41.1 41.5 47.3

Laser Doppler units. Arnold Chiari 1 associated syringomyelia. c Post-traumatic syringomyelia. b

Post-shunt (L.D.U.)

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Milhorat et al. were the first to report on LDF measurements in syringomyelia in two separate publications [24,25]. The data in Milhorat’s study was much more variable with regards to pre-shunting values as compared to our study: Milhorat pre-shunt values (0.40 –31.60 L.D.U.) versus our pre-shunt values (8.4– 20.8 L.D.U.). The lower L.D.U. values in Milhorat’s study may be indicative of more severe spinal cord ischemia. Moreover, in Milhorat’s study, flow was increased to a much greater degree after syrinx decompression than in our study: Milhorat post-shunt values (110.4–420.0 L.D.U.) versus our post-shunt values (40.2 –42.3 L.D.U.). Milhorat also demonstrated a greater hyperemic response during recordings taken 1 minute after syrinx decompression. Improvement of SSEP’s was also a more consistent finding in Milhorat’s study. In Milhorat’s study, it was not mentioned whether LDF measurements over large blood vessels was avoided. Measurements over large vessels can cause falsely elevated readings. This fact may explain in part the higher values in Milhorat’s study. Our study provides additional evidence that blood flow is an important factor in the pathophysiology of syringomyelia. The lack of improvement of SSEP’s suggest that LDF may be a more sensitive indicator in our study. However, given the small number of patients, these findings should be interpreted cautiously. Future studies may provide additional insights regarding the role of ischemia in the pathophysiology of syringomyelia.

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