Mechanism of increased cerebrospinal fluid pressure with thoracic aortic occlusion Giancarlo Piano, M D , and Bruce L. Gewertz, M D ,
Chicago, Ill.
Recent clinical reports have suggested that drainage of cerebrospinal fluid lowers the incidence of perioperative paraplegia in patients with thoracoabdominal aneurysms. Unfortunately, the precise mechanisms for both the neurologie deficits and the beneficial effects of cerebrospinal fluid drainage remain unclear. To better understand the relationship between cerebrospinal fluid pressure, central venous pressure, and the compliance of the cerebrospinal fluid compartment, we studied 12 anesthetized dogs subjected to thoracic aortic occlusion. Pericardia were opened in six (group I), and left intact in six (group II). Systemic hemodynamics and cerebrospinal fluid pressure (ram Hg) were measured before and after thoracic aortic occlusion. In group II, intravenous volume loading (15 ml/kg) was superimposed on aortic occlusion. Compliance of the cerebrospinal fluid space (ml/mm Hg) was measured at each interval by use of sequential injection and withdrawal of small aliquots of fluid. Results are expressed as mean + SE; 3*p < 0.05. Thoracic aortic occlusion resulted in predictable changes in mean arterial pressure (group I 95.8 - 7.1 to 123.3 4. 7.1 ~-, group II 82.5 + 6.9 to 98.3 4- 9.53*) and central venous pressure (1.9 4- 0.7 to 3.8 4- 0.63., 3.0 4- 0.8 to 4.0 4- 0.93*). Although cerebrospinal fluid pressure was increased by thoracic aortic occlusion in both groups (8.0 4- 1.2 to 12.6 - 1.93.; 5.8 4. 0.9 to 8.5 4. 1.13.), compliance of the dural space was not changed (0.61 4. 0.19 to 0.60 4- 0.18; 0.54 4- 0.14 to 0.62 4- 0.09). In group II animals cerebrospinal fluid pressure was further increased with volume loading (8.0 4- 1.5 to 13.3 4- 1.53.) and changes in cerebrospinal fluid pressure and central venous pressure were correlated (r = 0.54). The increase in cerebrospinal fluid pressure with volume loading and thoracic aortic occlusion was significantly greater than the increase in eerebrospinal fluid pressure and thoracic aortic occlusion alone (5.3 4- 0.4 vs 2.8 4- 0.63*). Increased cerebrospinal fluid pressure with thoracic aortic occlusion is due to volume changes in venous capacitance beds within the dural space. This change in pressure is not associated with any decrease in compliance; hence, there is no rationale for direct compression of the cord (spinal cord compartment syndrome). Based on anatomic considerations, it appears that any benefits of cerebrospinal fluid drainage reflect enhanced patency of thin-walled intradural veins, which are prone to collapse (Starling resistor concept). Further definition of the complex relationship between central and local venous volumes and pressures may allow a unified explanation for immediate and delayed neurologic deficits. (J VAsc SURG 1990;11:695-701.)
A most dreaded complication o f thoracoabdominal and suprarenal aortic reconstructions is permanent spinal cord injury. A particularly frustrating aspect o f this problem is its relative unpredictability. T o date, no specific anatomic or physiologic indicators can reliably discriminate the patients likely to suffer postoperative paraplegia. Even more puzzling is the fact that paraplegia may occur hours to days after the surgical procedure. From the Department of Surgery, the Universityof Chicago. Presented at the Thirteenth Annual Meeting of the Midwestem Vascular Surgical Society,Chicago, Ill., Sept. 29-30, 1989. Reprint requests: B. L. Gewertz,MD, Professorof Surgery, Section of Vascular Surgery,Universityof Chicago,Box 129, 5841 S. Maryland Ave., Chicago, IL 60637. 24/6/19358
Although the cause o f this complication is undoubtedly multifactorial, the predominant mechanism is thought to be thoracic spinal cord ischemia caused by temporary occlusion o f the aorta during reconstruction and exclusion o f "critical" intercostal vessels. Efforts to reduce the incidence o f paraplegia have included minimization o f aortic occlusion times, preservation o f as many intercostal and lumbar vessels as possible, and maintenance o f distal aortic perfusion with extraanatomic shunts.1 More recently, cerebrospinal fluid (CSF) drainage has been advocated. 2 This maneuver is based on numerous experimental and clinical observations that cerebrospinal fluid pressure (CSFP) often increases substantially with aortic occlusion? ,4 In theory such increases in intrathecal pressure could lower spinal cord perfusion pressure (de695
]'ournal of VASCULAR SURGERY
696 Piano and Gewertz
l~,-fore TAO i3;] After TAO ~[3 Volume Loading
15.0
10.0 z
N \
E E 5.0-
0.0
*
i 'x
Group I
Group 11
Fig. 1. Aortic occlusion resulted in increased CVP, which was augmented by volume loading (*p < 0.05). fined by some as distal aortic pressure minus CSFP). Still unclear, however, is the potentially important contribution of venous pressure to this calculation. We studied anesthetized dogs subjected to thoracic aortic occlusion to better understand the dynamic relationship between CSFP and central venous pressure (CVP). In addition, we determined the compliance of the CSF space in varying conditions to assess if a spinal "compartment syndrome" was present. METHODS All animal care outlined below was in accordance with the Guiding Principles o f the American Physiological Society; the protocol was reviewed and approved by the Animal Care Committee at The University of Chicago. Animal care complied with the "Principles of Laboratory Animal Care" (formulated by the National Society for Medical Research) and the "Guide for the Care andUse of Laboratory Animals" (NIH Publication No, 80-23, revised 1985). Twelve mongrel dogs weighing 20 to 30 kg were sedated with thiamytal sodium (Surital, 10 mg/kg intravenously) and received atropine sulfate (0.5 mg/kg). After intubation, the dogs were ventilated with 2% halothane and 60% oxygen to maintain anesthesia. A constant volume positive pressure animal ventilator (Harvard Instruments, Andover, Mass.) was set at 15 ml/kg tidal volume and 10 to 12 cycles/min to yield an arterial oxygen saturation of greater than 98% and an arterial Pco2 of 30 to
35 torr. Ringer's lactate solution was administered intravenously at a rate of 5 rnl/kg/hr, and the animals were systemically heparinized. The following vessels were cannulated with polyethylene catheters for pressure monitoring: left common carotid artery for proximal systemic arterial pressure, superior vena cava via the right internal jugular vein for CVP, and left femoral artery for distal systemic arterial pressure. Cannulas were connected to Gould Stathum 23 !D transducers (Oxnard, Calif.), which were zero referenced to the right atrium. With the dog positioned in the right lateral decubitus position, an 18-gauge spinal needle was percutaneously introduced into the cisterna magna to monitor CSFP. The CSFP transducers were zero referenced to the level of the cistema magna. The aorta was exposed through a left thoracotomy, and a vessel occlusion snare was positioned around the descending aorta just distal to the left subclavian artery. The six animals in group I were studied after the pericardium was opened widely. The pericardium was left intact in the six animals in group II to allow increases in CVP with volume loading. Protocol Animals were allowed to stabilize for at least 20 minutes. After initial recordings of all systemic hemodynamics, CSFP and dural compliance (subsequently reported as control values), the thoracic aorta was occluded by tightening the vessel occlusion
Volume 11 Number 5 May 1990
Cerebrospinaifluid pressure 697
Table I. Changes in systemic hemodynamics, CSFP and compliance of CSF space; volume ~oading (15 ml/kg) was performed only in group II (~p < 0.05) Mean arterial pressure (mm Hg) Control Postocclusion Volume loading Central venous pressure (ram Hg) Control Postocclusion Volume loading Cerebrospinal fluid pressure (mm Hg) Control Postocdusion Volume loading Compliance ( m l / m m Hg) Control Postocclusion Volume loading
snare. Continuous recordings of the hemodynamic parameters were continued until a steady state was reached 1 to 2 minutes after aortic occlusion. At that time, postocdusion measurements of hemodynamics and dural compliance were recorded. In group II animals volume loading was superimposed on thoracic aortic occlusion. Rapid infusions of 15 ml/kg of normal saline were administered, then measurements of hemodynamics, CSFP, and compliance were repeated (reported as volumeloading values). Animals were killed by injection of a lethal dose o f embutramide (T-61 euthanasia solution, Hoechst-Roussel, Somerville, N.J.). Measurement o f compliance o f cerebrospinal
fluid space Compliance of the CSF space was calculated by use of sequential injection and withdrawal of 2 ml aliquots of normal saline into the CSF compartment according to the method of Marmarou? With this technique, exponential curves are generated by plotting the immediate CSFP response to successive injections and withdrawals of fluid. As would be expected, at higher CSFP disproportionately greater pressure elevations are produced by each successive injection of fluid. Hence, compliance (defined as ~V/A~P) depends strongly on the basal level of CSF pressure. It is useful to convert this single exponential function to a linear function by plotting the pressure response on a logarithmic scale. The slope of the resulting straight line is defined as the pressure volume index (PVI), which is the volume of fluid (expressed in milliliters) necessary to raise the CSFP by
Group I
Group II
95.8 + 7.1 t23.3 +- 7.1 ~ --
82.5 - 6.9 98.3 -+ 9.5 ~ 103.3 + 9.2
1.9 _+ 0.7 3.8 + 0.6 ~ --
3.0 +- 0.8 4.0 +_ 0.9 ~ 10.7 _+ 0.8 °e
8.0 -+ 1.2 12.6 -+- 1.9 ~ --
5.8 ± 0.9 8.5 ± 1.1 ~ 13.3 + 1.5 ~
0.61 -+ 0.19 0.60 _+ 0.18 --
0.54 + 0.14 0.62 _+ 0.09 0.84 _+ 0.09 ~
a factor of 10. Extensive work has confirmed that the compliance (C) of the CSF space is inversely related to the CSF pressure at which it is evaluated, and that this relationship can be expressed as follows: C = 0.4343 PVI/CSFP.
Data analysis All values are reported as mean --_ standard error. Paired t tests were performed within groups as appropriate. Significance was assumed ifp was less than 0.05. RESULTS H e m o d y n a m i c changes Thoracic aortic occlusion resulted hi predictable hemodynamic changes (Table I): proximal mean arterial pressure increased (group I: 95.8 -+ 7.1 to 123.3 + 7.1 mm Hg; group II: 82.5 + 6.9 to 98.3 + 9.5 mm Hg); distal mean arterial pressure decreased (group I: 95.8 + 7.1 to 25.5 -+ 2.7 mm Hg; group II: 82.5 + 6.9 to 21.4 + 3.1 mm Hg); central venous pressure (Fig. 1) increased (group I: 1.9 + 0.7 to 3.8 + 0.6 mm Hg; group II: 3.0 +0.8 to 4.0 _ 0.9 mm Hg). All postocclusion values noted above were significantly different from corresponding control values, p < 0.05. Changes in cerebrospinal fluid pressure and compliance Mean CSFP was slightly higher than mean CVP at control conditions in both groups I and II. Cerebrospinal fluid pressure (Fig. 2) was increased by thoracic aortic occlusion (group I: 8.0 +_ 1.2 to 12.6 + 1.9 mm Hg; group II: 5.8 + 0.9 to 8.5 +
Journal of VASCULAR SURGERY
698 Piano and Gewertz
r--i Before TAO After TAO r - ~ Volume Looding
16.0-
7
/
12.0 -
,/ 3:
E E
A A A A A A A A
8.0
4.0
0.0
Group
I
Group
II
Fig. 2. The increase in CSFP in response to thoracic aortic occlusion was greatest in volume loaded animals (~p < 0.05).
1.1 mm Hg; p < 0.05). The absolute increase in CSFP invariably equalled or exceeded the increase in CVP seen with this maneuver (Fig. 3). Despite these increases in CSFP, compliance of the dural space was not changed by aortic occlusion alone (group I: 0.61 ___ 0.19 to 0.60 -+ 0.18 ml/mm Hg; group II: 0.54 + 0.14 to 0.62 + 0.9 ml/mm Hg) (Fig. 4). In group II animals CSFP was further increased with volume loading (8.0 -+ 1.5 to 13.3 -- 1.5 mm Hg; p < 0.05), and changes in CSFP and CVP were directly correlated (r = 0.54). The increase in CSFP with combined thoracic aortic occlusion and volume loading was significantly greater than the increase in CSFP with aortic occlusion alone (5.3 -- 0.4 vs 2.8 _+ 0.6 rnm Hg; p < 0.05). It is noteworthy that despite the significant increases in CSFP with volume loading, the compliance of the dural space in group II animals after simultaneous aortic occlusion and volume loading was increased (0.70-+ 0.13 to 0.84 + 0.09 ml/mm Hg; p < 0.05). DISCUSSION In 1962 Blaisdell and Cooley4 confirmed previous observations s that there was a rapid rise in CSFP in anesthetized dogs undergoing thoracic aortic occlusion. Drainage of CSF uniformly lowered the incidence of postoperative paraplegia in three different experimental preparations in which intercostal arteries were ligated. McCullough et al.6 directly correlated elevations in CSF pressure with neurologic out-
come and noted that spinal cord perfusion pressure during aortic occlusion (defined as distal aortic pressure-CSFP) was 8 mm Hg lower in those animals experiencing paraplegia. Another study by this group used microspheres to measure regional spinal cord blood flow in both white and grey matter, z Distal thoracic spinal cord blood flow was markedly reduced in untreated animals subjected to thoracic aortic occlusion, whereas those undergoing CSF drainage maintained cord blood flow at near control levels. Perioperative CSF drainage was advocated by Berendes et al.s after they observed a severe neurologic deficit in one patient manifesting extremely high CSF pressures (greater than 40 mm Hg) during clamping of the thoracic aorta. More recently Hollier2 reported encouraging clinical results of this approach. Indeed, monitoring and draining CSF in this setting is rational and unlikely to be harmful. However, other rational approaches to the problem of postoperative paraplegia, including maintenance of distal perfusion by extraanatomic shunts and reattachment of intercostal arteries have been unsuccessful in preventing the complication. 9 Furthermore, in experimental work in primates, Svensson et a1.1°were unable to demonstrate that CSF drainage via laminectomy either maintained spinal cord blood flow or prevented paraplegia. Finally, the occurrence of delayed deficits cannot be well explained by such transient intraoperative increases in CSF pressure.
Volume 11 Number 5 May 1990
Cerebrospinalfluid pressure 699
//
15
m=l
// // // / m
.I-
//
10
o 5
0
~/~// //////////// ////
o'
1o /~
CVP
mm Hg
Big. 3. With aortic occlusion, the increase in CSFP (~P0) was equal to or greater than the increase in CVP (~CVP) (*p < 0.05).
¢P
1.5
r--1 Before TAO I ~ After TAO 1~3 Volume Loading
1.0
T
0.5
f i f //
-rE
/
E
i 0.0
Group I
Group II
Fig. 4. Compliance was not changed by aortic occlusion alone. Volume loading in group II was associated with an increase in compliance (*p < 0.05).
The purpose of this investigation was not to confirm or refute the clinical use of CSF drainage but rather to (1) explain the mechanisms of elevated CSFP and (2) define the relationship of CSFP to central venous volumes and pressures. With thoracic aortic occlusion we observed consistent elevations in CSFP ranging from 2 to 8 mm Fig. Such changes
were correlated with increases in CVP and were exaggerated by superimposed intravenous volume loading in animals with closed pericardium (group II). This correlation was expected based on the classic observations of Queckenstedt in 1916. In other investigations, increases in CSFP have been observed irrespective of the mechanism by which venous pres-
~ournal of VASCULAR SURGERY
700 Piano and Gewertz
V
A
~\\NNNN\NNNNNN\K~
BONE Fig. 5. Starling resistor model applied to spinal cord blood flow (see text). If CSFP exceeds local venous pressure, veins can collapse (arrows) thereby increasing outflow resistance.
sure is elevated (i.e., atrial compression, volume ioading, or aortic occlusion), aa The common mechanism is apparently the increased volume of blood sequestered in veins within the dura and bony neural axis. The largest capacitance beds are the intracranial venom sinuses that would be expected to enlarge with thoracic aortic occlusion in response to the translocation of blood volume to the upper half of the body. a2 This phenomenon ofengorgement ofintracranial venous capacitance beds is responsible for the paradoxic increase in compliance that we saw after volume loading in group II animals. As suggested by Chopp et al.a3 incremental injections of fluid into the dural space compress these venous channels well before the neural parenchyma is compromised. The greater the venous volume, the greater the apparent elastance or compliance o f the dural space. Hence, when intracranial venous sinuses are dilated (e.g., during thoracic aortic occlusion), capacitance is facilitated by a hydraulic "shock absorbing" system. Such a large volurne ofdisplaceable fluid under low pressure may not be present in other situations of increased CSF pressure (e.g., acute subdural hematoma). The dinkal significance of the relationship between CSF and CVP relates to the anatomy of the spinal cord circulation. The principal venous drainage of spinal cord blood flow is via 8 to 12 radicu-
lospinal veins that derive from sinusoidal channels extending along the posterior aspect of the cord. 14 The radiculospinal veins travel through the dural space, narrow considerably as they pass through the dura, and lie in the epidural fat before emptying into larger extradural veins. This somewhat circuitous route creates a physiologic valve mechanism by which the spinal cord is protected against sudden increases in peripheral venous pressure. The collapsible intradural portions of these veins can be modeled as a classic Starling resistor (Fig. 5). a3 When external pressure (CSFP) within the rigid osseous encasement of the spinal cord exceeds that within the veins ("critical dosing pressure"), the tube collapses mad flow decreases or stops depending on inflow pressure, as This pressure can be modified by the active tone within vascular smooth muscle; hence, arteries are less affected by this phenomenon. Our observation that the change in CSF pressure with thoracic aortic occlusion exceeds the change in CVP suggests that the best rationale for CSF drainage is enhanced patency of these thin-walled intradural veins. It must be acknowledged that our measurements of GVP may not directly reflect pressures of hltradural veins. More precise measurement of these pressures without violating dural integrity will be needed to further eluddate these relationships. However, our present data would suggest that the rote of CSF
Volume 11 Number 5 May 1990
drainage in preventing spinal cord ischemia may be quite variable. When venous volumes are low (i.e., during intraoperative blood loss), dural compliance would be decreased since the disptaceable intradural venous volumes would be tow. Even minimal elevations in CSF pressure may then achieve the critical closing pressure. In situations of high venous volumes and pressures, CSF pressure would be less important, and local venous pressure would represent the true outflow resistance. In effect, spinal cord perfusion pressure should be considered as spinal cord perfusion pressure = mean arterial pressure greater value of local venous pressure or CSFP.26 These results do not exclude the fact that drainage of CSF may have a role in thoracoabdominal aortic surgery. They do suggest that further definition of the complex interactions between central and local venous volumes and pressures is needed to allow a unified explanation for immediate and delayed neurologic deficits. The authors gratefully acknowledge the technical assistance o f Silas Brown, consultation and statistical analysis o f Mariann R. Piano, and the manuscript preparation of Eileen M. Wayte. REFERENCES 1. CrwwfordES, Crawford JL, Sail HJ, et at. Thoracoabdominal aortic aneurysms: preoperative and intraoperafive factors determining immediate and long-term results of operations in 605 patients. J VAsc SUF.G 1986;3:389-404. 2. Hollier LH. Protecting the brain and spinal cord. J VAsc SURG 1987;5:524-8. 3. Miyamoto K, Ueno A, Wada T, Kimoto S. A new and simple method of preventing spinal cord damage following temporary occlusion of the thoracic aorta by drairting the cerebrospinal fluid. J Cardiovasc Surg 1960;16:188-97. 4. BlaisdeUFW, Cooley DA. The mecahnism of paraplegia after temporary thoracic aortic occlusion in its relationship to spinal fluid pressure. Surgery 1962;5t:351-5.
Cerebrospinalfluid pressure 701
5. Marmarou A, Shulman K, LaMorgese J. Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 1975;43:523-34. 6. McCutlough JL, HoUier LH, Nugent M. Paraplegia after thoracic aortic occlusion: influence of cerebrospinal fluid drainage; experimental and early clinical results. J VAsc SuRG 1988;7:153-60. 7. Bower TC, Murray M], Gloviczki P, et al, Effects of thoracic aortic occlusion and cerebrospinal fluid drainage on regional spinal cord blood flow in dogs: correlation with neurologic outcome. J VAse St;r,G 1988;9:135-44. 8. Berendes IN, Bredee JJ, Schipperheyn JJ, et al. Mechanism of spinal cord injury after cross-clamping of the descending thoracic aorta. Circtdation 1982;66(suppi):II2-6. 9. Laschinger JC, Cunningham IN, Nathan IM~ et al. Experimental and c~ical assessment of the adequacy of partial bypass in maintenance of spinal cord blood flow during operations on the thoracic aorta. Ann Thorac Surg 1983;36:41726. I0. Svensson LG, Von Ritter C.bl, Groeueveld FIT, et al. Crossclamping of the thoracic aorta: influence of aortic shunts, lamS_nectomy,papaverine, calcium channel blocker, allopurinol and superoxide dismutase on spinal cord blood flow and paraplegia in baboons. Ann Surg 1986;204:38-47. 1I. Raisis JE, Kindt GW, McGillicuddy JE, et al. The effects of primary elevation of cerebral venous pressure on cerebral hemodynamics and intracranial pressure. J Surg Res I979;26: 10I-7. I2. Stene JK, Bums B, Permutt S, et al. Increased cardiac output following occlusion of the descending thoracic aorta in dogs. Am J Physiol 1982;243:R152-8. 13. Chopp M, Pormoy H, Branclx C. Hydraul/c model of the cerebrovasenlar bed: an aid to understanding the volumepressure test. Neurosurgery 1983;13:5-I1. 14. Tadie J, Hemet J, Freger P, et aL Anatomie morphologique et circulatoire des veines de [a moetle (Morphological and functional anatomy, of spmat cord veins). J Neuroradiology I985;12:3-20. 15. Permutt S, Riley RL. Hemodynamics of collapsible vessels with tone: the vascular waterfall. J Appl Physiol 1963;18: 924-32. 16. Wagner EM, Traystman RJr, Hydrostatic determinants of cerebrai perfusion. Crit Care Med 1986;14:484-90.
Chicago, Ill.
Recent clinical reports have suggested that drainage of cerebrospinal fluid lowers the incidence of perioperative paraplegia in patients with thoracoabdominal aneurysms. Unfortunately, the precise mechanisms for both the neurologie deficits and the beneficial effects of cerebrospinal fluid drainage remain unclear. To better understand the relationship between cerebrospinal fluid pressure, central venous pressure, and the compliance of the cerebrospinal fluid compartment, we studied 12 anesthetized dogs subjected to thoracic aortic occlusion. Pericardia were opened in six (group I), and left intact in six (group II). Systemic hemodynamics and cerebrospinal fluid pressure (ram Hg) were measured before and after thoracic aortic occlusion. In group II, intravenous volume loading (15 ml/kg) was superimposed on aortic occlusion. Compliance of the cerebrospinal fluid space (ml/mm Hg) was measured at each interval by use of sequential injection and withdrawal of small aliquots of fluid. Results are expressed as mean + SE; 3*p < 0.05. Thoracic aortic occlusion resulted in predictable changes in mean arterial pressure (group I 95.8 - 7.1 to 123.3 4. 7.1 ~-, group II 82.5 + 6.9 to 98.3 4- 9.53*) and central venous pressure (1.9 4- 0.7 to 3.8 4- 0.63., 3.0 4- 0.8 to 4.0 4- 0.93*). Although cerebrospinal fluid pressure was increased by thoracic aortic occlusion in both groups (8.0 4- 1.2 to 12.6 - 1.93.; 5.8 4. 0.9 to 8.5 4. 1.13.), compliance of the dural space was not changed (0.61 4. 0.19 to 0.60 4- 0.18; 0.54 4- 0.14 to 0.62 4- 0.09). In group II animals cerebrospinal fluid pressure was further increased with volume loading (8.0 4- 1.5 to 13.3 4- 1.53.) and changes in cerebrospinal fluid pressure and central venous pressure were correlated (r = 0.54). The increase in cerebrospinal fluid pressure with volume loading and thoracic aortic occlusion was significantly greater than the increase in eerebrospinal fluid pressure and thoracic aortic occlusion alone (5.3 4- 0.4 vs 2.8 4- 0.63*). Increased cerebrospinal fluid pressure with thoracic aortic occlusion is due to volume changes in venous capacitance beds within the dural space. This change in pressure is not associated with any decrease in compliance; hence, there is no rationale for direct compression of the cord (spinal cord compartment syndrome). Based on anatomic considerations, it appears that any benefits of cerebrospinal fluid drainage reflect enhanced patency of thin-walled intradural veins, which are prone to collapse (Starling resistor concept). Further definition of the complex relationship between central and local venous volumes and pressures may allow a unified explanation for immediate and delayed neurologic deficits. (J VAsc SURG 1990;11:695-701.)
A most dreaded complication o f thoracoabdominal and suprarenal aortic reconstructions is permanent spinal cord injury. A particularly frustrating aspect o f this problem is its relative unpredictability. T o date, no specific anatomic or physiologic indicators can reliably discriminate the patients likely to suffer postoperative paraplegia. Even more puzzling is the fact that paraplegia may occur hours to days after the surgical procedure. From the Department of Surgery, the Universityof Chicago. Presented at the Thirteenth Annual Meeting of the Midwestem Vascular Surgical Society,Chicago, Ill., Sept. 29-30, 1989. Reprint requests: B. L. Gewertz,MD, Professorof Surgery, Section of Vascular Surgery,Universityof Chicago,Box 129, 5841 S. Maryland Ave., Chicago, IL 60637. 24/6/19358
Although the cause o f this complication is undoubtedly multifactorial, the predominant mechanism is thought to be thoracic spinal cord ischemia caused by temporary occlusion o f the aorta during reconstruction and exclusion o f "critical" intercostal vessels. Efforts to reduce the incidence o f paraplegia have included minimization o f aortic occlusion times, preservation o f as many intercostal and lumbar vessels as possible, and maintenance o f distal aortic perfusion with extraanatomic shunts.1 More recently, cerebrospinal fluid (CSF) drainage has been advocated. 2 This maneuver is based on numerous experimental and clinical observations that cerebrospinal fluid pressure (CSFP) often increases substantially with aortic occlusion? ,4 In theory such increases in intrathecal pressure could lower spinal cord perfusion pressure (de695
]'ournal of VASCULAR SURGERY
696 Piano and Gewertz
l~,-fore TAO i3;] After TAO ~[3 Volume Loading
15.0
10.0 z
N \
E E 5.0-
0.0
*
i 'x
Group I
Group 11
Fig. 1. Aortic occlusion resulted in increased CVP, which was augmented by volume loading (*p < 0.05). fined by some as distal aortic pressure minus CSFP). Still unclear, however, is the potentially important contribution of venous pressure to this calculation. We studied anesthetized dogs subjected to thoracic aortic occlusion to better understand the dynamic relationship between CSFP and central venous pressure (CVP). In addition, we determined the compliance of the CSF space in varying conditions to assess if a spinal "compartment syndrome" was present. METHODS All animal care outlined below was in accordance with the Guiding Principles o f the American Physiological Society; the protocol was reviewed and approved by the Animal Care Committee at The University of Chicago. Animal care complied with the "Principles of Laboratory Animal Care" (formulated by the National Society for Medical Research) and the "Guide for the Care andUse of Laboratory Animals" (NIH Publication No, 80-23, revised 1985). Twelve mongrel dogs weighing 20 to 30 kg were sedated with thiamytal sodium (Surital, 10 mg/kg intravenously) and received atropine sulfate (0.5 mg/kg). After intubation, the dogs were ventilated with 2% halothane and 60% oxygen to maintain anesthesia. A constant volume positive pressure animal ventilator (Harvard Instruments, Andover, Mass.) was set at 15 ml/kg tidal volume and 10 to 12 cycles/min to yield an arterial oxygen saturation of greater than 98% and an arterial Pco2 of 30 to
35 torr. Ringer's lactate solution was administered intravenously at a rate of 5 rnl/kg/hr, and the animals were systemically heparinized. The following vessels were cannulated with polyethylene catheters for pressure monitoring: left common carotid artery for proximal systemic arterial pressure, superior vena cava via the right internal jugular vein for CVP, and left femoral artery for distal systemic arterial pressure. Cannulas were connected to Gould Stathum 23 !D transducers (Oxnard, Calif.), which were zero referenced to the right atrium. With the dog positioned in the right lateral decubitus position, an 18-gauge spinal needle was percutaneously introduced into the cisterna magna to monitor CSFP. The CSFP transducers were zero referenced to the level of the cistema magna. The aorta was exposed through a left thoracotomy, and a vessel occlusion snare was positioned around the descending aorta just distal to the left subclavian artery. The six animals in group I were studied after the pericardium was opened widely. The pericardium was left intact in the six animals in group II to allow increases in CVP with volume loading. Protocol Animals were allowed to stabilize for at least 20 minutes. After initial recordings of all systemic hemodynamics, CSFP and dural compliance (subsequently reported as control values), the thoracic aorta was occluded by tightening the vessel occlusion
Volume 11 Number 5 May 1990
Cerebrospinaifluid pressure 697
Table I. Changes in systemic hemodynamics, CSFP and compliance of CSF space; volume ~oading (15 ml/kg) was performed only in group II (~p < 0.05) Mean arterial pressure (mm Hg) Control Postocclusion Volume loading Central venous pressure (ram Hg) Control Postocclusion Volume loading Cerebrospinal fluid pressure (mm Hg) Control Postocdusion Volume loading Compliance ( m l / m m Hg) Control Postocclusion Volume loading
snare. Continuous recordings of the hemodynamic parameters were continued until a steady state was reached 1 to 2 minutes after aortic occlusion. At that time, postocdusion measurements of hemodynamics and dural compliance were recorded. In group II animals volume loading was superimposed on thoracic aortic occlusion. Rapid infusions of 15 ml/kg of normal saline were administered, then measurements of hemodynamics, CSFP, and compliance were repeated (reported as volumeloading values). Animals were killed by injection of a lethal dose o f embutramide (T-61 euthanasia solution, Hoechst-Roussel, Somerville, N.J.). Measurement o f compliance o f cerebrospinal
fluid space Compliance of the CSF space was calculated by use of sequential injection and withdrawal of 2 ml aliquots of normal saline into the CSF compartment according to the method of Marmarou? With this technique, exponential curves are generated by plotting the immediate CSFP response to successive injections and withdrawals of fluid. As would be expected, at higher CSFP disproportionately greater pressure elevations are produced by each successive injection of fluid. Hence, compliance (defined as ~V/A~P) depends strongly on the basal level of CSF pressure. It is useful to convert this single exponential function to a linear function by plotting the pressure response on a logarithmic scale. The slope of the resulting straight line is defined as the pressure volume index (PVI), which is the volume of fluid (expressed in milliliters) necessary to raise the CSFP by
Group I
Group II
95.8 + 7.1 t23.3 +- 7.1 ~ --
82.5 - 6.9 98.3 -+ 9.5 ~ 103.3 + 9.2
1.9 _+ 0.7 3.8 + 0.6 ~ --
3.0 +- 0.8 4.0 +_ 0.9 ~ 10.7 _+ 0.8 °e
8.0 -+ 1.2 12.6 -+- 1.9 ~ --
5.8 ± 0.9 8.5 ± 1.1 ~ 13.3 + 1.5 ~
0.61 -+ 0.19 0.60 _+ 0.18 --
0.54 + 0.14 0.62 _+ 0.09 0.84 _+ 0.09 ~
a factor of 10. Extensive work has confirmed that the compliance (C) of the CSF space is inversely related to the CSF pressure at which it is evaluated, and that this relationship can be expressed as follows: C = 0.4343 PVI/CSFP.
Data analysis All values are reported as mean --_ standard error. Paired t tests were performed within groups as appropriate. Significance was assumed ifp was less than 0.05. RESULTS H e m o d y n a m i c changes Thoracic aortic occlusion resulted hi predictable hemodynamic changes (Table I): proximal mean arterial pressure increased (group I: 95.8 -+ 7.1 to 123.3 + 7.1 mm Hg; group II: 82.5 + 6.9 to 98.3 + 9.5 mm Hg); distal mean arterial pressure decreased (group I: 95.8 + 7.1 to 25.5 -+ 2.7 mm Hg; group II: 82.5 + 6.9 to 21.4 + 3.1 mm Hg); central venous pressure (Fig. 1) increased (group I: 1.9 + 0.7 to 3.8 + 0.6 mm Hg; group II: 3.0 +0.8 to 4.0 _ 0.9 mm Hg). All postocclusion values noted above were significantly different from corresponding control values, p < 0.05. Changes in cerebrospinal fluid pressure and compliance Mean CSFP was slightly higher than mean CVP at control conditions in both groups I and II. Cerebrospinal fluid pressure (Fig. 2) was increased by thoracic aortic occlusion (group I: 8.0 +_ 1.2 to 12.6 + 1.9 mm Hg; group II: 5.8 + 0.9 to 8.5 +
Journal of VASCULAR SURGERY
698 Piano and Gewertz
r--i Before TAO After TAO r - ~ Volume Looding
16.0-
7
/
12.0 -
,/ 3:
E E
A A A A A A A A
8.0
4.0
0.0
Group
I
Group
II
Fig. 2. The increase in CSFP in response to thoracic aortic occlusion was greatest in volume loaded animals (~p < 0.05).
1.1 mm Hg; p < 0.05). The absolute increase in CSFP invariably equalled or exceeded the increase in CVP seen with this maneuver (Fig. 3). Despite these increases in CSFP, compliance of the dural space was not changed by aortic occlusion alone (group I: 0.61 ___ 0.19 to 0.60 -+ 0.18 ml/mm Hg; group II: 0.54 + 0.14 to 0.62 + 0.9 ml/mm Hg) (Fig. 4). In group II animals CSFP was further increased with volume loading (8.0 -+ 1.5 to 13.3 -- 1.5 mm Hg; p < 0.05), and changes in CSFP and CVP were directly correlated (r = 0.54). The increase in CSFP with combined thoracic aortic occlusion and volume loading was significantly greater than the increase in CSFP with aortic occlusion alone (5.3 -- 0.4 vs 2.8 _+ 0.6 rnm Hg; p < 0.05). It is noteworthy that despite the significant increases in CSFP with volume loading, the compliance of the dural space in group II animals after simultaneous aortic occlusion and volume loading was increased (0.70-+ 0.13 to 0.84 + 0.09 ml/mm Hg; p < 0.05). DISCUSSION In 1962 Blaisdell and Cooley4 confirmed previous observations s that there was a rapid rise in CSFP in anesthetized dogs undergoing thoracic aortic occlusion. Drainage of CSF uniformly lowered the incidence of postoperative paraplegia in three different experimental preparations in which intercostal arteries were ligated. McCullough et al.6 directly correlated elevations in CSF pressure with neurologic out-
come and noted that spinal cord perfusion pressure during aortic occlusion (defined as distal aortic pressure-CSFP) was 8 mm Hg lower in those animals experiencing paraplegia. Another study by this group used microspheres to measure regional spinal cord blood flow in both white and grey matter, z Distal thoracic spinal cord blood flow was markedly reduced in untreated animals subjected to thoracic aortic occlusion, whereas those undergoing CSF drainage maintained cord blood flow at near control levels. Perioperative CSF drainage was advocated by Berendes et al.s after they observed a severe neurologic deficit in one patient manifesting extremely high CSF pressures (greater than 40 mm Hg) during clamping of the thoracic aorta. More recently Hollier2 reported encouraging clinical results of this approach. Indeed, monitoring and draining CSF in this setting is rational and unlikely to be harmful. However, other rational approaches to the problem of postoperative paraplegia, including maintenance of distal perfusion by extraanatomic shunts and reattachment of intercostal arteries have been unsuccessful in preventing the complication. 9 Furthermore, in experimental work in primates, Svensson et a1.1°were unable to demonstrate that CSF drainage via laminectomy either maintained spinal cord blood flow or prevented paraplegia. Finally, the occurrence of delayed deficits cannot be well explained by such transient intraoperative increases in CSF pressure.
Volume 11 Number 5 May 1990
Cerebrospinalfluid pressure 699
//
15
m=l
// // // / m
.I-
//
10
o 5
0
~/~// //////////// ////
o'
1o /~
CVP
mm Hg
Big. 3. With aortic occlusion, the increase in CSFP (~P0) was equal to or greater than the increase in CVP (~CVP) (*p < 0.05).
¢P
1.5
r--1 Before TAO I ~ After TAO 1~3 Volume Loading
1.0
T
0.5
f i f //
-rE
/
E
i 0.0
Group I
Group II
Fig. 4. Compliance was not changed by aortic occlusion alone. Volume loading in group II was associated with an increase in compliance (*p < 0.05).
The purpose of this investigation was not to confirm or refute the clinical use of CSF drainage but rather to (1) explain the mechanisms of elevated CSFP and (2) define the relationship of CSFP to central venous volumes and pressures. With thoracic aortic occlusion we observed consistent elevations in CSFP ranging from 2 to 8 mm Fig. Such changes
were correlated with increases in CVP and were exaggerated by superimposed intravenous volume loading in animals with closed pericardium (group II). This correlation was expected based on the classic observations of Queckenstedt in 1916. In other investigations, increases in CSFP have been observed irrespective of the mechanism by which venous pres-
~ournal of VASCULAR SURGERY
700 Piano and Gewertz
V
A
~\\NNNN\NNNNNN\K~
BONE Fig. 5. Starling resistor model applied to spinal cord blood flow (see text). If CSFP exceeds local venous pressure, veins can collapse (arrows) thereby increasing outflow resistance.
sure is elevated (i.e., atrial compression, volume ioading, or aortic occlusion), aa The common mechanism is apparently the increased volume of blood sequestered in veins within the dura and bony neural axis. The largest capacitance beds are the intracranial venom sinuses that would be expected to enlarge with thoracic aortic occlusion in response to the translocation of blood volume to the upper half of the body. a2 This phenomenon ofengorgement ofintracranial venous capacitance beds is responsible for the paradoxic increase in compliance that we saw after volume loading in group II animals. As suggested by Chopp et al.a3 incremental injections of fluid into the dural space compress these venous channels well before the neural parenchyma is compromised. The greater the venous volume, the greater the apparent elastance or compliance o f the dural space. Hence, when intracranial venous sinuses are dilated (e.g., during thoracic aortic occlusion), capacitance is facilitated by a hydraulic "shock absorbing" system. Such a large volurne ofdisplaceable fluid under low pressure may not be present in other situations of increased CSF pressure (e.g., acute subdural hematoma). The dinkal significance of the relationship between CSF and CVP relates to the anatomy of the spinal cord circulation. The principal venous drainage of spinal cord blood flow is via 8 to 12 radicu-
lospinal veins that derive from sinusoidal channels extending along the posterior aspect of the cord. 14 The radiculospinal veins travel through the dural space, narrow considerably as they pass through the dura, and lie in the epidural fat before emptying into larger extradural veins. This somewhat circuitous route creates a physiologic valve mechanism by which the spinal cord is protected against sudden increases in peripheral venous pressure. The collapsible intradural portions of these veins can be modeled as a classic Starling resistor (Fig. 5). a3 When external pressure (CSFP) within the rigid osseous encasement of the spinal cord exceeds that within the veins ("critical dosing pressure"), the tube collapses mad flow decreases or stops depending on inflow pressure, as This pressure can be modified by the active tone within vascular smooth muscle; hence, arteries are less affected by this phenomenon. Our observation that the change in CSF pressure with thoracic aortic occlusion exceeds the change in CVP suggests that the best rationale for CSF drainage is enhanced patency of these thin-walled intradural veins. It must be acknowledged that our measurements of GVP may not directly reflect pressures of hltradural veins. More precise measurement of these pressures without violating dural integrity will be needed to further eluddate these relationships. However, our present data would suggest that the rote of CSF
Volume 11 Number 5 May 1990
drainage in preventing spinal cord ischemia may be quite variable. When venous volumes are low (i.e., during intraoperative blood loss), dural compliance would be decreased since the disptaceable intradural venous volumes would be tow. Even minimal elevations in CSF pressure may then achieve the critical closing pressure. In situations of high venous volumes and pressures, CSF pressure would be less important, and local venous pressure would represent the true outflow resistance. In effect, spinal cord perfusion pressure should be considered as spinal cord perfusion pressure = mean arterial pressure greater value of local venous pressure or CSFP.26 These results do not exclude the fact that drainage of CSF may have a role in thoracoabdominal aortic surgery. They do suggest that further definition of the complex interactions between central and local venous volumes and pressures is needed to allow a unified explanation for immediate and delayed neurologic deficits. The authors gratefully acknowledge the technical assistance o f Silas Brown, consultation and statistical analysis o f Mariann R. Piano, and the manuscript preparation of Eileen M. Wayte. REFERENCES 1. CrwwfordES, Crawford JL, Sail HJ, et at. Thoracoabdominal aortic aneurysms: preoperative and intraoperafive factors determining immediate and long-term results of operations in 605 patients. J VAsc SUF.G 1986;3:389-404. 2. Hollier LH. Protecting the brain and spinal cord. J VAsc SURG 1987;5:524-8. 3. Miyamoto K, Ueno A, Wada T, Kimoto S. A new and simple method of preventing spinal cord damage following temporary occlusion of the thoracic aorta by drairting the cerebrospinal fluid. J Cardiovasc Surg 1960;16:188-97. 4. BlaisdeUFW, Cooley DA. The mecahnism of paraplegia after temporary thoracic aortic occlusion in its relationship to spinal fluid pressure. Surgery 1962;5t:351-5.
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5. Marmarou A, Shulman K, LaMorgese J. Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 1975;43:523-34. 6. McCutlough JL, HoUier LH, Nugent M. Paraplegia after thoracic aortic occlusion: influence of cerebrospinal fluid drainage; experimental and early clinical results. J VAsc SuRG 1988;7:153-60. 7. Bower TC, Murray M], Gloviczki P, et al, Effects of thoracic aortic occlusion and cerebrospinal fluid drainage on regional spinal cord blood flow in dogs: correlation with neurologic outcome. J VAse St;r,G 1988;9:135-44. 8. Berendes IN, Bredee JJ, Schipperheyn JJ, et al. Mechanism of spinal cord injury after cross-clamping of the descending thoracic aorta. Circtdation 1982;66(suppi):II2-6. 9. Laschinger JC, Cunningham IN, Nathan IM~ et al. Experimental and c~ical assessment of the adequacy of partial bypass in maintenance of spinal cord blood flow during operations on the thoracic aorta. Ann Thorac Surg 1983;36:41726. I0. Svensson LG, Von Ritter C.bl, Groeueveld FIT, et al. Crossclamping of the thoracic aorta: influence of aortic shunts, lamS_nectomy,papaverine, calcium channel blocker, allopurinol and superoxide dismutase on spinal cord blood flow and paraplegia in baboons. Ann Surg 1986;204:38-47. 1I. Raisis JE, Kindt GW, McGillicuddy JE, et al. The effects of primary elevation of cerebral venous pressure on cerebral hemodynamics and intracranial pressure. J Surg Res I979;26: 10I-7. I2. Stene JK, Bums B, Permutt S, et al. Increased cardiac output following occlusion of the descending thoracic aorta in dogs. Am J Physiol 1982;243:R152-8. 13. Chopp M, Pormoy H, Branclx C. Hydraul/c model of the cerebrovasenlar bed: an aid to understanding the volumepressure test. Neurosurgery 1983;13:5-I1. 14. Tadie J, Hemet J, Freger P, et aL Anatomie morphologique et circulatoire des veines de [a moetle (Morphological and functional anatomy, of spmat cord veins). J Neuroradiology I985;12:3-20. 15. Permutt S, Riley RL. Hemodynamics of collapsible vessels with tone: the vascular waterfall. J Appl Physiol 1963;18: 924-32. 16. Wagner EM, Traystman RJr, Hydrostatic determinants of cerebrai perfusion. Crit Care Med 1986;14:484-90.
