Ann Thorac Surg 1997;63:419-424
© 1997 The Society of Thoracic Surgeons
Original Article: Cardiovascular
Intraluminal Shunt for the Thoracic Aorta: Blood Flow and Function in Chronic Studies
Steven J. Van Voorst, MD,
Gregory S. Labranche, DVM,
Samir Rustom, MD,
Alina F. Jukkola, MD,
Charles W. Leffler, PhD
Departments of Surgery, Comparative Medicine, and Physiology/Biophysics, Laboratory for Research in Neonatal Physiology, University of Tennessee College of Medicine; and Veterans Affairs Medical Center, Memphis, Tennessee
Accepted for publication August 17, 1996.
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Abstract
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Background. Aortic cross-clamping during operations on the thoracic aorta may result in paraplegia or kidney failure.
Methods. A nonshunting method of repair was compared with intraluminal shunting in two groups of young pigs: the no-shunt group, which received simple aortic cross-clamping at the ligamentum for 15 minutes; and the shunt group, which received an aortic graft with a temporary intraluminal shunt and balloon occlusion of the inferior vena cava only during shunt insertion and removal. Blood flow to the spinal cord and viscera was measured with radiolabeled microspheres on days 1, 3, 5, and 7 after operation. Renal and neurologic function and histology also were studied.
Results. In the no-shunt group, there was hyperemia of the lumbar cord compared with the shunt group. There were no significant differences in renal cortex blood flow or creatinine clearance. Seven of 10 animals in the no-shunt group had paraplegia, compared with none in the shunt group. Histologic studies of the lower lumbar cord showed bilateral central necrosis of gray matter in the no-shunt group, but no evidence of necrosis in the shunt group.
Conclusions. An intraluminal shunt allowed thoracic aorta reconstruction without paraplegia.
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Introduction
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Reconstruction of the thoracic aorta for traumatic rupture or aneurysm has a high rate of morbidity due to paraplegia and renal failure. Operative management remains controversial because passive external shunting and pump-bypass methods have not completely prevented these complications, and there are multiple potential problems related to extracorporeal circulation. Therefore, many surgeons have abandoned currently used shunt/bypass methods and have espoused the no-shunt ("clamp and sew") technique [1–3]. Because paraplegia, renal failure, and various degrees of injury to other tissues result from ischemia and reperfusion, provision of distal flow during aortic reconstruction would be advantageous.
We have developed a temporary intraluminal shunt to maintain blood flow to the lower half of the body during aortic repair. Sporadic reports dating back to Carrel in 1910 [4] have suggested that a temporary intraluminal shunt may have merit [5–9], but it has not been widely used clinically, probably because of the type of materials initially used (glass and methyl methacrylate) and the lack of experimental data demonstrating significant benefits over other techniques. We have shown previously in acute studies that baseline spinal cord and visceral blood flow can be maintained during a 1-hour period with an intraluminal thoracic aorta shunt [10]. The data also show that there is a "trickle" of blood flow to the lumbar cord and viscera when the aorta is cross-clamped at the ligamentum, and we believe that this is the primary reason for postoperative paraplegia. The intraluminal shunt addresses this problem by providing normal distal blood flow during aortic reconstruction.
To determine the efficacy of this technique, we compared the nonshunting method of repair with intraluminal shunting in two groups of young pigs: the no-shunt group, which received simple aortic cross-clamping at the ligamentum for 15 minutes; and the shunt group, which received an aortic graft with a temporary intraluminal shunt and balloon occlusion of the inferior vena cava (IVC) only during shunt insertion and removal. The animals were observed for 1 week after the procedure, and regional blood flows, proximal arterial pressure, renal and neurologic function, and histology of the spinal cord, kidney, and small intestine were compared between the groups.
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Material and Methods
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Young pigs were chosen for the animal model because of logistic problems associated with disposal of larger radioactive animals. The experimental protocol was approved by the Animal Care and Use Committee of the University of Tennessee, Memphis. All animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985).
Pigs (5 to 7 kg) were given general endotracheal anesthesia using ketamine/acepromazine (35/5 mg/kg) intramuscularly for induction. Maintenance was achieved with inhalation of isoflurane (0.5 to 0.8 vol%), nitrous oxide, and oxygen using a veterinary anesthesia ventilator. Prophylactic antibiotics—penicillin (20,000 U/kg) and gentamicin (3 mg/kg)—were given intramuscularly. Core temperature was monitored by a rectal probe and maintained at 37.8° ± 0.6°C with a circulating water blanket. Under aseptic conditions, operative exposure was obtained by left cervical and posterolateral thoracotomy incisions. To facilitate thoracic exposure, a 1-cm segment of the rib below the intercostal incision was excised posteriorly, and the costochondral junction of the rib above was incised anteriorly. In addition, animals in the shunt group had dissection of the right femoral vein for insertion of a balloon catheter, which was advanced into the IVC. Infant feeding tubes (5F) were placed in the left carotid artery, left internal jugular vein, and left atrium to measure proximal arterial pressure, to administer intravenous fluids, and to inject microspheres, respectively. Catheters were tunneled subcutaneously and exited through stab wounds near the dorsal midline. They were secured to the skin by sutures and cyanoacrylate adhesive. Heparin was used intraoperatively (flush solution) and postoperatively (1,000 U/mL) for catheter patency. Intravenous fluid (0.9% normal saline solution) was administered during the procedure at 100 to 150 mL/h, and dextrose (10 to 15 g intravenously) was given to prevent hypoglycemia. Before wound closure, 0.5% bupivacaine (3 mL diluted to 15 mL) was injected along the intercostal nerve one rib above and below the incision, and atelectatic segments of the left lung were expanded by hyperinflation. Chest tubes were not used. A zippered vest with a side pocket to hold the catheters was placed on the animal after operation. Butorphanol tartrate (0.01 mg/kg intramuscularly) was used for postoperative pain management. Pig milk replacer was resumed on the first postoperative day. Those animals with inadequate oral intake were given supplemental intravenous fluids.
There were two experimental groups. (1) In the no-shunt group (n = 10), the thoracic aorta was cross-clamped at the ligamentum arteriosum for 15 minutes. (2) In the intraluminal shunt group (n = 10), a 1-cm segment of polytetrafluoroethylene graft (10 mm) was sutured into the thoracic aorta just below the ligamentum, using an intraluminal shunt to provide distal blood flow during the anastomoses. The shunt was a 5-cm segment of thin-walled, clear silicone tubing (outer diameter, 
inch; inner diameter, 3/16; inch) with retention rings adhered to both ends with medical-grade silicone adhesive. The distal end was beveled to facilitate insertion. The aorta was cross-clamped proximally between the brachiocephalic trunk and the left subclavian artery and distally above the first aortic intercostal artery while the shunt was inserted and removed. The intraluminal shunt was placed inside the polytetrafluoroethylene graft, and both were inserted into the aorta through a transverse aortotomy. After the shunt was secured with Rummel tourniquets using silicone vessel loops, the aorta was divided completely and the distal anastomosis was performed first, by starting a running suture in the middle of the posterior row. The proximal anastomosis was done next, again starting in the middle of the posterior row. When the proximal anterior row was near completion, the aorta again was cross-clamped, the shunt was removed, thrombi were irrigated from the aortic lumen, and the suture line was completed. To reduce proximal aortic pressure during the two brief periods of cross-clamping, we occluded the IVC with a 5F Pruitt occlusion catheter only during shunt insertion and removal (Fig 1
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Fig 1. . Diagram of the intraluminal shunt technique. The shunt is secured in the lumen of the aorta by Rummel tourniquets using silicone vessel loops. The balloon catheter in the inferior vena cava is inflated only during shunt insertion and removal.
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Regional Blood Flow Determinations
Radiolabeled microspheres were used to determine regional blood flows and cardiac output with the technique described by Heymann and associates [11]. Microspheres, 15 µm in diameter and labeled with scandium 46, cobalt 57, niobium 96, ruthenium 103, stannum 113, or indium 114, were injected through the left atrial catheter. A different isotope was used for each time period. Microspheres were injected during the operation before cross-clamping and on days 1, 3, 5, and 7 after the procedure. Data from the first microsphere injection are not presented because the injection occurred under general anesthesia, and the data are not comparable with the other data, which were taken in awake, unanesthetized animals.
Reference blood samples were withdrawn with a Harvard pump from the left carotid artery catheter at 1.03 mL/min. Radioactivity was measured with a Packard gamma counter, using a count time of 1 minute per specimen. Cardiac output was calculated according to the following formula:
, where Q = cardiac output, Ct = total number of counts injected, Qr = withdrawal rate of the arterial reference blood sample, Cr = counts per minute of the reference blood sample, and Wtkg = the animal's weight in kilograms. A minimum of 1 x 106 counts/min was injected into the animal for each blood flow determination.
Multiple tissue specimens from the spinal cord and viscera were removed at the end of the experiment. The cord was divided into upper, mid-, and lower thoracic and upper and lower lumbar segments. Entire segments of the spinal cord were counted (except for a small sample taken from each for histologic studies), whereas representative sections were taken of the kidneys, gastrointestinal tract, liver, and pancreas. Blood flow was calculated using computer software and reported in mL/min per 100 g of tissue.
Proximal Arterial Pressure
Proximal arterial pressure was recorded through a left carotid artery catheter, which was advanced into the aortic arch. Measurements were taken in all of the no-shunt animals but in 5 of the shunt animals, because of recorder unavailability and one technical problem.
Renal Function
Twenty-four–hour urine collections for creatinine clearance were started the day before operation and were repeated on days 2, 4, and 6 after operation. Serum creatinine levels were determined during the procedure and on postoperative days 3, 5, and 7, at the time of microsphere injection.
Neurologic Function
Animals were observed for their ability to walk after the operation. Those unable to walk because of weakness or paralysis of both rear extremities were determined to be paraplegic.
Histologic Studies
Tissue samples were taken from each of the five segments of spinal cord as well as from kidney and small intestine immediately upon sacrifice of the animal. The specimens were preserved in 10% formalin and stained with hematoxylin and eosin before being reviewed with a pathologist. Specimens were taken from all of the no-shunt animals and 5 of the shunt animals.
Data Analysis
Statistical analyses were performed using analysis of variance with the least-squares method. Values are presented as mean ± standard error of the mean. A p value of 0.05 or less was considered significant.
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Results
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In the no-shunt group (cross-clamp time 15 minutes), the proximal mean arterial pressure increased 63 mm Hg during the cross-clamp period (52 mm Hg baseline to 115 mm Hg cross-clamped). Cardiac output increased daily as the animals recovered from operation (177 to 258 mL•min-1•kg-1). Spinal cord blood flow was increased in the lumbar segments compared with the higher thoracic segments on each of the days after operation (Fig 2). Blood flows to the kidneys and abdominal viscera were maintained after the procedure (Figs 3, 4). Creatinine clearance was not significantly changed from baseline preoperative determinations (16.7 mL/min baseline and 20.9 mL/min on postoperative day 7). Nonshunted animals gained an average of 1.3 kg over the 1-week period of observation (5.9 kg start and 7.2 kg finish). Seven of the 10 nonshunted animals were paraplegic. Four of these 7 were paraplegic immediately after operation; the other 3 animals had onset of paraplegia 3 to 4 days later. Histologic studies of the lower lumbar cord from paraplegic animals showed bilateral central necrosis of gray matter with loss of motor neurons in the anterior horns (Fig 5). Animals with delayed-onset paraplegia had less necrosis of the lower lumbar cord. Histologic analysis of kidneys and small intestine showed no pathologic changes.
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Fig 2. . Spinal cord blood flow in the no-shunt and shunt animals on postoperative days (POD) 1 to 7. (*p  0.05 compared with shunt.)
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Fig 4. . Gastrointestinal tract, pancreas, and liver blood flows in the no-shunt and shunt animals on postoperative days (POD) 1 to 7. (*p 0.05 compared with shunt.)
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Fig 5. . Histology of the lower lumbar cord from no-shunt (A, B) and shunt (C, D) animals. (N = motor neurons present in shunt animals.) (Hematoxylin and eosin; A, C x6.25; B, D x31.25; all before 8% reduction.)
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In the intraluminal shunt group, the proximal mean arterial pressure increased 31 mm Hg during the first of the two aortic cross-clamp periods (52 mm Hg baseline to 83 mm Hg cross-clamped) and 18 mm Hg during the second cross-clamp period (51 mm Hg baseline to 69 mm Hg cross-clamped) (n = 5). An average of 3.2 minutes was required to insert the shunt during the first cross-clamp period (range, 2.7 to 4.3 minutes), and an average of 6.8 minutes was needed to remove the shunt and repair the aorta during the second cross-clamp period (range, 5.7 to 10.3 minutes) (n = 10). Including shunt insertion and removal time, an average of 60.8 minutes was required to implant the aortic graft (range, 50 to 77 minutes). Cardiac output increased slightly each day after operation (range, 158 to 206 mL•min-1•kg-1). Spinal cord, renal cortex, and visceral blood flows increased slightly over the course of the experiment. Creatinine clearance was increased on postoperative day 3, but otherwise was not significantly different from the preoperative baseline clearance (16.6 mL/min baseline and 20.6 mL/min on postoperative day 7). Animals in the shunt group gained an average of 1.7 kg (6.1 kg start and 7.8 kg finish).
None of the shunted animals were paraplegic, but there were two peripheral neuropathies in this group. One animal had a foot drop because of deep placement of an electrocardiogram needle near the sciatic nerve, but was able to stand and walk. The other had a right femoral neuropathy due to electrocautery injury during dissection of the femoral vein, and could not stand. The leg was observed to twitch as electrocautery was used to divide the pudendal artery branches crossing the femoral vein, and there was a superficial burn in the ipsilateral gluteal region, near the location of the inferior margin of the metal ground plate upon which the animal was lying. We believe that this injury was caused by faulty grounding of the electrocautery device. Histologic analysis of the spinal cord from the animal with femoral neuropathy and from 4 other animals in the shunt group revealed no evidence of necrosis. Histologic studies of the kidneys and small intestine from shunted animals were also normal.
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Comment
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This study demonstrates that intraluminal shunting of the thoracic aorta during engraftment prevents postoperative paraplegia, whereas paraplegia developed in 70% of the animals whose thoracic aorta was cross-clamped for 15 minutes.
In the no-shunt group, there was hyperemia of the lumbar cord in the postoperative period compared with shunted animals, as has been shown by others [12]. Blood flow to the abdominal viscera was not significantly altered. Creatinine clearance also was not significantly different from that in the shunted animals after this relatively short cross-clamp period. The main disturbance was in the motor function of these animals; 7 of 10 could not use their hind limbs after operation. The histopathologic results correlated well with the clinical presentation. Those animals that were paralyzed immediately after operation had the most striking central necrosis of the cord gray matter, whereas those animals with delayed onset of paraplegia had an intermediate degree of necrosis. In the intraluminal shunt group, all of the animals could walk after operation, except for 1 that had an injury unrelated to the aortic procedure.
Inferior vena cava occlusion was not used in the no-shunt group, to simulate the "clamp and sew" method currently used clinically. Intermittent IVC occlusion was used in the shunt group for preload reduction to facilitate shunt insertion and removal. These experiments were not designed to measure other possible advantages of IVC occlusion, such as reduced central venous or cerebrospinal fluid pressures. In nonshunted animals, systolic blood pressure increased from 76 mm Hg baseline to 178 mm Hg (+102 mm Hg) during the cross-clamp period (n = 10). On the other hand, in shunted animals with IVC balloon occlusion only during shunt insertion and removal, systolic blood pressure increased from 75 mm Hg baseline to 129 mm Hg (+54 mm Hg) and from 82 mm Hg to 108 mm Hg (+26 mm Hg) during the two clamp periods, respectively (n = 5). Compared with nonshunted animals, those in the shunt group showed a significantly reduced peak systolic pressure with intermittent IVC occlusion (p = 0.0001 for both shunt insertion and removal) (Fig 6). In our studies, the thoracic aorta and IVC were simultaneously occluded for relatively short periods, but in a study in which both vessels were clamped for a longer time, Gelman and associates [13] found no significant change in arterial pressure.
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Fig 6. . Proximal arterial blood pressure (aortic arch) from 2 animals, 1 each representative of the no-shunt and shunt groups. (IVC = inferior vena cava; xclamp = cross-clamp.)
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This is a sensitive animal model for spinal cord ischemia. The reason for its sensitivity is unknown, but may be related to the spinal cord anatomy of pigs, their young age, or the creation of ischemia at normothermia. The high incidence of delayed-onset paraplegia is most likely the result of "borderline" ischemia, as described by Naslund and colleagues [14]. Subclinical neuronal injury is induced in some animals, which then initiates reperfusion injury leading to delayed paraplegia, whereas acute paraplegia is induced in others. Fifteen minutes of occlusion is well below the generally accepted 30 minutes of allowable spinal cord ischemia in humans. The fact that the intraluminal shunt is able to prevent paraplegia in this sensitive model should lend credence to its clinical efficacy. According to the literature, the average cross-clamp time required to repair a ruptured thoracic aorta without a shunt is 32 minutes [15]. With an intraluminal shunt, the aorta also must be cross-clamped to insert (3.2 minutes) and to remove the shunt and complete the aortic repair (6.8 minutes), but these are brief periods compared with the "clamp and sew" method, and they are separated by approximately 50 minutes of normal blood flow while the graft is actually being sutured. The time required for graft implantation is of less physiologic consequence because the intraluminal shunt provides blood flow to distal tissues during this period, thereby diminishing ischemic injury. The shunt gives the surgeon additional time to accomplish the repair without fear of paraplegia. Compared with other methods currently available for thoracic aorta reconstruction, use of the shunt does not require specialized equipment for extracorporeal circulation. We recommend continued investigation of intraluminal shunting for wider clinical use.
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Acknowledgments
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Statistical analyses were performed by Elizabeth Tolley, PhD, Department of Biostatistics and Epidemiology. Technical assistance was provided by Mildred Jackson, Lucille Williams, Debra Van Voorst, and Therese Mangold. This study was supported in part by National Institutes of Health grants HL34059 and HL42851.
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Footnotes
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Address reprint requests to Dr Van Voorst, Department of Surgery, University of Tennessee, 956 Court Ave, Memphis, TN 38163.
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References
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Abstract
Introduction
