Spinal Cord Vascularization by Intact Omentum

Harry S. Goldsmith, MD, Philadelphia, Pennsylvania Serge Duckett, MD; PhD, Philadelphia, Pennsylvania Wei-Fan Chen, MD, Philadelphia, Pennsylvania

A previous report from this laboratory has shown that the intact omentum can be placed directly on the brain of the dog with the subsequent develop- ment of vascular anastomoses between these two structures [I]. It has also been learned recently that the presence of the omentum on the brain can prevent the development of brain infarction when the middle cerebral artery is occluded [2]. The purpose of this paper is to report that vascular connections develop in the dog between the nor- mal spinal cord and omentum when the latter structure is laid on the surface of the cord.

Material and Methods

Fifteen dogs of both sexes, weighing 40 to 60 pounds, were anesthetized with pentobarbital sodium, placed in a prone position, and subjected to laminectomy per- formed at the level of the thirteenth thoracic to first lumbar vertebrae. After laminectomy, the dura was opened and the dorsal aspect of the spinal cord exposed. Cerebrospinal fluid drained freely through the opening in the dura. After the spinal cord was exposed, the wound was protected with saline-soaked gauze bandages and the dog repositioned in a right lateral position. A midline abdominal incision was made and the omentum lengthened by removing it from its junction with the spleen, which required splenectomy, and from its mid- dle and distal attachments to the greater curvature of the stomach. The omentum was then brought out through a new incision located on the left lateral abdom-

From the Departments of Surgery and Neurology, Jefferson Medical Col- lege, Philadelphia, Pennsylvania.

Reprint requests should be addressed to Harry S. Goldsmith, MD, De- partment of Surgery, Jefferson Medical College, 1025 Walnut Street, Philadelphia, Pennsylvania 19107.

inal wall. (Figure 1.) After its exit from the abdominal cavity, the omentum was placed in a subcutaneous tun- nel and laid on the spinal cord. (Figures 2 and 3.) Sever- al sutures were placed between the omentum and the edges of the dura mata to maintain close contact and minimize any sheering effect at the omental-spinal cord interface. The vascular supply to the intact omentum was predominantly through branches from the splenic artery which had been ligated distally.

The abdominal, flank, and dorsal wounds were closed routinely. No abdominal drains were left in the dogs, and they all received 5 cc of Combiotic@ (one million units of procaine penicillin G and 1.25 gm of dyhydro- streptomycin) daily for seven days. A regular canine diet was resumed on the day after surgery.

To determine the rapidity with which vascular con- nections developed at the interface between the omen- turn and spinal cord, dogs were sacrificed at various pe- riods. The number of dogs and the corresponding post- operative periods were: two dogs, four hours; one dog, twelve hours; one dog, twenty-two hours; one dog, twenty-four hours; one dog, two days; one dog, three days; one dog, four days; one dog, six days; one dog, five weeks; one dog, six weeks; one dog, eight weeks; one dog, five and a half months; and two dogs, six months.

Gross identification of the vascular connections that had developed between the omentum, meninges, and spinal cord were clearly evident after the injection of 25 cc of india’ink mixed with neoprene latex (INL) into an omental artery. To be certain the injected INL arrived at the spinal cord only by way of vascular channels with- in the omentum, the spinal cord-omental preparation was removed intact from the dog. This was accom- plished by sectioning the vertebral bodies three seg- ments above and below the level of the previous lami- nectomy. The spinal cord was therefore divided superi- orly and inferiorly in relation to its omental attachment.

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Spinal Cord Vascularization by Intact Omentum

Figure 1. Lengthened omentum brought out of abdominai cavity into incision on left lateral abdomlnai wall.

Portions of the omental-spinal cord preparation were dehydrated in absolute alcohol and cleared with methyl salicylate.

Tissue specimens of the omentum and spinal cord of all the dogs were dehydrated, embedded in paraffin, sec- tioned, and stained with hematoxylin-eosin, hematoxy- lin-van-Gieson, Nissl, and Loyez staining methods for cells and myelin, and phosphotungstic acid-hematoxylin for glial cells.

Results

The omental-spinal cord preparations of all specimens that had been cleared with methyl sali- cylate showed INL in blood vessels in the omen- turn, meninges, and spinal cord. The presence of the INL within blood vessels in the spinal cord re- moved four to forty-eight hours after application of the omentum to the spinal cord was sparse when compared with the amount seen in speci- mens procured three days and thereafter. (Figure

4.1 Observations of histologic sections of the dogs

are presented here in a chronologic sequence based on the postoperative time lapse: (A) Four hours postoperatively (two dogs): The INL was present in vessels of the omentum and meninges and in a few capillaries in the spinal cord. Small hemor- rhages were present at the site of the omental-spi- nal cord interface in the subarachnoid space. (B) Twelve hours postoperatively (one dog): The his- tologic appearance was the same as that seen in the previous specimens. In addition, the majority of white cells present in the hemorrhages were mo- nonuclear. (C) Twenty-two, twenty-four and forty-eight hours postoperatively (three dogs):

Figure 2. Omentwn delivered through subcutaneous tun- nei prior to piacement on spinai cord.

LEVEL : T 13

Figure 3. Cross sectional depiction of cord interface.

omentai-spinai

The meninges at the site of the omental-spinal cord junction were thickened by an infiltration of mononuclear cells and macrophages. Hypertrophy of axons was present in the white matter in the im- mediate vicinity of the omental-spinal cord junc- tion in the forty-eight hour specimen. (0) Three days postoperatively (one dog): Widespread pres- ence of INL was noted in blood vessels within the

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Goldsmith, Duckett, and Chen

Figure 4. Cross sectlon of spinal cord with surrounding omentum seventy-two hours post transposition. Methyl salicylate clearing of the cord shows INL within blood vessels of the spinal cord (arrows).

spinal cord in this dog and all subsequent dogs with longer postoperative survival. Mononuclear cells and macrophages were present in large num- bers in the meninges in the area of the omental- spinal cord junction. Hypertrophied capillaries surrounded by areas of edema, tissue destruction, and loss of neurons were observed in the gray mat- ter of the spinal cord with demyelination in the white matter. (E) Four days postoperatively (one dog): The spinal cord was normal and the sur- rounding meninges were thickened by large num- bers of fibroblasts and collagen. (F) Extended postoperative state (seven dogs): Dogs with post- operative survival longer than four days presented with extensive anastomoses between the omentum and spinal cord which were clearly demonstrated by the presence of INL. The omentum and spinal cord were not observed to have fused, but rather the two structures were separated by a fibrous coat that consisted mainly of fibrocytes and collagen in which anastomotic blood vessels were present. These communicating blood vessels were con- nected between the omentum and meninges, the meninges and spinal cord, but not directly be- tween the omentum and spinal cord. In one speci- men (six weeks postoperative), the omental-spinal cord junction was separated by a thick fibrous coat that was visible to the naked eye. Another speci- men (six months postoperative) developed cystic degeneration of the gray matter that was also visi- ble to the naked eye.

All dogs in this experiment demonstrated INL within blood vessels in the meninges and paren- chyma of the spinal cord after injection of the ma-

terial through an omental artery. The connecting anastomotic channels were established between the omentum and spinal cord possibly as early as four hours after operation and definitely by three days after surgery. The early demonstration of INL in capillaries in the spinal cord within the first few postoperative hours might possibly have resulted from the injected material inadvertently entering blood vessels at a point of hemorrhage rather than through newly established capillaries. However, this possibility was eliminated in speci- mens obtained at seventy-two hours postopera- tively and thereafter, since there was such ‘a wide- spread distribution of INL throughout the spinal cord vessels.

The development of anastomotic channels be- tween the omentum and meninges appeared to re- sult from normal wound healing processes. How- ever, three dogs who had laminectomy early in the experiment demonstrated histologic evidence of spinal cord disease that could have been due to ia- trogenic trauma to the cord at surgery. These pathologic findings consisted of hypertrophied axons in one animal (sacrificed two days postoper- atively), hypertrophied capillaries surrounded by necrosis in the second (sacrificed three days post- operatively), and cystic degeneration in the spinal cord in the third dog (sacrificed six months post- operatively).

It was of interest that in none of the dogs in this experiment did a cerebrospinal fluid fistula devel- op through the incision. This would strongly suggest that the intact omentum has an excellent capacity for absorbing cerebrospinal fluid, a find- ing that may eventually prove to be significant in treating clinical conditions in which there is an ex- cessive amount of cerebrospinal fluid.

Comments

Many problems dealing with spinal cord injuries have not been resolved over the years. Experimen- tal evidence has shown that spinal cord injuries are adversely influenced by a diminished blood flow to the spinal cord [3]. Ducker and Perot [4] noted a progressive fall in spinal cord blood flow at the site of injury with reduction in the partial pressure of oxygen (POz) in the injured area. In addition to diminished blood flow in the ‘area of traumatized cord, Locke et al [5] have shown ele- vation of lactic acid at the injured site [5]. Ost- erholm and associates [6] have suggested that there is an increased amount of norepinephrine in this area which is believed to cause vasoconstric-

264 The Amerkan Journal ol Surgery

Spinal Cord Vascularization by Intact Omentum

tion of blood vessels at the site of trauma resulting in &hernia and necrosis of the spinal cord. It would seem reasonable to suspect that transposing the omentum to an injured spinal cord would add a new source of blood to the structure. This might compensate for the loss of vascular flow resulting from the trauma and could aid in removing injuri- ous biochemical products at the site of injury by way of the network of lymphatic and venous chan- nels that are present within the omentum.

Summary

The intact omentum can be placed directly on the spinal cord with subsequent development of vascular connections at the omental-spinal cord interface. The ability to form vascular connections between these two structures took place in three days and possibly within several hours after sur- gery.

Addendum

On November 6, 1974, an adult female cat had the spinal cord completely transected at the level of the eighth thoracic vertebra, followed by onlay- ing of the intact omentum on the transected site.

The hind limbs of the cat were completely para- lyzed for one month. Shortly thereafter, she began to stand on all four legs. On December 20, the cat took six steps. Presently (February 3, 1975), the cat can walk up to 8 feet before her right hind leg col- lapses. A series of cats have recently had the spinal cord completely transected at the level of the eighth thoracic vertebra to determine whether this phenomenon can be repeated.

References

1. Goidsmith HS. Chen W-F, Duckett SW: Brain vascularization by intact omentum. Arch Surg 106: 695, 1973.

2. Gotdsmfth HS, Chen W-F, Duckett SW: Prevention of cerebral infarction in the dog by intact omentum. Am J Surg accept- ed for publication.

3. Dohrmann GJ, Wagner FC, Bucy PC: The microvasculature in transitory traumatic paraplegia. J Neurosurg 35: 263, 1971.

4. Ducker TB, Perot PL: Local tissue oxygen and blood flow in the acutely injured spinal cord, p 29. Proceedings of the 16th V.A. Spinal Cord Injury Conference. Washington, DC, Veterans Administration, 197 1.

5. Locke GE, Yashon D, Feidman RA, Hunt WE: lschemia in pri- mate spinal cord injury. J Neurosurg 34: 614, 197 1.

6. Osterholm JL, Mathews GJ, Irvin JD. Angeiakos ET: A review of attered norepinephrine metabolism attending severe spi- nal injury, p 17. Proceedings of the 16th V.A. Spinal Cord Injury Conference. Washington, DC, Veterans Administra- tion, 1971.

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