Shaocheng ZHANG ¹, M.D, Laurance JOHNSTON, ², Ph.D., Shuo-Gui XU ¹, M.D., Jingfeng LI ¹, M.D., and Yu PANG ³, M.D.

ABSTRACT:

Objective: To promote additional functional recovery in patients with traumatic, incomplete spinal cord injury (SCI).

Methods: An intradural-lysis and peripheral-nerve implantation microsurgical procedure was performed on 35 patients with obsolete or chronic (i.e., non-acute) incomplete SCI. After the endorachis was opened, fibrous bands adhering to the spinal cord from the arachnoid, pia mater spinalis, ligamenta denticulatum, and initiating part of the nerve-root were removed. The injury site was opened by three to six 0.1-0.2-mm-deep incisions that were slightly longer than the abnormality area. The spinal cord cyst was opened, and its liquid sucked off. Harvested autogenous, sural-nerve segments were stripped of their spineurium and perineurium - making them resemble cauda equine tissue - and implanted into the incisions. Finally, the spinal cord was sutured with pia mater spinalis, and the endorachis was sutured over with a sacrospinal muscular pedicle flap.

Results: Patients were postoperatively followed for a period ranging from 1 to 6 (average 2.5) years. In 32 of 35 cases, sensory and motor function increased at least one grade using the Frankel SCI classification scale; the other three cases recovered only one sensation grade. Of the 32 cases, main upper-leg muscle strength improved one grade in 23 cases and two grades in nine cases. All 32 recovered some ambulatory ability.

Conclusion: Removing the endorhachis adhesions, cutting into the cicatricial spinal cord, and implanting autogenous peripheral-nerve segments enhanced functional recovery in individuals who have obsolete paralysis caused by incomplete SCI.

INTRODUCTION:

Obsolete or chronic paralysis caused by traumatic SCI remains a challenging problem. Although many post-injury changes in the spinal cord can be readily observed with imaging technology, such as MRI, an individual with SCI may, nevertheless, have a near-normal MRI.⁷ Indeed, apart from compression and instability factors, patients with similar MRI changes may have much difference in functional recovery. Through anatomical and surgical observations, we believe that the main factors in these differences are adhesions within the endorachis, resulting, for example, from fibrous strip traction and the traumatic scar and cyst’s overall physical characteristics, including degeneration-related mollescence. Since 1994, we have treated 35 patients, whose functional recovery, we believe, was inhibited by such factors, by microsurgical intradural-lysis and peripheral-nerve implantation procedures. Results indicate that the procedures promoted additional functional recovery.

CLINICAL MATERIAL & METHODS:

Patient Population:

The study group of 35 patients with obsolete or chronic paraplegia (i.e., non-acute) included 30 males and 5 females. Their age ranged from 16 to 42 (average 31) years. Ten, nineteen, and six patients were injured in the thoracic T₇-T₉ region, T₁₀-T₁₂ region, and lumbar L₁-L₂ region, respectively. Seven had been injured from falls from high places, five from heavy objects crashing down on them, three from gunshot, two from knife, and 18 from traffic accidents. The time interval from injury to the surgical intervention ranged from 6 to 26 (average 13) months.

Before the subject surgical intervention (i.e., in the acute stage), decompression and bone-grafting and internal fixation procedures (24 by pedicle screw; 11 by Z plate) had been carried out in all patients. In sixteen, the internal fixation devices had been removed before the microsurgical intervention. In addition, 11 patients were treated with hyperbaric oxygen. Although imaging indicated no compression or instability, three months after decompression and fixation functional recovery had ceased in all patients and remained so until the intradural-lysis and nerve-implantation procedure.

According to the Frankel impairment classification scale,⁴ 31 patients were initially level B, and 4 were level C. (In this scale, A represents a complete injury and E normal function; B through D represent incomplete injuries).

Operative Technique:

Patients were placed in a lateral position and subjected to general anesthesia. After making a midline incision, the endorhachis was exposed and opened with the assistance of a 4-6X forehead microscope. The arachnoid, pia mater spinalis, initiating nerve-root component, and the space between the front and back branch were observed carefully for bands, strips, scars, or adhesions, and for any area affected by ligamenta-denticulatum dragging. Because such elements were small, careful, repeated observations were necessary to ensure therapeutic effectiveness.

The initial part of the nerve root routinely adhered to the spinal cord, with a strip between the front and back nerve-root branch that dragged or pinched the cord. In addition, the adhesion of the arachnoid and the pulling of the ligamenta denticulatum transformed the spinal cord. For example, the pia mater spinalis became thicker and, as a result, adhered and compressed the cord. Adhesions between the spinal cord and the arachnoid, pia mater spinalis, ligamenta denticulatum, nerve root, as well as the peripheral fibrous strip were completely relieved.

After lysis, the injured cord area was opened by three to six 0.1-0.2-mm-deep incisions that were slightly longer than the injury area. If the cyst was one-cm² or bigger as indicated by the pre-surgical MRI or could be clearly observed through its dark-colored, undulant, and thin-walled nature, it was punctured and incisioned, and its fluid sucked off.  

Autogenous sural-nerve segments were harvested corresponding to the length of the area of abnormality. After the segments were microsurgically denuded of their spineurium and perineurium - making them resemble cauda equine tissue, they were implanted into the aforementioned incisions and cyst cavity. Finally, the opened spinal dural was sutured with the pedicle muscular flap and the incision covered with sacrospinal muscle.

RESULTS:

Patients were postoperatively followed for a period ranging from 1 to 6 (average 2.5) years. In 32 of 35 cases, sensory and motor function increased at least one grade using the Frankel SCI classification scale; the other three cases recovered only one sensation grade. Of the 32 cases, main upper-leg muscle strength improved one grade in 23 cases (21 from Frankel B to C, two from C to D) and two grades in nine cases (7 from Frankel B to D and two from C to E). All 32 patients recovered some ambulatory ability. The patients who improved two grades could walk without crutches, and, in the case of the two that improved from Frankel C to E, near-normal function was acquired. In 21 cases, bowel and bladder function clearly improved. Of the six cases who suffered serious nerve-root pain before the operation, pain was completely alleviated in two, slight pain remained in two, and little improvement noted in two.

DISCUSSION:

Rationale for Intradural Lysis: Normally, pia mater spinalis is soft and rich in blood vessels. It clings to the spinal cord’s surface and goes deep into the fissurae mediana anterior at the cord’s front side. Together with nerve roots, it goes through subarachnoid space and connects to the endorachis. On the side surface, there are two rows of triangle ligaments called ligamenta denticulatum, which present two lamina-like layers, starting from the foramina magnum and reaching to the terminal cone at the first lumbar vertebral level.

On the ligamenta denticulatum’s external surface, 19 to 21 dentations extend from the pia mater spinalis in a sawtooth fashion. Their tips push the arachnoid to the outside, and attach to the endorachis’ inner surface between the upper and lower nerve root, fixing the spinal cord. Hence, the pia mater spinalis, arachnoid, two neighboring nerve roots, ligamenta denticulatum between two nerve roots, and the endorachis constitute a relatively separate unit.²

When the spinal cord is injured, dural sac blood will adhere to these tissues, the fibrous scar, and the cord.⁷ Various spinal-cord restricting adhesions were present at the traumatic area in all cases. Spinal-cord deformity caused by harmful ligamenta denticulatum stress traction could also be seen.

The anterior and posterior radicular arteries supply the cord’s blood, and play a compensatory role when the anterior and posterior arteriae mediana are injured. However, when the anterior and posterior radicular arteries as well as the anterior and posterior arteriae mediana are injured or pressed at the same time, the blood supply will be severely compromised, which, in turn, aggravates the injury.

Because the injury area overlaps with surrounding structures and because the scar is thin and slender, function-inhibiting adhesions cannot be clearly seen by CT or sagittal MRI imaging, and the coronary MRI reveals little. Hence, pathological changes cannot be documented by imaging techniques.⁷ These changes cannot be relived by routine fracture reduction, decompression, and fixation procedures because they are routinely undertaken outside the endorachis (Fig 4).

Rationale for Peripheral Nerve Implantation: Because under routine circumstances, an injured neuron cannot be replaced and a damaged axon cannot readily reproduce,⁶ it is difficult for appropriate anatomical and functional connections to be reestablished. Because some intact neurons remain in an incomplete injury, a transplant will bridge them and injured axons, enhancing axonal regeneration potential, and, in turn, spinal-cord functional recovery.⁸

The muscles affected by the necrosis of the anterior gray column cells of the 1st-2nd segments may not be completely paralyzed. However, in a pyramidal tract injury, all muscles controlled by the injured and lower-segment spinal cord are paralyzed. As such, it is important for a potential treatment to accelerate the regeneration of the long-conductive bind and to create regeneration-enhancing conditions for the spinal cord.

Ideally, a graft should not only have bridging capabilities but also be able to provide the appropriate extracellular matrix components and cellular trophic factors conducive to neuronal regeneration.

We believe that autogenous peripheral-nerve segments are good grafting candidates. First, after an incomplete injury, surviving neurons are isolated from each other in islands of non-functional cell mass separated by intervening dead neuronal or micro-scar tissue. If connections can be reestablished between surviving neurons, some conduction through the injury site will be restored. As such, the purpose of our transplantation procedure is to enhance axonal regeneration through the graft’s guiding, bridging, and matrix-supporting characteristics. Such axonal regeneration will help connect the cell-mass islands, forming synaptic junctions between the cord’s contused ends and, in turn, enhancing conduction and functional recovery.  

Second, our microsurgically prepared grafts provide the extracellular foundation and growth factors to trigger the axonal regeneration that forms the basis for regeneration of the long conductive strip. Studies suggest that the cord’s long-conductive strip neurons can penetrate the graft-host interface and form extensive connections that enhance the cord’s functional recovery.

In contrast to other grafting procedures, the spineurium and perineurium of our grafts have been removed, which allows the spinal cord to directly connect and interact with nerve fibers, glial cells, and other beneficial factors that exert guiding effects for regenerating nerve cells. ^5,3

Third, our microsurgically prepared grafts contain important cells, such as Schwann cells and fibroblasts, and a variety of important trophic factors. Because these peripheral-nervous tissue elements are not readily flushed away from the injury area by cerebrospinal fluid, a sustained effect is observed.

Fourth, we believe that our procedures are superior to olfactory or fetal nervous tissue transplantation, or the exogenous or endogenous application of nerve-growth factors. By providing an excellent environment for neuronal regeneration, our grafts promote spinal-cord functional recovery. ⁶ Other advantages include immunological acceptance, ready integration of the graft into the host tissue, no need for highly specialized graft-preparation methodology, and a relatively straightforward, clinically generalized surgery.

Indications for Operation: As mentioned earlier, surgical indications were incomplete paraplegia that showed some functional recovery soon after injury but reached a plateau three months post-injury that continued for an additional three months. Provided that these cases showed no evidence of bone compression, canales spinalis stenosis, or spinal unsteadiness, the injured cord should be surgically examined, and scar tissue completely loosened. As a result, the spinal cord compression is alleviated and blood flow improved.

The basis for the time of operation was that after bone compression and instability was alleviated, the incompletely injured spinal cord had lived through microcirculation disturbance and edema, and nerve function reached its first recovery peak. At the same time, the scar tissue began to grow and reached its peak after three months. If the scar compressed the spinal cord, recovery would cease or even decline. ^1,3

Because three months later the scar began to soften and partly be absorbed, the compression gradually vanished, and the second recovery peak appeared. If the cord’s functional recovery completely ceased at this time, it was concluded that the scar-tissue compression could not be relieved by the body itself; hence, the intradural-lysis procedure should be performed.

For cases who showed no evident bone compression, canales spinalis stenosis and spine unsteadiness in MRI and CT images, yet whose spinal functional recovery had ceased, the compression in the dural sac is likely the main cause. The diminutive scars and fibrous strips are difficult to be observed with imaging techniques. Because they cling to the cord and there is no buffering action of the cerebrospinal fluid and fat as there is outside the endorachis, the influence of these tissues is more direct and serious.

It is always observed that the scar tissue in the dural sac forms laterigrade or tilted strips, compressing the cord. The spinal pulse is observed at the proximal site and disappears at the distal site; after getting rid of the strips, the pulse reappears. Although the intradural-micro-lysis procedure is efficacious, it is neglected in the routine decompression operation, which may help explain the operation’s poor results in some cases. Because our procedures are performed in the dural sac, the surgeon must have rich micro-neurosurgery experience to prevent further functional loss.

CONCLUSION

The main objective of most decompression operations is to eliminate outside compression of the dural sac and stabilize the spine. Intradural scar and adhesion influences on spinal cord functional recovery are often ignored. By completely loosening such scars and adhesions, our microsurgical procedures eliminate these function-inhibiting influences. As a result, significant improvement was noted in all treated patients.

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