Innervation of parasympathetic postganglionic neurons and bladder detrusor muscle directly after sacral root transection and repair using nerve transfer

Abstract

Aims-This is a continuation of studies examining the effectiveness of root repairs and nerve transfers for bladder reinnervation. Our previous retrograde fluorogold tracing studies from the bladder to the spinal cord found regrowth of axons from the spinal cord through the nerve repair site to the bladder which was confirmed electrophysiologically (Ruggieri et al., 2006). The current study determines whether the pattern of axonal regrowth from the repaired nerves or roots to the bladder is different between the surgical reanastomosis methods.Methods-The canine bladder was denervated by transection of all nerve roots from the sacral spinal cord mediating bladder contraction. Reinnervation surgeries included end-on-end repair of transected sacral ventral roots, transfer of coccygeal to sacral ventral roots (CG NT), or transfer of genitofemoral to pelvic nerves (GF NT).Results-Postmortem dialkylcarbocyanine dye tracing with Neurotrace DiI from the distal pelvic nerve to the bladder wall, combined with PGP9.5 neuronal immunohistochemistry, demonstrated innervation by DiI-labeled axons of only parasympathetic postganglionic intramural ganglia in normal controls and sham operated controls, but reinnervation of both intramural ganglia and detrusor muscle directly after repair of sacral ventral roots. GF NT and CG NT also resulted in reinnervation of both intramural ganglia and detrusor muscle, although to a lesser extent than repaired roots.Conclusions-Bladder reinnervation with either the same nerve (orthotopic reinnervation) or with either a primarily somatic nerve (coccygeal) or a primarily sensory nerve (genitofemoral) results in reinnervation of both intramural ganglia as well as direct innervation of detrusor muscle.

Anatomical feasibility of performing a nerve transfer from the femoral branch to bilateral pelvic nerves in a cadaver: a potential method to restore bladder function following proximal spinal cord injury

“…6,7,20,27,30 There are several recent reports of successful somatic nerve transfers in animal models and in patients for restoration of bladder function. 3,4,9,10,14,19-22,26,31 We found, using a canine model, that bladder reinnervation after sacral ventral root transection can be achieved by nerve transfer and surgical coaptation of coccygeal roots to the severed sacral roots, or transfer of genitofemoral nerves to the pelvic nerve as evidenced by increased bladder pressure upon functional electrical stimulation of these nerves after time had elapsed for reinnervation. In the majority of animals in each group, effective detrusor contractions were elicited with stimulation of the reinnervated pelvic nerve.…”

“…4,21,22 Anterograde axonal tracing also confirmed regrowth of axons from the genitofemoral nerve into the bladder detrusor muscle after these heterotopic somatic nerve transfers. 3 …”

Neuromuscular Nicotinic Receptors Mediate Bladder Contractions Following Bladder Reinnervation with Somatic to Autonomic Nerve Transfer after Decentralization by Spinal Root Transection

“…In the normal bladder, all axons in the pelvic nerve innervate intramural postganglionic (parasympathetic) ganglia cells; 24 this pathway is not blocked by SCh. However, the new neuronal pathway, achieved by either GFNT or FNT, is blocked by SCh.…”

Neural reconstruction methods of restoring bladder function

“…19, 34, 35 In an initial study using intercostal nerves as donor nerves in one dog, 35 the immediate postoperative recovery was poor. We next examined the feasibility of transferring the ilioinguinal or iliohypogastric nerves, but each was too short to reach the bladder base.…”

“…We have previously found that transfer of the genitofemoral nerve (a mixed somatic sensory and motor nerve) to the pelvic nerve leads to innervation of neurons of intramural ganglia, as well as direct innervation of smooth muscle fibres. 19 However, the end organ targets after transfer of other nerve types have yet to be examined. Lastly, the types of receptors activated by the transferred nerves for storage and voiding reflexes need to be determined in physiological studies.…”