Bladder reinnervation using a primarily motor donor nerve (femoral nerve branches) is functionally superior to using a primarily sensory donor nerve (genitofemoral nerve)

Abstract

Purpose: We determined whether transfer of a primarily motor nerve (femoral) to the anterior vesicle branch of the pelvic nerve would allow for more effective bladder reinnervation than transfer of a primarily sensory nerve (genitofemoral).

Materials and methods: A total of 41 female mongrel dogs underwent bladder decentralization and then bilateral nerve transfer, or served as sham operated or unoperated controls. Decentralization was achieved by bilateral transection of all sacral roots that induced bladder contraction upon electrical stimulation. Retrograde neuronal labeling dye was injected in the bladder 3 weeks before sacrifice.

Results: Increased detrusor pressure after direct stimulation of the transferred nerve, lumbar spinal cord or spinal root was observed in 12 of 17 dogs with genitofemoral nerve transfer and in 9 of 10 with femoral nerve transfer (mean ± SEM 7.6 ± 1.4 and 11.7 ± 3.1 cm H2O, respectively). Mean detrusor pressure after direct electrical stimulation of transferred femoral nerves was statistically significantly greater than after stimulation of transferred genitofemoral nerves. Retrograde labeled neurons from the bladder observed in upper lumbar cord segments after genitofemoral and femoral nerve transfer confirmed bladder reinnervation, as did labeled axons at the nerve transfer site.

Conclusions: While transfer of a mixed sensory and motor nerve (genitofemoral) or a primarily motor nerve (femoral) can reinnervate the bladder, using the primarily motor nerve provided greater return of nerve evoked detrusor contraction. This surgical approach may be useful to achieve bladder emptying in patients with lower motor spinal cord injury.

Keywords: autografts; femoral nerve; innervation; spinal cord injuries; urinary bladder.

Figure 1

Diagrams representing surgical methods used. A) Bilateral bladder decentralization. B) Genitofemoral nerve transfer (GFNT). C) Femoral nerve transfer (FNT). DRG= dorsal root ganglion; CMG= caudal mesenteric ganglia; HGN= hypogastric nerve; PP= pelvic plexus; PdN= pudendal nerve; L= lumbar.

Figure 2

Representative in vivo bladder and detrusor pressure recordings during electrical stimulation. A) GFNT Dog 12 during direct electrical stimulation of L2-3 cord segments, prior to euthanasia at 293 days post-surgery. B) FNT Dog 18 during direct electrical stimulation of L2 cord segment, prior to euthanasia at 224 days. C) Decentralized Dog 30 during direct electrical stimulation of PN, prior to euthanasia at 95 days. D) Sham/control Dog 34 during direct electrical stimulation of PN with implanted nerve cuff electrode interfaced with RF micro-stimulator prior to euthanasia at 251 days.

Figure 3

Dissection and microscope images of transferred GFNs and FNs, after coaptation to PN. A) GFNT at euthanasia. B) FNT at euthanasia. C) Normal bladder innervation. D) Serosa-nerve preparation from a GFNT dog, in a petri dish. E) Fluorogold labeled axons in GFNT, proximal to coaptation site (spinal cord side). Combined bright field and fluorescence on an inverted scope. F) Inverted scope view of FNT specimen, and G) fluorogold labeled axons of same specimen, distal to suture site. White arrow indicates same axonal process. H) Fluorogold labeled axons in same FNT sample, proximal to suture site. I) Fluorogold labeled axons in another FNT, 2 cm proximal to coaptation. Scale bars in G–H = 10 micrometers.

Figure 4

Maximum detrusor pressure (MDP) after FES. A) MDP after spinal cord FES. *p<0.05, compared to sham/unoperated dogs. B) MDP after FES of pelvic nerve (PN) or pelvic plexus (PP) in the sham/unoperated and decentralized groups and FES of the transferred GFN or FN in the GFNT and FNT groups. ##: p<0.01, compared to FNT group; *&:p<0.05 compared to Sham/unoperated or decentralized groups.

Figure 5

Location of fluorogold (FG) labeled neurons in lamina VII–IX of lumbar (L) and sacral (S) ventral horns (VH) after dye injection into bladder. A,E) Sham control dog. B,F) Decentralized control dog. C,G) GFNT dog. D,H) FNT dog. I) Location of motor neurons innervating bladder in lumbar cord of GFN and FN dogs. J) Location of motor neurons innervating bladder of sham/unoperated control dogs.

Figure 6

Mean number of retrogradely labeled cells (fluorogold) per mm² in ventral horn spinal cord segments. A) Sham/unoperated controls. B) Decentralized controls. C) GFNT. D) FNT. CG = coccygeal, L= lumbar, S = sacral. * and **:p<0.05 and p<0.01, compared to decentralized dogs; # and ##:p<0.05 and p<0.01, compared to sham/unoperated dogs; &&: p<0.01, compared to FNT dogs.