Obturator to pelvic nerve transfer one year after bladder decentralization restores bladder sensation and emptying function in canines.

Tiwari E1, Braverman A S2, Hobson L2, Salvadeo D M2, Pontari M2, Barbe M F2, Ruggieri M R2

Research Type

Pure and Applied Science / Translational

Abstract Category

Neurourology

Abstract 506
Open Discussion ePosters
Scientific Open Discussion Session 28
Friday 31st August 2018
13:25 - 13:30 (ePoster Station 1)
Exhibition Hall
Animal Study Anatomy Pathophysiology
1. Electrical and Computer Engineering, Temple University, 2. Lewis Katz School of Medicine at Temple University
Presenter
A

Alan S Braverman

Links

Poster

Abstract

Hypothesis / aims of study
We previously demonstrated motor reinnervation of the decentralized canine urinary bladder by increased detrusor pressure induced by electrical stimulation of the transferred genitofemoral or femoral nerves in 21 of 28 animals {1}.  Evidence of bladder and bowel fullness sensation in these new neuronal pathways was based on observation of micturition postures in the reinnervated animals {2}. This interpretation would be less certain if decentralized only animals also display these urination postures after decentralization. Our focus here was to determine whether these postures are eliminated in decentralized animals up to one year after nerve transection and then to determine whether these same animals are capable of sensing bladder fullness after reinnervation. This was addressed by observation of their urination postures at regular intervals and to observe their ability to empty a full bladder.
Study design, materials and methods
Decentralization was performed by bilateral transection of the hypogastric nerves, all spinal roots caudal to L7 (dorsal and ventral), and the dorsal roots of L7 bilaterally in a group of 7 female canines.  In 3 of these 7 animals, 12 months after decentralization fascicles of the obturator nerve were transferred bilaterally to the anterior vesical branch of the pelvic nerve for bladder reinnervation. Another group of 6 animals was decentralized without transection of the L7 dorsal roots. The frequency of urination postures were recorded over 24 hour periods at monthly intervals for 12 months after the decentralization surgery as well as after reinnervation surgery using video surveillance in their housing cages. Conscious filling urodynamics studies were and ability to empty a filled bladder were assessed during these monthly post-operative intervals. Animals were anesthetized with propofol for insertion of bladder, urethra, rectal and anal sphincter catheterization and after recovery from the propofol the detrusor, urethral and anal sphincter pressures were monitored in the non-anesthetized state.  The bladder was filled to cystometric capacity, and the animal was returned to its transport cage, the catheter was removed with the bladder full and the animal was monitored for voluntarily bladder emptying for 10 minutes. Any bladder contents expelled during this period was collected, measured and compared to the cystometric capacity volume that was previously infused into the bladder. At the end bladder was expressed using the Credé maneuver and residual volume was measured.
Results
Urination postures were consistently observed after decentralization in all 6 animals decentralized without transection of the L7 dorsal roots.  During 12 months following decentralization, 2 of the 7 with the additional L7 dorsal root transections showed no micturition postures, one showed only one urination posture at 5 and 10 months and one showed an increased frequency (<10/day) at 2 and 4 months. In 2 of these 4 animals, intermediate postures between urination and defecation were observed coincident with culture confirmed bacteriuria and these disappeared with antimicrobial treatment.  One of these 4 animals was euthanized at 9 months due to kidney stone problem. Three of the 7 that did show consistent micturition postures at monthly observation periods were euthanized at 8-9 months.  Obturator to pelvic nerve transfer was done in the 2 animals that showed no urination postures and in the one that showed intermediate postures only during culture confirmed bacteriuria.  These urination postures were observed in all 3 of these reinnervated animals 4-6 months after the reinnervation surgery.  When returned to the transport after bladder filling, one of these 3 animals assumed the urination posture and partially emptied the bladder voluntarily on 2 occasions.
Interpretation of results
With either genitofemoral or femoral nerve transfer to the anterior vesical branch of the pelvic nerve, we previously found that neuronal cell bodies became retrogradely labelled with fluorogold from the bladder appear in ventral horn regions of lumbar spinal cord segments, as opposed to sacral spinal cord segments seen in sham/un-operated controls suggesting functional reinnervation through new neuronal pathways {1}. For these previous studies, the decentralization did not include elimination of the hypogastric nerve sympathetic innervation or the sensory contribution from the L7 dorsal roots.  In the current studies, with the additional hypogastric nerve and L7 dorsal root transections, we found these postures to be eliminated completely in some animals during 12 month decentralization period and reappear 3-6 months after nerve transfer induced reinnervation. Also one animal clearly showed evidence of voluntarily urination.  Because urination postures were consistently observed in all 6 animals with intact L7 dorsal roots but hypogastric nerve transections, the sensory innervation from the L7 spinal segment and not the sympathetic innervation from the hypogastric nerve  appears to be sufficient to mediated urination behavior.
Concluding message
In the L7 dorsal root intact decentralized group, all were able to sense bladder fullness suggesting residual sensory bladder innervation likely from the remaining lower lumbar dorsal root fibers. Fewer dogs with the additional L7 dorsal root transection were able to detect bladder fullness. The ability some of the animals in the L7 dorsal root transected decentralized group to sense bladder fullness may be from sensory nerve sprouting or variations in the bladder sensory innervation, as described previously {3}.  In at least one animal that showed no urination postures for 12 months after decentralization, nerve transfer induced both the ability to sense bladder fullness and bladder emptying behavior confirming both motor and sensory bladder reinnervation.
References
  1. Gomez-Amaya, Sandra M., Mary F. Barbe, Justin M. Brown, Neil S. Lamarre, Alan S. Braverman, Vicky S. Massicotte, and Michael R. Ruggieri Sr. 2015. 'Bladder Reinnervation Using a Primarily Motor Donor Nerve (Femoral Nerve Branches) is Functionally Superior to Using a Primarily Sensory Donor Nerve (Genitofemoral Nerve)', The Journal of Urology, 193: 1042-51.
  2. Ruggieri, Michael, Sandra Gomez-Amaya, Alan Braverman, Neil Lamarre, and Mary Barbe. 2016. 'MP28-07 SENSATION OF BLADDER FULLNESS BY A NEW NEURONAL PATHWAY ESTABLISHED BY GENITOFEMORAL OR FEMORAL NERVE TRANSFER TO AN ANTERIOR VESICAL PELVIC NERVE BRANCH IN A CANINE DECENTRALIZED BLADDER MODEL', The Journal of Urology, 195: e373.
  3. Gomez-Amaya, S. M., M. R. Ruggieri, S. A. Arias Serrato, V. S. Massicotte, and M. F. Barbe. 2015. 'Gross Anatomical Study of the Nerve Supply of Genitourinary Structures in Female Mongrel Hound Dogs', Anatomia, histologia, embryologia, 44: 118-27
Disclosures
Funding NIH-NINDS NS070267 to MRR and MFB Clinical Trial No Subjects Animal Species Canine Ethics Committee Temple University Institutional Animal Care & Use Committee (IACUC)
27/03/2024 23:36:24