Nerve transfer for restoration of lower motor neuron-lesioned bladder function. Part 2: correlation between histological changes and nerve evoked contractions

Author:

Barbe Mary F.1ORCID,Testa Courtney L.1,Cruz Geneva E.1,Frara Nagat A.1,Tiwari Ekta2,Hobson Lucas J.1,McIntyre Brian S.3,Porreca Danielle S.2,Giaddui Dania2,Braverman Alan S.2,Day Emily P.1,Amin Mamta2,Brown Justin M.4,Mazzei Michael5,Pontari Michel A.6,Wagner Ida J.5,Ruggieri Michael R.12ORCID

Affiliation:

1. Department of Anatomy and Cell Biology, Lewis Katz School of Medicine, Temple University, Philadelphia, Pennsylvania

2. Department of Electrical and Computer Engineering, College of Engineering, Temple University, Philadelphia, Pennsylvania

3. Drexel University College of Medicine, Philadelphia, Pennsylvania

4. Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts

5. Department of Surgery, Lewis Katz School of Medicine, Philadelphia, Pennsylvania

6. Department of Urology, Lewis Katz School of Medicine, Temple University Health System, Philadelphia, Pennsylvania

Abstract

We determined the effect of pelvic organ decentralization and reinnervation 1 yr later on urinary bladder histology and function. Nineteen canines underwent decentralization by bilateral transection of all coccygeal and sacral (S) spinal roots, dorsal roots of lumbar (L)7, and hypogastric nerves. After exclusions, eight were reinnervated 12 mo postdecentralization with obturator-to-pelvic and sciatic-to-pudendal nerve transfers, then euthanized 8-12 mo later. Four served as long-term decentralized only animals. Before euthanasia, pelvic or transferred nerves and L1–S3 spinal roots were stimulated and maximum detrusor pressure (MDP) recorded. Bladder specimens were collected for histological and ex vivo smooth muscle contractility studies. Both reinnervated and decentralized animals showed less or denuded urothelium, fewer intramural ganglia, and more inflammation and collagen, than controls, although percent muscle was maintained. In reinnervated animals, pgp9.5+ axon density was higher compared with decentralized animals. Ex vivo smooth muscle contractions in response to KCl correlated positively with submucosal inflammation, detrusor muscle thickness, and pgp9.5+ axon density. In vivo, reinnervated animals showed higher MDP after stimulation of L1–L6 roots compared with their transected L7–S3 roots, and reinnervated and decentralized animals showed lower MDP than controls after stimulation of nerves (due likely to fibrotic nerve encapsulation). MDP correlated negatively with detrusor collagen and inflammation, and positively with pgp9.5+ axon density and intramural ganglia numbers. These results demonstrate that bladder function can be improved by transfer of obturator nerves to pelvic nerves at 1 yr after decentralization, although the fibrosis and inflammation that developed were associated with decreased contractile function.

Funder

HHS | NIH | National Institute of Neurological Disorders and Stroke

Publisher

American Physiological Society

Subject

Physiology (medical),Physiology

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