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A decellularized nerve matrix scaffold inhibits neuroma formation in the stumps of transected peripheral nerve after peripheral nerve injury.

ABSTRACT: Traumatic painful neuroma is an intractable clinical disease characterized by improper extracellular matrix (ECM) deposition around the injury site. Studies have shown that the microstructure of natural nerves provides a suitable microenvironment for the nerve end to avoid abnormal hyperplasia and neuroma formation. In this study, we used a decellularized nerve matrix scaffold (DNM-S) to prevent against the formation of painful neuroma after sciatic nerve transection in rats. Our results showed that the DNM-S effectively reduced abnormal deposition of ECM, guided the regeneration and orderly arrangement of axon, and decreased the density of regenerated axons. The epineurium-perilemma barrier prevented the invasion of vascular muscular scar tissue, greatly reduced the invasion of α-smooth muscle actin-positive myofibroblasts into nerve stumps, effectively inhibited scar formation, which guided nerve stumps to gradually transform into a benign tissue and reduced pain and autotomy behaviors in animals. These findings suggest that DNM-S-optimized neuroma microenvironment by ECM remodeling may be a promising strategy to prevent painful traumatic neuromas.

SUBMITTER: Qiu S

PROVIDER: S-EPMC9727462 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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A decellularized nerve matrix scaffold inhibits neuroma formation in the stumps of transected peripheral nerve after peripheral nerve injury.

Qiu Shuai S Deng Pei-Jun PJ He Fu-Lin FL Yan Li-Wei LW Tu Zhe-Hui ZH Liu Xiao-Lin XL Quan Da-Ping DP Bai Ying Y Zheng Can-Bin CB Zhu Qing-Tang QT

Neural regeneration research 20230301 3

Traumatic painful neuroma is an intractable clinical disease characterized by improper extracellular matrix (ECM) deposition around the injury site. Studies have shown that the microstructure of natural nerves provides a suitable microenvironment for the nerve end to avoid abnormal hyperplasia and neuroma formation. In this study, we used a decellularized nerve matrix scaffold (DNM-S) to prevent against the formation of painful neuroma after sciatic nerve transection in rats. Our results showed ...[more]

PMID: 36018192

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Project description:OBJECTIVE: Neuroma is a psychologically and physically disabling problematic condition without any current standard therapy. For that reason, we investigated whether end-to-side anastomosis of the proximal end of the transected nerve into the adjacent nerve will prevent the development of neuroma in different types of nerve injuries. STUDY DESIGN: In this study, hind legs of 18 Sprague-Dawley female rats were used. Six groups were formed. In group I, peroneal nerves were transected and its proximal end was attached end-to-side through the epineural window to the adjacent tibial nerve. In group II, contrary to group I, an epineural window was created in the tibial nerve and the same number of sutures were employed. In group III, tibial nerve was transected proximal to the end-to-side repair site, whereas in group IV, distal segment of the nerve was cut, and an end-to-end repair procedure was repeated. In group V, unlike group I, an approximately 1-cm segment was resected and removed distal (from tibial nerve) to the end-to-side repair site. In group VI, an epineural window was created in the tibial nerve and the same number of sutures were used, and also a 1-cm distal nerve segment was resected. The rats were followed for 2 months, and then all of the groups were evaluated histopathologically, and weights of the posterior muscle groups of hind legs were evaluated. FINDINGS AND CONCLUSIONS: No neuroma formation was observed in the proximal stumps of peroneal nerve segments in end-to-side repair sites in groups I, III, IV, and V, and proximal stumps of the tibial nerve in group V. In group VI, neuroma formation was observed in the proximal end of the tibial nerve. When weights of the posterior muscle groups of hind legs in groups I and II were comparatively assessed, statistically significant difference was not detected. In conclusion, based on histological data obtained for proximal nerve ends and segments distal to the end-to-side repair sites, we think that end to side neurorrhaphy of the proximal end of the damaged nerve to adjacent nerve will prevent the development of neuroma without injuring the intact nerve segment.

Project description:Rationale: Peripheral nerve injury (PNI) is a great challenge for regenerative medicine. Nerve autograft is the gold standard for clinical PNI repair. Due to its significant drawbacks, artificial nerve guidance conduits (NGCs) have drawn much attention as replacement therapies. We developed a combinatorial NGC consisting of longitudinally aligned electrospun nanofibers and porcine decellularized nerve matrix hydrogel (pDNM gel). The in vivo capacity for facilitating nerve tissue regeneration and functional recovery was evaluated in a rat sciatic nerve defect model. Methods: Poly (L-lactic acid) (PLLA) was electrospun into randomly oriented (PLLA-random) and longitudinally aligned (PLLA-aligned) nanofibers. PLLA-aligned were further coated with pDNM gel at concentrations of 0.25% (PLLA-aligned/0.25% pDNM gel) and 1% (PLLA-aligned/1% pDNM gel). Axonal extension and Schwann cells migration were evaluated by immunofluorescence staining of dorsal root ganglia cultured on the scaffolds. To fabricate implantable NGCs, the nanofibrous scaffolds were rolled and covered with an electrospun protection tube. The fabricated NGCs were then implanted into a 5 mm sciatic nerve defect model in adult male Sprague-Dawley rats. Nerves treated with NGCs were compared to contralateral uninjured nerves (control group), injured but untreated nerves (unstitched group), and autografted nerves. Nerve regeneration was monitored by an established set of assays, including T2 values and diffusion tensor imaging (DTI) derived from multiparametric magnetic resonance imaging (MRI), histological assessments, and immunostaining. Nerve functional recovery was evaluated by walking track analysis. Results: PLLA-aligned/0.25% pDNM gel scaffold exhibited the best performance in facilitating directed axonal extension and Schwann cells migration in vitro due to the combined effects of the topological cues provided by the aligned nanofibers and the biochemical cues retained in the pDNM gel. Consistent results were obtained in animal experiments with the fabricated NGCs. Both the T2 and fractional anisotropy values of the PLLA-aligned/0.25% pDNM gel group were the closest to those of the autografted group, and returned to normal much faster than those of the other NGCs groups. Histological assessment indicated that the implanted PLLA-aligned/0.25% pDNM gel NGC resulted in the largest number of axons and the most extensive myelination among all fabricated NGCs. Further, the PLLA-aligned/0.25% pDNM gel group exhibited the highest sciatic nerve function index, which was comparable to that of the autografted group, at 8 weeks post-surgery. Conclusions: NGCs composed of aligned PLLA nanofibers decorated with 0.25% pDNM gel provided both topological and biochemical guidance for directing and promoting axonal extension, nerve fiber myelination, and functional recovery. Moreover, T2-mapping and DTI metrics were found to be useful non-invasive monitoring techniques for PNI treatment.

Dataset Information

A decellularized nerve matrix scaffold inhibits neuroma formation in the stumps of transected peripheral nerve after peripheral nerve injury.

Publications

A decellularized nerve matrix scaffold inhibits neuroma formation in the stumps of transected peripheral nerve after peripheral nerve injury.

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