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Does Cryoneurolysis Result in Persistent Motor Deficits? A Reg Anesth Pain Med: first published as 10.1136/rapm-2019-101141 on 29 January 2020. Downloaded from Original research Does cryoneurolysis result in persistent motor deficits? A controlled study using a rat peroneal nerve injury model Sameer B Shah,1 Shannon Bremner,1 Mary Esparza,1 Shanelle Dorn,1 Elisabeth Orozco,1 Cameron Haghshenas,1 Brian M Ilfeld ,2 Rodney A Gabriel ,2 Samuel Ward1 1Orthopedic Surgery, University ABSTRact Cryoneurolysis is a non- opioid analgesic modality of California, San Diego, La Background Cryoneurolysis of peripheral nerves uses used to treat both acute and chronic pain involving Jolla, California, USA 2 the application of extremely low temperatures to Anesthesiology, University of localised intense cold to induce a prolonged block over California, San Diego, La Jolla, multiple weeks that has the promise of providing potent a peripheral nerve to induce Wallerian degenera- California, USA analgesia outlasting the duration of postoperative pain tion and consequent abrogation of nerve conduc- following surgery, as well as treat other acute and tion.2 Axons regenerate along the undisturbed Correspondence to chronic pain states. However, it remains unclear whether epineurium, perineurium, and endoneurium from Dr Brian M Ilfeld, persistent functional motor deficits remain following the site of ablation towards their distal targets at Anesthesiology, University of about 1–2 mm/day,3 resulting in a nerve block California, San Diego, La Jolla, cryoneurolysis of mixed sensorimotor peripheral nerves, CA 92093, USA; greatly limiting clinical application of this modality. To with a variable duration, but typically measured in bilfeld@ ucsd. edu help inform future research, we used a rat peroneal multiple weeks.4 While cryoanalgesia has been used nerve injury model to evaluate if cryoneurolysis results in for decades to treat primarily chronic pain,4–8 the Received 11 November 2019 persistent deficits in motor function. advent of percutaneous cannulas and ultrasound Revised 13 January 2020 Accepted 14 January 2020 Methods Male Lewis rats (n=30) had their common guidance dramatically increases the potential appli- 9–11 Published Online First peroneal nerves exposed bilaterally at the proximal cations for its use in treating acute pain as well. 29 January 2020 lateral margin of the knee and subsequently underwent To date, most published research involves the cryoneurolysis on one limb and sham treatment on the functional and histological recovery of sensory contralateral limb. Outcomes were evaluated on days 3, nerves12–16; however, mixed motor- sensory nerves 14, 30, 90 and 180. The primary end point was motor may also be targeted.4 10 17 18 Because cryoneurolysis function, based on ankle dorsiflexion torque. In addition, affects both sensory and motor neurons, concern sensory function was tested based on von Frey’s filament exists regarding residual and persistent motor sensitivity to the peroneal sensory distribution. A subset weakness due to either incomplete regeneration or of animals was sacrificed following functional testing motor unit clustering. Given that interest in cryo- at each time point, and general tissue morphology, neurolysis is increasing due to an increased aware- http://rapm.bmj.com/ connective tissue deposition, and axon counts were ness of the pervasiveness of inadequately-controlled evaluated. postoperative pain,19 current public health efforts Results Motor deficits in treated limbs were observed to decrease opioid use,20 and recognition that at 3 and 14 days but had resolved at time points chronic, persistent postoperative pain is associated beyond 1 month. Bilateral sensory deficits were also with inadequately- controlled perioperative pain,21 observed at 3 and 14 days, and also resolved within it is imperative that any long- term cryo- induced 1 month. Consistent with motor functional deficits, axon motor deficits be identified. on September 24, 2021 by guest. Protected copyright. counts trended lower in treated nerves compared with In this controlled study, we used a sensitive and contralateral controls at 3 days; however, axon counts validated rat common peroneal (fibular) nerve were not significantly different at later time points. injury model to evaluate if cryoneurolysis results Conclusions When applied to a mixed sensorimotor in persistent motor function deficits, based on nerve, cryoneurolysis did not result in persistent motor recovery of ankle dorsiflexion torque. deficits. METHODS Study intervention Thirty 300 g male Lewis rats underwent survival INTRODUCTION surgery under isoflurane anaesthesia with analgesia Pain following surgery is frequently treated with provided with preoperative subcutaneous injec- © American Society of Regional Anesthesia & Pain Medicine local anesthetic- based peripheral nerve blocks to tion of 0.3 mg sustained release buprenorphine 2020. Re-use permitted under improve analgesia, decrease/negate opioid reliance, (Buprenorphine SR- LAB, ZooPharm, Windsor, CC BY-NC . No commercial and decrease the incidence/severity of persistent Colorado, USA). Common peroneal (fibular) re-use . Published by BMJ. postsurgical pain. However, the duration of surgical nerves were exposed bilaterally at the proximal To cite: Shah SB, pain is often far longer than the duration of even lateral margin of the knee joint using a technique 22 23 Bremner S, Esparza M, the longest- acting single- injection peripheral previously described. The fascial sheath over- et al. Reg Anesth Pain Med nerve block; and, perineural local anesthetic infu- lying the nerve was left intact. On the left limb, 2020;45:287–292. sion is limited to less than 1 week in most cases.1 cryoneurolysis was performed with a console based Shah SB, et al. Reg Anesth Pain Med 2020;45:287–292. doi:10.1136/rapm-2019-101141 287 Reg Anesth Pain Med: first published as 10.1136/rapm-2019-101141 on 29 January 2020. Downloaded from Original research clinical cryoneurolysis machine (PainBlocker, Epimed Inter- peroneal nerve was harvested bilaterally, and snap frozen using national, Farmers Branch, Texas, USA). An 18 G trocar with a liquid nitrogen cooled isopentane.26 Transverse sections of the tapering tip was positioned immediately adjacent to the target nerve underlying the distal edge of the cryoablation site and nerve and three 2 min cryoneurolysis cycles separated by 1 min axial sections of tibialis anterior (TA) muscle ~5 mm distal to thaw periods were applied using nitrous oxide. This protocol its insertion at the knee were taken per previously published is a typical clinical protocol,3 and given the size and exposure methods, and slides were stored at −80°C until use.23 26 Sections of the rat peroneal nerve, may be viewed as aggressive. On the were stained with H&E, Masson’s trichrome (Polysciences, right limb, sham cryoneurolysis was performed, with exposure, Warrington, Pennsylvania, USA), Wheat Germ Agglutinin tip contact, and time of contact as above, but no freezing. (WGA) conjugated to AlexaFLuor 594, DAPI, and/or β3- tubu- Multiple criteria were considered to retain consistency within lin+laminin. The neuron- specific β3-tubulin was used as an our cryoneurolysis protocol. Frosting of the cannula tip as well as axonal marker for axon counting, laminin provided an outline formation of an ice ball encompassing the nerve was confirmed for delineating distinct nerve fibers, and WGA outlined muscle for each cycle. Repeatability in freezing technique was confirmed fibers. Sections were permeabilised with 0.2% Triton- X, blocked based on: (i) consistent exposure of the peroneal nerve; (ii) with blocking buffer (10% goat serum, 3% bovine serum albumin device indicator confirming sufficiently cooled cannula tip; (iii) (BSA) in phophate buffered saline (PBS)) then incubated with frosting of cannula; (iv) visual verification of contact of cannula primary antibodies mouse anti-β3- tubulin (Sigma- Aldrich; 1:500 tip directly on fascial sheath overlying peroneal nerve; (v) ice dilution) and rabbit anti-laminin (Sigma- Aldrich; 1:1000 dilu- ball formation on tissue surrounding nerve; (vi) fasciculations on tion) for 1 hour. Slides were then incubated with AlexaFluor 488 at least one of the freeze cycles. Increased local blood flow was goat-anti- mouse and AlexaFluor 594 goat-anti- rabbit secondary typical during a freeze cycle. Cannulas were thawed completely antibodies, then coverslipped with Vectashield Hardset with before detachment from tissue to avoid imposing mechanical 4',6- diamidino-2- phenylindole (DAPI ;Vector Labs, Burlingame, force on the nerve by cannula manipulation. California, USA). On the contralateral limb, the sham (control) treatment was Fluorescent images were acquired using a Leica DM6000 administered by positioning the cryoablation cannula immedi- microscope (Leica Microsystems, Buffalo Grove, Illinois, USA) ately adjacent to the target nerve for the same three 2 min on, equipped with a Leica DFC365 FX camera (Leica Microsys- 1 min off pattern as before, but without freezing (ie, no nitrous tems) using a 10X or a 63X oil immersion objective, and bright- oxide). Overlying muscles were repaired by closing the fascia field images were acquired at 20X using a Leica SCN400 slide with 4–0 polyglycolic acid (PGA) sutures, and wound clips were scanner (Leica Microsystems). Axon counts were estimated from used to close the skin incision. two sections, based on manual counting of β3- tubulin- positive puncta in selected 63X images covering at least 35% of the nerve cross-sectional area, and subsequent
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