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Innervation Patterns of Thumb Trapeziometacarpal Joint Ligaments

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Innervation Patterns of Thumb Trapeziometacarpal Joint Ligaments SCIENTIFIC ARTICLE Innervation Patterns of Thumb Trapeziometacarpal Joint Ligaments Elisabet Hagert, MD, PhD, Julia Lee, MD, Amy L. Ladd, MD Purpose The human thumb trapeziometacarpal (TM) joint is a unique articulation that allows stability during pinch and grip and great degrees of mobility. Because the saddle-shaped articulating surfaces of the TM joint are inherently unstable, joint congruity depends on the action of restraining ligaments and periarticular muscles. From other joints, it is known that proprioceptive and neuromuscular joint stability depend on afferent information from nerve endings within ligaments. We hypothesize that the TM joint ligaments may similarly be innervated, indicating a possible proprioceptive function of the joint. Methods We harvested 5 TM joint ligaments in entirety from 10 fresh-frozen cadaver hands with no or only minor signs of osteoarthritis and suture-marked them for proximal-distal orientation. The ligaments harvested were the dorsal radial, dorsal central, posterior oblique, ulnar collateral, and anterior oblique ligaments. After paraffin-sectioning, we stained the ligaments using a triple-antibody immunofluorescent technique and analyzed them using immunofluorescence microscopy. Results Using the triple-stain technique, mechanoreceptors could be classified as Pacinian corpuscles, Ruffini endings, or Golgi-like endings. The 3 dorsal ligaments had significantly more nerve endings than the 2 volar ligaments. Most of the nerve endings were close to the bony attachments and significantly closer (P ϭ .010) to the metacarpal insertion of each ligament. The anterior oblique ligament had little to no innervation in any of the specimens analyzed. Discussion The TM joint ligaments had an abundance of nerve endings in the dorsal ligaments but little to no innervation in the anterior oblique ligament. The Ruffini ending was the predominant mechanoreceptor type, with a greater density in the mobile metacarpal portion of each ligament. Clinical relevance Presence of mechanoreceptors in the dorsal TM joint ligaments infers a proprioceptive function of these ligaments in addition to their biomechanical importance in TM joint stability. (J Hand Surg 2012;37A:706–714. Copyright © 2012 by the American Society for Surgery of the Hand. All rights reserved.) Key words Innervation, ligaments, mechanoreceptors, proprioception, thumb. From the Department of Clinical Science and Education, Karolinska Institutet, Stockholm, Sweden; and Foundation for purchase of equipment and support of E.H. and J.L., the OREF/RJOS/DePuy Career the Department of Orthopaedic Surgery, Robert A. Chase Hand and Upper Extremity Center, Stanford DevelopmentAwardforpurchaseofequipment,andtheHirschFoundation(KarolinskaInstitutet)for University,PaloAlto,CA. support of E.H. Received for publication October 12, 2011; accepted in revised form December 21, 2011. Corresponding author: Elisabet Hagert, MD, PhD, Department of Clinical Science and Education, No benefits in any form have been received or will be received related directly or indirectly to the Hand and Foot Surgery Center, Karolinska Institutet, Storängsv.10, 11542 Stockholm, Swe- subject of this article. den; e-mail: [email protected]. TheauthorsthankAlexSox-Harris,PhD,forinvaluablehelpinthestatisticalanalysisofthemanuscript. 0363-5023/12/37A04-0012$36.00/0 doi:10.1016/j.jhsa.2011.12.038 This study was supported by a National Institute of Health (NIH) grant NIH/SBIR grant# 2 R44 EB003067-02A1 for the purchase of cadaver specimens, the Ronald and Ann Williams Charitable 706 ᭜ © ASSH ᭜ Published by Elsevier, Inc. All rights reserved. INNERVATION PATTERNS OF THUMB TMJ LIGAMENTS 707 HE ORIGIN OF THE HUMAN thumb trapeziometa- MATERIALS AND METHODS carpal (TM) joint with its complex saddle shape Specimens has been traced to the advent of terrestrial bi- T We dissected 10 fresh-frozen human cadaver hands for pedalism, when primates evolved from an arboreal an- this study: 3 female and 5 male (mean age, 65 y; range, imal with long fingers and redundant thumbs to a ter- 53–74 y; age unknown in 2 specimens). Using loupe restrial primate with more equal digital lengths and the 1,2 magnification, standard hand surgical instruments, and ability to perform thumb opposition and handle tools. meticulous dissection, we identified the nerve branches The human TM joint appears to be a morphological to the dorsal and volar TM joint capsule, as we did the compromise from that of our primate ancestors and is ligaments stabilizing the joint, which we then prepared. flat enough to allow for a high grade of mobility while Of the 10 specimens, 9 had macroscopic signs of mild being curved enough to support precise and powerful osteoarthritic (OA) changes involving 25% or less of 3 grips. The combination of mobility and strength places the proximal and distal carpometacarpal joint surfaces, unusually high demands on the stability of the TM joint. whereas 1 of the 10 samples showed no signs of OA This depends on a balance between compressive and according to the Outerbridge classification.17 The lig- tensile forces across the joint. Articular congruence aments harvested were the dorsal radial (DRL), permits stability in compression, whereas ligamentous dorsal central (DCL), posterior oblique (POL), an- restraint permits stability in tension.4 However, the terior oblique (AOL), and ulnar collateral (UCL) unique shape and looseness of the TM joint renders it (Fig. 1). We harvested each ligament at the insertion into inherently unstable in all positions, with the exception bone and suture-marked it for proximal-distal orientation. of the final screw-home torque seen in full opposition, In addition, we excised sections of the median nerve as Edmunds5 purported. As such, this joint is highly from 2 hands to use for control staining. dependent on the secondary and dynamic stability that The local institutional review board granted approval is created by periarticular muscles. for this project and the handling of human remains was Recent studies on the scapholunate ligament propose in strict accordance with ethical and practical protocols. that the dynamic neuromuscular stability of the scapholu- Slide preparation and immunohistochemistry nate joint depends on the innervation of mechanorecep- tors and nerve endings in the joint capsule and We immediately fixed all harvested specimens in 4% ligaments,6,7 which transmit afferent information formaldehyde, placed them in paraffin wax, and sec- ␮ through the nerves innervating the wrist joint,8 tioned them into 8- m-thick slices before mounting resulting in alterations of wrist muscle function.9,10 them on glass slides. We deparaffinized specimens us- ϫ This suggests the intact proprioceptive function is ing serial xylene washes (3 3 min) followed by gradual rehydration. We used a microwave antigen important in maintaining stability of the scapholunate retrieval method to expose antibody-binding sites. joint. Numerous studies on the knee, shoulder, and Specimens were then made permeable with 1% Triton- ankle joints support similar findings, where an intact X100 and blocked with Image-iT FX (Invitrogen, joint innervation and preserved proprioceptive func- Carlsbad, CA). Afterward, we stained the specimen tion is essential for a normal joint homeostasis.11–14 samples with primary antibodies for 1 hour at 37°C in There are 2 studies describing the precise macro- ϫ 15,16 a humid chamber, rinsed them for 3 5 minutes in 0.1 scopic innervation of the TM joint but no publica- mol/L phosphate-buffered solution (PBS), and stained tions on the microscopic innervation and possible pres- them with secondary antibodies under the same condi- ence of mechanoreceptors in TM joint ligaments. Both tions. We executed a final 3 ϫ 5-minute rinse in 0.1 macroscopic studies describe numerous branches from mol/L PBS before using ProLong Gold Anti-Fade Re- the palmar cutaneous and thenar branches of the median agent with 4=,6=-diamidino-2-phenylindole (DAPI) (In- nerve, lateral cutaneous nerve of the forearm, and su- vitrogen) to mount the slides. perficial branch of the radial nerve terminating at or around the joint. Given the extensive innervation to the Antibodies TM joint, we hypothesized that the ligaments stabiliz- We used 2 antibodies in conjunction with DAPI to yield ing the joint may be innervated with mechanoreceptors a dual-color stain: p75 and PGP9.5. Rabbit anti-nerve and sensory nerve endings and that the pattern of in- growth factor (NGF) receptor 75 (p75) is an antibody nervation may add knowledge to the role of various directed against the low-affinity NGF receptor p75, also ligaments in the neuromuscular stability of the TM known as p75NTR or CD271. This transmembrane joint. protein is expressed on the cell membrane of nerve cells JHS ᭜ Vol A, April 708 INNERVATION PATTERNS OF THUMB TMJ LIGAMENTS FIGURE 1: A The 5 ligaments harvested from the dorsal aspect of the TM joint were the DRL, the DCL, and the POL. B Those harvested from the volar TM joint were the UCL and the AOL. MC1, first metacarpal; MC2, second metacarpal; APL, abductor pollicis longus. Asterisk indicates the dorsal tubercle of the trapezium (Tz). and responsible for signaling related to neuronal goat anti-mouse Alexa Fluor 647 (Invitrogen) as the growth, migration, differentiation, and cell death. p75 is secondary antibody to emphasize PGP9.5. This anti- considered the primary antibody in marking and identify- body was optimally diluted to 1:200 with 0.1 mol/L ing the Pacinian corpuscle.18 We optimized rabbit anti- PBS
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