J Wrist Surg 2015; 04(04): 284-291
DOI: 10.1055/s-0035-1564982
Scientific Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Altered Innervation Pattern in Ligaments of Patients with Basal Thumb Arthritis

Cassie A. Ludwig
1   Department of Orthopaedic Surgery, Robert A. Chase Hand and Upper Limb Center, Stanford University, Palo Alto, California
,
Nathalie Mobargha
2   Department of Hand and Plastic Surgery, Stavanger University Hospital, Stavanger, Norway
3   Department of Clinical Science and Education, Karolinska Institute, Stockholm, Sweden
,
Janet Okogbaa
1   Department of Orthopaedic Surgery, Robert A. Chase Hand and Upper Limb Center, Stanford University, Palo Alto, California
,
Elisabet Hagert
3   Department of Clinical Science and Education, Karolinska Institute, Stockholm, Sweden
4   Hand and Foot Surgery Center, Stockholm, Sweden
,
Amy L. Ladd
1   Department of Orthopaedic Surgery, Robert A. Chase Hand and Upper Limb Center, Stanford University, Palo Alto, California
› Institutsangaben
Weitere Informationen

Publikationsverlauf

Publikationsdatum:
29. Oktober 2015 (online)

Abstract

Purpose The population of mechanoreceptors in patients with osteoarthritis (OA) lacks detailed characterization. In this study, we examined the distribution and type of mechanoreceptors of two principal ligaments in surgical subjects with OA of the first carpometacarpal joint (CMC1).

Methods We harvested two ligaments from the CMC1 of eleven subjects undergoing complete trapeziectomy and suspension arthroplasty: the anterior oblique (AOL) and dorsal radial ligament (DRL). Ligaments were divided into proximal and distal portions, paraffin-sectioned, and analyzed using immunoflourescent triple staining microscopy. We performed statistical analyses using the Wilcoxon Rank Sum test and ANOVA with post-hoc Bonferroni and Tamhane adjustments.

Results The most prevalent nerve endings in the AOL and DRL of subjects with OA were unclassifiable mechanoreceptors, which do not currently fit into a defined morphological scheme. These were found in 11/11 (100%) DRLs and 7/11 (63.6%) AOLs. No significant difference existed with respect to location within the ligament (proximal versus distal) of mechanoreceptors in OA subjects.

Conclusion The distribution and type of mechanoreceptors in cadavers with no to mild OA differ from those in surgical patients with OA. Where Ruffini endings predominate in cadavers with no to mild OA, unclassifiable corpuscles predominate in surgical patients with OA. These findings suggest an alteration of the mechanoreceptor population and distribution that accompanies the development of OA.

Clinical Relevance Identification of a unique type and distribution of mechanoreceptors in the CMC1 of symptomatic subjects provides preliminary evidence of altered proprioception in OA.

 
  • References

  • 1 Van Heest AE, Kallemeier P. Thumb carpal metacarpal arthritis. J Am Acad Orthop Surg 2008; 16 (3) 140-151
  • 2 Linscheid RL, Dobyns JH. Dynamic carpal stability. Keio J Med 2002; 51 (3) 140-147
  • 3 Johansson H, Sjölander P, Sojka P. A sensory role for the cruciate ligaments. Clin Orthop Relat Res 1991; (268) 161-178
  • 4 Michelson JD, Hutchins C. Mechanoreceptors in human ankle ligaments. J Bone Joint Surg Br 1995; 77 (2) 219-224
  • 5 Diederichsen LP, Nørregaard J, Krogsgaard M, Fischer-Rasmussen T, Dyhre-Poulsen P. Reflexes in the shoulder muscles elicited from the human coracoacromial ligament. J Orthop Res 2004; 22 (5) 976-983
  • 6 Moraes MR, Cavalcante ML, Leite JA, Ferreira FV, Castro AJ, Santana MG. Histomorphometric evaluation of mechanoreceptors and free nerve endings in human lateral ankle ligaments. Foot Ankle Int 2008; 29 (1) 87-90
  • 7 Bressel E, Larsen BT, McNair PJ, Cronin J. Ankle joint proprioception and passive mechanical properties of the calf muscles after an Achilles tendon rupture: a comparison with matched controls. Clin Biomech (Bristol, Avon) 2004; 19 (3) 284-291
  • 8 Pötzl W, Thorwesten L, Götze C, Garmann S, Steinbeck J. Proprioception of the shoulder joint after surgical repair for Instability: a long-term follow-up study. Am J Sports Med 2004; 32 (2) 425-430
  • 9 Sharma L. Proprioceptive impairment in knee osteoarthritis. Rheum Dis Clin North Am 1999; 25 (2) 299-314, vi vi.
  • 10 Lund H, Juul-Kristensen B, Hansen K , et al. Movement detection impaired in patients with knee osteoarthritis compared to healthy controls: a cross-sectional case-control study. J Musculoskelet Neuronal Interact 2008; 8 (4) 391-400
  • 11 Hurley MV, Scott DL, Rees J, Newham DJ. Sensorimotor changes and functional performance in patients with knee osteoarthritis. Ann Rheum Dis 1997; 56 (11) 641-648
  • 12 Hurley MV. The role of muscle weakness in the pathogenesis of osteoarthritis. Rheum Dis Clin North Am 1999; 25 (2) 283-298, vi vi.
  • 13 Roos EM, Herzog W, Block JA, Bennell KL. Muscle weakness, afferent sensory dysfunction and exercise in knee osteoarthritis. Nat Rev Rheumatol 2011; 7 (1) 57-63
  • 14 Abraira VE, Ginty DD. The sensory neurons of touch. Neuron 2013; 79 (4) 618-639
  • 15 Berenbaum F. Osteoarthritis as an inflammatory disease (osteoarthritis is not osteoarthrosis!). Osteoarthritis Cartilage 2013; 21 (1) 16-21
  • 16 Hagert E, Forsgren S, Ljung BO. Differences in the presence of mechanoreceptors and nerve structures between wrist ligaments may imply differential roles in wrist stabilization. J Orthop Res 2005; 23 (4) 757-763
  • 17 Bisceglia M, Bisceglia S, Bisceglia ML. Muscle spindle and Pacinian corpuscle: conceptions, misconceptions, and the far-fetched hypothesis of an experienced surgical pathologist. Pathologica 2011; 103 (1) 4-7
  • 18 Morisawa Y. Morphological study of mechanoreceptors on the coracoacromial ligament. J Orthop Sci 1998; 3 (2) 102-110
  • 19 Rein S, Hanisch U, Zwipp H, Fieguth A, Lwowski S, Hagert E. Comparative analysis of inter- and intraligamentous distribution of sensory nerve endings in ankle ligaments: a cadaver study. Foot Ankle Int 2013; 34 (7) 1017-1024
  • 20 Petrie S, Collins J, Solomonow M, Wink C, Chuinard R. Mechanoreceptors in the palmar wrist ligaments. J Bone Joint Surg Br 1997; 79 (3) 494-496
  • 21 Hagert E, Persson JK, Werner M, Ljung BO. Evidence of wrist proprioceptive reflexes elicited after stimulation of the scapholunate interosseous ligament. J Hand Surg Am 2009; 34 (4) 642-651
  • 22 Arcand MA, Rhalmi S, Rivard CH. Quantification of mechanoreceptors in the canine anterior cruciate ligament. Int Orthop 2000; 24 (5) 272-275
  • 23 Ladd AL, Lee J, Hagert E. Macroscopic and microscopic analysis of the thumb carpometacarpal ligaments: a cadaveric study of ligament anatomy and histology. J Bone Joint Surg Am 2012; 94 (16) 1468-1477
  • 24 Lee J, Ladd A, Hagert E. Immunofluorescent triple-staining technique to identify sensory nerve endings in human thumb ligaments. Cells Tissues Organs 2012; 195 (5) 456-464
  • 25 Mobargha N, Ludwig C, Ladd AL, Hagert E. Ultrastructure and innervation of thumb carpometacarpal ligaments in surgical patients with osteoarthritis. Clin Orthop Relat Res 2014; 472 (4) 1146-1154
  • 26 Eaton RG, Glickel SZ. Trapeziometacarpal osteoarthritis. Staging as a rationale for treatment. Hand Clin 1987; 3 (4) 455-471
  • 27 Bettinger PC, Linscheid RL, Berger RA, Cooney III WP, An KN. An anatomic study of the stabilizing ligaments of the trapezium and trapeziometacarpal joint. J Hand Surg Am 1999; 24 (4) 786-798
  • 28 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA. Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate ligament: a demonstration of its proprioceptive role and clinical relevance. J Arthroplasty 1998; 13 (8) 916-922
  • 29 Hagert E, Lee J, Ladd AL. Innervation patterns of thumb trapeziometacarpal joint ligaments. J Hand Surg Am 2012; 37 (4) 706-714.e1
  • 30 Imai S, Kikuchi K, Matsusue Y. Digital pacinian corpuscle hyperplasia. J Hand Surg Am 2003; 3 (3) 175-180
  • 31 Jones NF, Eadie P. Pacinian corpuscle hyperplasia in the hand. J Hand Surg Am 1991; 16 (5) 865-869
  • 32 Hanesch U. Neuropeptides in dural fine sensory nerve endings—involvement in neurogenic inflammation?. Prog Brain Res 1996; 113: 299-317
  • 33 McDonald DM, Bowden JJ, Baluk P, Bunnett NW. Neurogenic inflammation. A model for studying efferent actions of sensory nerves. Adv Exp Med Biol 1996; 410: 453-462
  • 34 Moraes MR, Cavalcante ML, Leite JA , et al. The characteristics of the mechanoreceptors of the hip with arthrosis. J Orthop Surg 2011; 6: 58
  • 35 Petrie S, Collins JG, Solomonow M, Wink C, Chuinard R, D'Ambrosia R. Mechanoreceptors in the human elbow ligaments. J Hand Surg Am 1998; 23 (3) 512-518
  • 36 Tsuda E, Okamura Y, Otsuka H, Komatsu T, Tokuya S. Direct evidence of the anterior cruciate ligament-hamstring reflex arc in humans. Am J Sports Med 2001; 29 (1) 83-87
  • 37 Dyhre-Poulsen P, Krogsgaard MR. Muscular reflexes elicited by electrical stimulation of the anterior cruciate ligament in humans. J Appl Physiol (1985) 2000; 89 (6) 2191-2195
  • 38 Brandt KD, Dieppe P, Radin E. Etiopathogenesis of osteoarthritis. Med Clin North Am 2009; 93 (1) 1-24, xv xv.
  • 39 Kennedy JC, Alexander IJ, Hayes KC. Nerve supply of the human knee and its functional importance. Am J Sports Med 1982; 10 (6) 329-335
  • 40 Corrigan JP, Cashman WF, Brady MP. Proprioception in the cruciate deficient knee. J Bone Joint Surg Br 1992; 74 (2) 247-250
  • 41 Crisco JJ, Pike S, Hulsizer-Galvin DL, Akelman E, Weiss AP, Wolfe SW. Carpal bone postures and motions are abnormal in both wrists of patients with unilateral scapholunate interosseous ligament tears. J Hand Surg Am 2003; 28 (6) 926-937
  • 42 Hagert E, Garcia-Elias M, Forsgren S, Ljung BO. Immunohistochemical analysis of wrist ligament innervation in relation to their structural composition. J Hand Surg Am 2007; 32 (1) 30-36
  • 43 Haara MM, Heliövaara M, Kröger H , et al. Osteoarthritis in the carpometacarpal joint of the thumb. Prevalence and associations with disability and mortality. J Bone Joint Surg Am 2004; 86-A (7) 1452-1457
  • 44 Anakwe RE, Middleton SD. Osteoarthritis at the base of the thumb. BMJ 2011; 343: d7122
  • 45 Bettinger PC, Smutz WP, Linscheid RL, Cooney III WP, An KN. Material properties of the trapezial and trapeziometacarpal ligaments. J Hand Surg Am 2000; 25 (6) 1085-1095
  • 46 Napier JR. The form and function of the carpo-metacarpal joint of the thumb. J Anat 1955; 89 (3) 362-369
  • 47 Bosmans B, Verhofstad MH, Gosens T. Traumatic thumb carpometacarpal joint dislocations. J Hand Surg Am 2008; 33 (3) 438-441
  • 48 Colman M, Mass DP, Draganich LF. Effects of the deep anterior oblique and dorsoradial ligaments on trapeziometacarpal joint stability. J Hand Surg Am 2007; 32 (3) 310-317