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CLINICAL ORTHOPAEDICS AND RELATED RESEARCH

Number 330. pp 35-39


@ 1996 Uppincott-Raven Publishers

Jon J.P. Warner,MD*; Scott Lephart, PhD,ATC"'*,'


and FreddieH. Fu, MDt

Proprioception is a specialized sensory modal- tures, however, function only at extreme po-
ity that gives information about extremity po- sitions of rotation to prevent excessive trans-
sition and direction of movement. This kind of lation or rotation of the humeral head on the
afferent sensory feedback is probably impor- glenoid. In the midranges of rotation, the
tant in mediating muscular control of the
capsuloligamentous structures remain rela-
shoulder joint. As this articulation is mini-
tively lax.II.19.20.29.36.38.~1
In the midranges of
mally constrained, such a coordinated dy-
namic control of muscles about the joint is nec- motion most joint stability is through dy-
essary for stability during arm motion. The namic action of the rotator cuff and biceps
authors evaluated proprioception in individu- tendons. Contraction of these muscle tendon
als with normal shoulders, unstable shoulders, units creates joint compression and increases
and after surgical stabilization, by assessing the concavity compression fit of the humeral
threshold to detection of passive motion and head into the glenoid socket.7.28 Further-
the ability to passively reposition the arm in more, a coordinated, synergistic contraction
space. In normal shoulders there is no differ- of the rotator cuff and biceps may protect the
ence between the dominant and nondominant
ligamentous structures from injury by in-
shoulder, though in unstable shoulders there is
creasing torque resistance against excessive
a significantly decreased proprioceptive abil-
rotation and preventing excessive transla-
ity. Surgical stabilization normalizes proprio-
ception of the shoulder. tions of the humeral head.6.8.9.13.14.22.32 Be-
cause the glenohumeral ligaments are rela-
tively weak4.31 compared with the knee
Because the human glenohumeral joint is ligaments, such a dynamic protective mecha-
minimally constrained by articular surface nism is important to prevent injury to these
conformity, static and dynamic stability is structures.
provided by the combined effect of both cap-
suloligamentous structures and rotator cuff HYPOTHESIS: THE ROLE OF
and biceps.21,37,40-42
The ligamentous struc- PROPRIOCEPTION
Placementof the hand for upper limb function
is partially dependent on the perception of
From the *Shoulder Service, **Athletic Trainer Pro- joint position and joint motion of the shoul-
gram, and tCenter for Sports Medicine, University of
Pittsburgh, Pittsburgh. PA.
der. This sensorymodality is termed proprio-
Reprint requests to Jon J.P. Warner, MD. 4601 Baum ception and is mediated by peripheral recep-
Boulevard, Pittsburgh, PA 15213. tors in articular, muscular, and cutaneous

35
structures. Specialized nerve endings, propri-
oceptive mechanoreceptors (Pacinian corpus-
cles, Ruffini endings, Golgi tendon organlike
endings), have been shown in the capsule
and ligaments of all joints. 1-3.10.12.15-18.24,33.35.39
These mechanoreceptors are specialized neu-
rons that transduce mechanical defonnation
into electrical signals that transmit infonna-
tion about joint position and motion. 16.17
Stim-
ulation of these receptors results in reflex
muscle contraction about the joint as an adap-
tive control to sudden movements of accelera-
tion or deceleration.3.35 It has been suggested Fig 1. Proprioception testing device. (a) Rota-
that receptors in the joint capsule respond pri- tional transducer (1 :3 mechanical speed reduc-
marily to extreme ranges of motion,'6.17 or tion gear train); (b) motor; (c) moving arm; (d)
deep pressure that may occur with translation control panel; (e) digital microprocessor; (f)
of the humeral head on the glenoid. 10.15-17 pneumatic compression device; (g) handheld
disengage switch; h = pneumatic compression
Proprioceptive sensibility encompasses sleeve. Threshold to detection of passive mo-
the sensation of joint motion (kinesthesia) tion is assessed by measuring angular dis-
and joint position (joint position sense). Nor- placement until the subject senses shoulder
mal proprioceptive sensation and the effect motion and presses the disengage switch (g).
of injury have been shown in the ankle 12.24 (Reprinted with permission from Lephart SM,
Warner JJP, Borsa PA, Fu FH: Proprioception of
and kneel.1.23.16.JOFurthennore, shoulder in- the shoulder joint in healthy, unstable, and sur-
stability is associated with proprioceptive gically repaired shoulders. J Shoulder Elbow
deficits.34 The hypothesis of the authors' Surg 3:371-380,1994).
studies is that the capsuloligamentous struc-
tures may contribute to stability by provid- abduction in the plane of the body with the
ing an afferent feedback for reflexive muscu- elbow at 90°, and all external stimuli were
lar contraction of the rotator cuff and biceps. eliminated by use of a pneumatic cuff ap-
This dynamic reflexive muscle action may plied to the arm, a blindfold, and white noise
protect against excessive translations and ro- introduced through headphones.The shoul-
tations of the glenohumeral joint. Blasier and der was moved at a constantangular velocity
coworkers5 have proposed a similar mecha- of 0.5° per second, with random movement
nism. Moreover, the authors have hypothe- into either internal or external rotation. The
sized that injury to these ligaments will re- test subject indicated when motion was felt
sult in measurable deficits in proprioception. by turning off the machine with a button he
or she held in the other hand. This tested
RECENT STUDIES TTDPM. The RPP was measuredby asking
the patient to reproducethe initial position in
For the past 5 years the authors have studied which the shoulder had been placed after it
proprioception in normal, anteriorly unstable, was moved from that reference point. Accu-
and surgically reconstructedshoulders.25.27 racy was measured as the error in degrees
from the starting position. {
TestingMethods
U sing a specialized testing apparatus(Fig I) Results
threshold to detection of passive motion and A total of 90 subjectswere tested:40 healthy
reproduction of passive positioning was college ageindividuals with normal shoulders;
tested. The shoulder was positioned at 900 30 patients with documented posttraumatic,
anteriorinstability; and 20 patientswho hadei- all testing conditionsand there was no signifi-
ther arthroscopicor open Bankart repairs. All canceof hand dominance(Fig 2A). The sub-
subjectswere comparablein genderand age. It jects with unstable shouldershad a TrDPM
was determined that the TTDPM in subjects value of approximately2.80 and this was sig-
with normal shouldersaveraged1.5to 2.10for nificantly (p < 0.005)increasedcomparedwith

cr Unstable
.Noninvo've.
.p .0.05

a
"
~
~B.
0
l-
I-

~ Involved
.Noninvolved

-u;
..
OJ

~2
0.
0.
CC

E Nou!. ~ IR NoUI. ~ ER ER -IR 30' ER ~ ER

Fig 2A-E. (A) Results are means and standard error of the mean forTTOPM (degrees) of the domi-
nant and nondominant shoulder from starting positions of neutral rotation and 300 external rotation
moving into both internal and external rotation. (8) Results are means and standard error of the
mean forTTOPM (degrees) of unstable and uninvolved shoulder from starting positions of neutral ro-
tation and 300 external rotation moving into both internal and external rotation. (C) Results are
means and standard error of the mean for RPP (degrees) for unstable and uninvolved shoulders
from starting positions of neutral and 300 external rotation moving into both internal and external ro-
tation. (0) Results are means and standard error of th mean for TTOPM (degrees) in reconstructed
and uninvolved shoulders from starting positions of neutral rotation and 300 external rotation moving
into both internal and external rotation. (E) Results are means and standard error of the mean for
RPP (degrees) in reconstructed and uninvolved shoulders from staring positions of neutral rotation
and 300 external rotation moving into internal and external rotation. (Reprinted with permission.27)

3D"
Clinical Orthopaedics
38 Warner et al and Related Research

the shoulders in the subjects with normal and direction of motion. Orthop Rev 23:45-50,
1994.
shoulders(Fig 2B). RPPwasalso significantly 6. Blasier RB, Goldberg RE. Tothman ED: Anterior
(p < 0.0 l) lessaccurateby approximately loin ~houlder ~tability: Contribution~ of rotator cutf
the unstableshoulderscomparedwith the nor- torces and cap~ularligamentsin a cadavermodel. J
Shoulder Elbow Surg 1:1~150. 1992.
mal shoulders (Fig 2C). In patients whose 7. Bowen MK. DengX. Warner JJP,Warren RF: The
shoulder instability had been repaired. the effect of joint compression on the stability of the
TfDPM and RPP were no different from that glenohumer.lljoint. Tran~ Orthop Res Soc 17:289.
1992.
in patientswith normalshoulders(Fig 2D). 8. Br.ldley JP.Tibone JE: Electromyogr.lphic analysis
of muscle action about the shoulder. Clin Sport~
Med 10:789-805. 1991.
CONCLUSIONS 9. Cain PR, Mut~chlerTA. Fu FH. Hamer CD: Ante-
rior stability of the glenohumeraljoint: A dynamic
It is concluded that there is an associationof model.AmJ Sports Med 15:144-148, 1987.
proprioceptive sensibility with shoulderinsta- 10. Clark FJ, BurgessPR: Slowly adapting recepto~ in
the cat kneejoint: can they signal joint angle.?J Neu-
bility, and surgeryrestoresnormal sensibility; rophy~ioI38:1448-1463. 1975.
however,the testing speedused in the present I I. Emery RJ. Mullaji MB: Glenohumeral instability in
study was much slower than the speedsthat normal adolescents.J Bone Joint Surg73B:406-408.
1991.
occur with throwing or swimming. Therefore, 12. Glencro~sD. Thornton E: Position sense following
it is difficult to extrapolatedirectly to the clin- joint injury. J SportsMed 21:23-27, 1981.
ical situation. It is proposedthat 1 mechanism 13. Glousman R, JobeFW. Tibone JE, Perry J. Moynes
DR: Dynamic electomyographic analysis of the
for gradual developmentof shoulderinstabil- throwing shoulderwith instability. J Bone Joint Surg
ity may be cumulative injury to the capsu- 70A:220-226. 1988.
loligamentousstructureswith loss of this pro- 14. GowanJP. JobeF\I!, Tibone JE, Perry J, Moyne:-DR:
A completeelectromyographicanalysis of the shoul-
prioceptive feedback mechanism and, thus, der during pitching. Am J Sports Med 15:586-590,
reflexive muscular protection against exces- 1987.
sive humeral head translationsand rotations. 15. Grigg P: Responsesof joint afferent neurons in cat
medial articular nerve to active and passive move-
Blasier and colleaguess.6have suggested ments of the knee. Brain Res 118:482-485, 1976.
that individuals with generalizedligamentous 16. Grigg P, Hoffman AH: Properties of Ruffini affer-
laxity have poorer proprioceptive abilities in ents revealed by stressanalysis of isolated sections
of cat kneecapsule.J NeurophysioI47:41-54. 1982.
their shoulders, though their numbers were 17. Grigg P, Hoffman AH: Calibrating joint capsule
small and their testing methods were some- mechanoreceptoras in-vivo soft tissue load cells. J
what different than those used here. Future Biomech22:781-785,1989.
18. Guyton AC: Textbook of Medical Physiology. 5
studies will examinethe effectivenessof pro- Philadelphia,WB Saunders104-146, 1976.
prioceptive training in nonoperativetreatment 19. HarrymanIII DT, Sidles JA, Clark JM, et al: Trans-
of instability, and the affect of constitutional lation of the humeral head on the glenoid with pas-
sive glenohumeral motion. J Bone Joint Surg
hyperlaxity on proprioceptivesensibility. 72A:1334-1343,1990.
20. Harryman III DT, Sidles JA, Harris SL, Matsen III
FA: Laxity of the normal glenohumeral joint: A
References quantitative in-vivo assessment.J Shoulder Elbow
I. Barrack RL, Skinner HB, Buckley SL: Propriocep- Surg 1:66-76, 1992.
tion in the anterior cruciate ligament deficient knee. 21. ltoi E, KuechleDK. NewmanSR. Morrey BF, Ar K-N:
Am J Sports Med 17:1-6, 1989. Stabilizingfunctionof the bicepsin ~tableand unstable
2. Barrack RL, Skinner HB. Brunet ME: Joint laxity shoulders.J BoneJointSurg75B:546-55I, 1993.
and proprioception in the knee. Physiol Sports Med 22. Itoi E, Newman SR, Kuechle DK, Morrey BF. An K-
N: Dynamic anterior stabilizers of the shoulder with
11:130-135,1983.
3. Barrett OS, Cobb AG, Bently G: Joint propriocep- the arm in abduction. J Bone Joint Surg 76B:
tion in normal, osteoarthritic and replaced knees. J 834-836, 1994.
Bone Joint Surg 13B:53-56, 1991. 23. KennedyJC, Alexander 11,HayesKC: Nerve supply
4. Bigliani LU, Pollock RG, Soslowski U. et al: Ten- of the human knee and its functional importance.
sile properties of the inferior glenohumeral liga- Am J SportsMed 10:329-335, 1982.
ment. J Orthop Res 10:187-197, 1992. 24. KonradsenL, RavenJB: Ankle instability caused by
5. Blasier RB, Carpenter JE, Huston U: Shoulder prolonged peroneal reaction time. Acta Orthop
proprioception. Effect of joint laxity, joint position, Scand61S:338-390, 1990.
Number 330
September. 1996 Pathoetiology of Shoulder Instability 39

25. LephartSM. ConnersC, Fu FH. Irrgang11,BorsaPA: 35. Sojka P, Sjolander P. Johansson H, Djup-
Proprioceptivecharacteristicsof trainedand untrained sjobacka M: Influence from stretch sensitive re-
collegefemales.Med Sci SportsExen:23:4,1991. ceptors in the collateral ligament of the knee
26. Lephart SM. Kocher MS, Fu FH, Borsa PA, Harner joint on the gamma-muscle spindle systems of
CD: Proprioception following ACL reconstruction.1 flexor and extensor muscles. Neurosci Res
SportsRehabill:188-196, 1992. 11:55-62,1991.
27. LephartSM. Warner llP, Borsa PA, Fu FH: Proprio- 36. Terry GC, Hammon D, France P, Norwood L: The
ception of theshoulderjoint in normal. unstable,and stabilizing function of passive shoulder restraints.
surgically repaired individuals. 1 Shoulder Elbow AmJ SportsMed 19:26-34.1991.
Sure 3:371-379, 1994. 37. Turkel SJ. Panio MW, Marshall JL, Girgis FG: Sta-
28. Lippitt SB, VanderhooftE. Hanis St. et al: Gleno- bilizing mechanismspreventing anterior dislocation
humeralstabilityfrom concavity-compression: A quan- of the glenohumeral joint. J Bone Joint Surg
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29. O'Connell PW, Nuber GW, Mileski RA, lauten- 38. Uthoff H, PiscopoM: Anterior capsular redundancy
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ligaments to anterior stability of the shoulderjoint. Joint Surg 67B:363-365, 1985.
Am 1 Spons Med 18:449-456, 1990. 39. VangsnessCT, Ennis M: Neural anatomy of the hu-
30. Pope MH. 10hnson RH, Brown DW: The role of man glenoid and shoulder ligaments. Annual Meet-
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31. ReevesB: Experimentson tensile strengthof the an- 40. Warner 11P:The Gross Anatomy of the Joint Sur-
terior capsular structures of the shoulder in man. 1 faces, Ligaments, Labrum, and Capsule. In Mat-
Bone 10int Surg50B:858-865. 1968. sen III FA, Fu FH, Hawkins RJ (eds). The
32. Rodosky MW. Harner CD, Fu FH: The role of the Shoulder: A Balance of Mobility and Stability.
long headof the bicepsmuscle and superior glenoid Rosemont, IL, AAOS 7-27, 1993.
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Sports Med 22:121-130.1994. M: Dynamic capsuloligamentous anatomy of the
33. Skoglund Cf: 10int Receptors and Kinesthesia. glenohumeral joint. J Shoulder Elbow Surg
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CLINICAL ORTHOPAEDICS AND RELATED RESEARCH
Number 330. pp 40-44
@ 1996 Lippincott-Raven Publishers

Coracoacromial Ligament: In Situ


Load and Viscoelastic Properties in
Rotator Cuff Disease
Louis J. Soslowsky,PhD; CharleneH. An, MS;
Christopher M. DeBano, BS; and JamesE. Carpenter,MD

The coracoacromial ligament plays a role in The most common cause of shoulder pain
rotator cuff disease.The changes in the in situ and disability in the worker whose occupa-
load and viscoelastic properties of the cora- tion requires repetitive overhead movements,
coacromial ligament in shoulders with rotator in the athlete engaging in repetitive overhead
cuff tears were evaluated. Coracoacromiallig- activities, and in the elderly population at
aments from 16 cadaveric shoulders (8 with ro-
large is injury to the rotator cuff tendons.Al-
tator cufT tears, 8 without tears) were evaluated
via biomechanical testing of bone ligament bone
though the etiology of this disease is un-
specimens. An in situ load existed in the cora- known, one hypothesisis that compressionor
coacromialligaments of 19.6 :t: 15.4 N (rotator impingementof the supraspinatustendon oc-
cuff tear) and 18.3 :t: 9.8 N (no rotator cuff curs under the coracoacromial arch.5-7The
tear). This difference was not statistically sig- arch is composed of the coracoid, coraco-
nificant. Cyclic loading of the ligaments acromial ligament, and acromion (Fig I).
demonstrated a greater drop in peak stress in This impingement of the cuff tendons is
rotator cufT tear shoulders than in normal thought to cause tendon injury resulting in
shoulders, whereas the stress relaxation re- pain, disability, and ultimately may lead to a
sponse was not different. These changes in the tear of the rotator cuff. It has been shown
coracoacromial ligament in shoulders with
that the prevalence of rotator cuff tears is
cuff tears may be attributable to ultrastruc-
higher when the bony anatomy of the acro-
tural changes within the ligament as a result of
an altered loading environment. It remains un- mion is more curved or hooked (Type II or
known whether they occur as a result of a rota- III), possibly as a result of reduced subacro-
tor cufT tear or if they contribute to the patho- mial space.I.2In some cases,the lateral band
genesis of cuff disease. of the coracoacromialligament has been im-
plicated as the portion of the arch (Fig l) re-
sponsible for the impingement.S.IO.11
Previous studies have shown differences
in the geometric and material properties
(from constant strain rates tests) of the cora-
From Orthopaedic ResearchLaboratories,The Univer- coacromialligament from shoulders with ro-
sity of Michigan, Ann Arbor, MI. tator cuff tears as compared with those from
Supported by the Whitaker Foundation.
normal shoulders.9 Anecdotal clinical evi-
Reprint requests to Louis J. Soslowsky, PhO, Or-
thopaedic Research Laboratories, The University of dence has suggested that the ligament may
Michigan, 400 North Ingalls. Room 0-0161, Ann Ar- be under an increased strain and tension in
bor, MI 48109-0486.

40

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