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THE GROSS ANATOMY OF THE PERI-ARTICULARTISSUES OF THE SHOULDER JOINT

BY

W. J. H. NAUTA and J. M. F. LANDSMEER

Department ofAnatomy and Embryology, State University, Leiden, Netherlands

Since it has become evident that the pathologicalchanges underlying disorders of the shouldermechanism are not, in a number of cases, localizedin one of the major joints of this region (scapulo-humeral and acromio-clavicular joints), but, instead,in the tissues surrounding these joints, the need fora thorough knowledge of the anatomy of this tissuehas imposed itself on all those who have to deal withsuch disorders. In the current textbooks ofanatomy, however, little attention has been paid tothe structures surrounding the shoulder joints.Although more or less adequate accounts of thematter are found in Rouviere's (1945) and in Frohseand Fraenkel's (1908) textbooks, and in somespecial papers dealing with the subject (Henke,1874; Pfuhl, 1934; Kahlmeter, 1941) the distribu-tion ofthese works has, perhaps, not been sufficientlywide to provide for a satisfactory introduction ofthe pertinent facts into clinical medicine. It is forthis reason that we submit the present account-which is based partly on the foregoing papers andpartly on our own observations on a large amount ofdissecting-room material-to those clinicians whowill be most interested in the anatomical basis ofshoulder movements.

Anatomical DescriptionA glance at a suitable illustration in an atlas of

anatomy will immediately disclose the importantfact that the glenoid fossa of the scapula is overhungon the cranial side by an osteofibrous arch, the so-called fornix humeri, which is formed by (from'before backwards) the coracoid process, the coraco-acromial ligament, and the acromion (Fig. la)..The fornix humeri bridges the lateral exit of thesupraspinous fossa (Fig. 4). The space betweenthis arch and the glenoid fossa is largest dorsally,that is, under the acromion. A large part of thisspace is occupied by the tendon of the supraspinatusmuscle (Fig. lb).

The capsule of the shoulder joint is largelyenveloped by the tendons of the muscles whichsurround the joint. The subscapularis, supra-spinatus, infraspinatus, and teres minor tendons alljoin in the formation of what Poirier (1904) hasaptly termed a musculo-tendinous cuff (coiffemusculo-tendineuse), surrounding and, to a variableextent, blending with the joint capsule. On thecranial side the cuff is completed by the coraco-humeral ligament, which bridges the gap betweenthe supraspinatus and subscapularis tendons (Fig.lb). Between the subscapular tendon and thecoraco-humeral ligament there is a slit-like orifice(the oval foramen of Weitbrecht) which allows thebursa subscapularis to anastomose with the joint.

It is especially the cranial part of the musculo-tendinous cuff that demands our attention, since thispart, which is formed by the supraspinatus tendonand the ventrally adjacent coraco-humeral ligament,is separated from the undersurface of the fornixhumeri virtually only by space. During abductorymovements in the shoulder joint the supraspinatusmuscle withdraws its tendon through the narrowtunnel under, the fornix humeri. At the final stageof the movement, however, the tendon is raised byits apophysis (the greater tubercle) to such anextent that its lateral part impinges on the acromionand the coraco-acromial ligament. Further abduc-tion in the joint is checked by this occurrence, but itseems certain that some additional abduction isrendered possible by an outward rotation of thehumerus, which moves the tendon and its apophysisbackwards into a position underneath the acromion,where more space is available. In view of the ever-returning conflict between the upper part of themusculo-tendinous cuff on the one hand and thefornix humeri on the other, it is not surprising that abursa has developed in the narrow space between thetwo. This bursa is usually designated the sub-deltoid bursa, but because this name is liable to

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AXATOMY OF THE SHOULDER JOINT

CORACOID PROCESSCORACO-ACROMIAL LIGAMENT I

ACROMION.

SUBSCAPULARIS TENDON

CORACO-HUMERAL LIGAME

SUPRASPINATUS TENDOIP-INFRASPINATUS TENDON

TERES MINOR TENDON

FIG. 1.-Schematic drawings of lateral aspects of: (a) fornix humeri, and (b) musculo-tendinous cuff of theshoulder joint. (b) has been redrawn and amplified from McGregor (1943).

cause confusion (see below) it will be referred to inthe following as " subacromial bursa" (Fig. 3). Tofacilitate an understanding of its topography it willbe necessary to deal with the fascial relations of theshoulder region.

Fascial Relations of the Shoulder Region.-On-the medial side the coraco-acromial ligament (whichcovers the lateral exit of the supraspinous fossa) iscontinuous with the much thinner supraspinousfascia. Laterally, it continues into the importantsubdeltoid fascia, a connective-tissue sheet ofconsiderable strength stretched out over the greatertubercle and the surgical neck of the humerus (Fig.2, 4, 6). Dorsally, the subdeltoid fascia continuesinto the infraspinous fascia, a strong fascia coveringthe infraspinous and teres minor muscles, andventrally it passes over into the subscapular fasciawhich covers the subscapularis muscle. The sub-deltoid fascia can thus be regarded as the result of ajunction of the several fasciae covering the muscleswhich take part in the formation of the musculo-tendinous cuff (that is, the fasciae subscapularis,supraspinata, and infraspinata). Distally, a smalldistance above the insertion of the deltoid muscle,the subdeltoid fascia blends with the periosteum ofthe surgical neck and is thus attached to the humerus.

Subdeltoid Fascia.-It will be clear from the fore-going description that the subdeltoid fascia is part ofa vast sheet of connective tissue which envelops thewhole complex formed by the upper part of thehumerus, the shoulder joint, with its musculo-tendinous cuff, and the muscles contributing to this

cuff (Fig. 2). On the scapular side this sheet isdivided into three divisions-the subscapular,supraspinous, and infraspinous fasciae-by thebony rims separating the scapular fossae of the samenames; on the lateral surface of the upper part ofthe humerus the three divisions unite to form thesubdeltoid fascia, which has a skeletal attachment tothe surgical neck of the humerus. It will benoticed that the fornix humeri is a strongly rein-forced strip of that part of the connective-tissuesheet under consideration which covers the superiorpart of the musculo-tendinous cuff (supraspinatustendon and coraco-humeral ligament).A further point of interest is the relation between

the subdeltoid fascia and the short head of thebiceps. The tendon of this muscle is sometimesfound to possess a broad lateral expansion blendingwith an aponeurotic subdeltoid fascia (Fig. 6).Although in the majority of cases this connexionis less strongly developed, a fibrous attachment ofthe lateral margin of the caput breve tendon to thesubdeltoid fascia is a constant finding (Fig. 2b). Itseems probable that the fascia can thus be madetaut by the caput breve of the biceps.On its ventral side the subdeltoid fascia is joined

by the fascia coraco-clavi-pectoralis (costo-coracoidmembrane). A superficial part of this fascia, afterhaving covered the pectoralis minor muscle, extendslaterally over the conjoined tendons of the caputbreve, of the biceps and the coraco-brachialismuscles and immediately afterwards comes to coverthe subdeltoid fascia. After it has run freely overthis fascia for a short distance the two fasciae blend

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166 AXNALS OF THE AUMAMTIC DISEAStSSUPRASPINOUS FASCIA

*CORACO-ACBOIAI U6NMENT 1A ^0% FADELTOID MUSCLE IN

DELTOID MUSCLE I

SUBDELTOID FASCIA

SUPRASPINATUS TENDONT ANTERII

CAPSULE a X U PLASUOSCAPULABIS

SUBSCAPULAR FASI

PECTORALIS MINO

a

SUBDELTOID FASIA BICEPS(CAPSREV.) PECTORALIS MAJOR

COSTO-CORACOID MEMBRANE

CORACO-BRACHIALIS

FIG. 2.-Schematic sections through the shoulder joint (a) in the frontal and (b) in the horizontal plane.The subacromial bursa is indicated by broken lines.In (a) notice that the subdeltoid fascia is a lateral extension of the coraco-acromial ligament (the

supraspinous fascia being the medial continuation of this ligament). Notice also that the coraco-acromialligament and the supraspinatus tendon are incorporated in the wall of the bursa. The small bundles ofthe deltoid muscle attaching to the -subdeltoid fascia are marked by an asterisk.

(b) shows the continuation of the subdeltoid fascia into the subscapular and infraspinous fasciae.Notice the relation of the subdeltoid fascia to the tendon of the caput breve m. bicipitis and to the costo-coracoid membrane (compare with Fig. 6).

along an approximately vertical line (Fig. 2b; inFig. 6 the fascia has been rolled up to this line).The Subacromial Bursa.-The subdeltoid fascia is

covered by the deltoid muscle, with which it isconnected by a loose, felt-like connective tissue. Wehave been unable to find a bursa in this tissue in anyof our preparations. For this reason we have fol-lowed Frohse and Fraenkel (1908) in omitting thename subdeltoid bursa for what is more properlycalled the subacromial bursa. It is of importanceto note that a rather variable number of smallbundles of the deltoid muscle, originating from thetuberositas deltoidea of the humerus, is constantlyfound attached to the upper part of the subdeltoidfascia in a proximal direction (Fig. 2a). Pre-sumably these bundles exert a distal pull on thefascia during abduction of the arm, and they maythus prevent the formation of folds in the fasciawhich would be liable to be incarcerated between thesupraspinatus tendon and the fornix humeri.

Proximal to the distal attachment of the sub-deltoid fascia to the periosteum of the humerus, alayer of extremely loose tissue is woven between thesubdeltoid fascia and the surgical neck of thehumerus. More proximally, just over the supra-spinatus tendon, the subdeltoid fascia is separated

from this tendon by the subacromial bursa (seebelow). It may be inferred from this fact-andmanipulation of the upper arm in the cadaver showsthe inference to be correct-that every movement ofthe upper arm in the shoulder joint is accompaniedby a displacement of the upper part of the humeruswith the musculo-tendinous cuff against the insideof the fibrous sheath encapsulating these structures.Since the fornix humeri forms a rigid and fixed partof this sheath the displacement relative to the sheathis greatest at this point.

It is, therefore, not surprising that the subacromialbursa is constantly found to occupy the narrow spaceunder the fornix humeri, separating the latter fromthe upper part of the musculo-tendinous cuff (thesupraspinatus tendon and the coraco-humeralligament). Friction, however, is exerted not onlyby the musculo-tendinous cuff but also by the outersurface of the greater tubercle, and it is exerted notonly against the under surface of the fornix humeribut also against the inner side of the sub-deltoidfascia (the latter of these two points will be under-stood if one realizes that, as mentioned in theprevious account, the subdeltoid fascia is kept ex-tended during abduction by part of the bundles ofthe deltoid muscle (Fig. 2a) ). This explains the

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ANATOMY OF THE SHOULDER JOINT

CORACO-ACROMIAL LIGAMENT

0- CORACOID PROCESS

CORACO-HUMERAL LIGAMENT

CAPSULE

SUBSCAPULARIS TENDON

FIG. 3.-Semidiagrammatic drawing of the lateral aspect of the shoulder joint and its surroundings afterexarticulation of the humerus. Notice that the capsule is in large part surrounded by the musculo-tendinous cuff, components of which are labelled. The coraco-humeral ligament radiates into thecapsule. The subacromial bursa is situated between the upper part of the cuff and the fornix humeri.The subdeltoid fascia, which covers the bursa, has been removed. The arrow points through aforamen into the subcoracoid bursa.

fact that the bursa is constantly found to extendlaterally beyond the insertion of the supraspinatusmuscle over the outer surface of the greater tubercleand under cover of the subdeltoid fascia. Since thislateral extension necessarily follows the downwardslope of the tuberosity, this is the deepest part of thesubacromial bursa, and corpuscular substances areliable to collect here. The degree of lateral extensionis, however, subject to important individual variation.A remarkably small lateral extension, for instance,is shown in Fig. 4; and Fig. 5 shows a subacromialbursa which reaches distally far over the lateral sur-face of the great tuberosity. When the arm is kepthanging down to the side of the body the opposite(medial or proximal) margin of the bursa rarely

extends for more than a small distance mediallybeyond the medial border of the coraco-acromialligament. This small part of the bursa is covered bythe supraspinous fascia (Fig. 2a). Dorsally, thebursa constantly extends for some distance unde.r-neath the acromion. To the ventral side the bursadoes not, as a rule, extend farther than the base of thecoracoid process, but Pfuhl (1934) whose papergives a good impression of the variability of thebursa subacromialis, records several instances oflarger ventral extension (recessus subcoracoideus) ofthe bursa.With respect to the relation of the subacromial

bursa to its surrounding tissues the following factsare of importance. As a rule, the bursa can easily

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ANNALS OF THE RHEUMATIC DISEASES

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ANNALS OF THE RHEUMA TIC DISEASES

be exposed by removing the subdeltoid fascia, whichis rather loosely attached to the outer bursal wall(Fig. 5). In a number of our preparations, however,the subdeltoid fascia consisted of several layers, andin such cases it was difficult to identify the wall of thebursa. Quite a different relation exists between thebursa and the fornix humeri. The coraco-acromialligament cannot be removed from the subjacentbursa without causing damage to the latter's outerwall. The acromion has a similar relation to thebursa. Like the adjacent part of the coraco-acromial ligament its under-surface is incorporatedin the outer wall of the bursa. The remainder ofthe coracc-acrcmial ligament (the part connectedwith the coracoid process) may lie free over thebursa, but it often also forms part of the outer wallof the latter. The relations of the inner wall of thesubacromial bursa are as follows. This wall sostrongly adheres to the underlying supraspinatustendon that it is possible to say that the tendon formspart of the inner wall of the bursa. Where the bursacovers the greater tubercle it can easily be lifted fromthe latter by blunt dissection.The strong adherence of the bursa to the supra-

spinatus tendon will cause the inner wall of theformer to be displaced with every movement of thelatter. During abduction, for instance, the innerwall of the bursa will be drawn medially with thesupraspinatus tendon. The position of the outerwall of the bursa is certainly less dependent on theposition of the humerus in the shoulder joint, sincepart of it is formed by the completely fixed fornixhumeri, while the remainder of the outer wall is inlarge part related to the subdeltoid fascia, whichduring abduction is kept taut by small bundles of thedeltoid muscle. The medial displacement of theinner wall of the bursa during abduction will implya medial shift of its distal line of reflexion, and thisshift is presumably facilitated by the loose attach-ment of the outer wall of the bursa to the subdeltoidfascia.

DiscussionIt is of great interest to note that Pfuhl (1934) has

demonstrated the presence of a layer of cartilaginoustissue covering that part of the undersurface of theacromion which stands in direct relation to thecavity of the subacromial bursa. On the basis ofthis finding Pfuhl has advocated the conception thatthe subacromial bursa should be regarded as a truejoint between the fornix humeri and the musculo-tendinous cuff. The shoulder joint as a functionalentity would thus be composed of a scapulo-humeral" Hauptgelenk " and a subacromial " Nebenge-lenk ". The intervening part of the musculo-tendinous cuff, which is formed by the supraspinatustendon and the coraco-humeral ligament, is regarded

by Pfuhl as an intra-articular disc. It is a wellknown fact (see, for instance, McGregor, 1943)that rupture of the supraspinatus tendon mayestablish a communication of the shoulder joint withthe subacromial bursa. It seems that such rupturesusually result from acute overaction of the supra-spinatus muscle, but Pfuhl (1934) has observed largeperforations of the tendon accompanying severearthritis deformans of the shoulder joint, so that itwould not seem impossible that some cases of ruptureof the supraspinatus tendon are caused by repeatedtrauma of the tendon against the rough articularsurface of the humeral head.There is, indeed, sufficient reason to regard the

subacromial bursa as a true joint rather than as anequivalent to the numerous other bursae whichassist in the proper functioning of the apparatus ofmotion. Apart from Pfuhl's argument that a smallpart of the wall of the bursa is formed by carti-laginous tissue, the following other facts can beadvanced in favour of this conception: (l) thesubacromial bursa is the only bursa which is knownto be able to reduce friction between two skeletalelements (greater tubercle of the humerus versusunder surface of the acromion), and (2) the bursa iscovered by and attached to a strong aponeuroticfascia, the subdeltoid fascia, which is kept extendedduring movements by some bundles of the deltoidmuscle and by the short head of the biceps. Com-parable mechanisms serving to prevent the formationof incarcerated folds in the capsule are formed inmany other joints (capsule stretchers).

Although it would thus seem justified to speak of asubacromial joint, it is evident that the joint is anexceptional one functionally and morphologically.With regard to its function, it should be realized thatits prime significance lies in the fact that it reducesthe conflict which is bound to arise between anexceptionally mobile joint like the shoulder joint andthe rigid tissues surrounding this joint. Mor-phologically it differs from most other joints in thatonly a very small part of its wall consists of cartilageand that it is largely a synovial sac with, of course,merely a virtual cavity. It follows that a slightproliferation of the wall of the subacromial joint inthe course of an inflammatory process may sufficeto result in partial or complete obliteration of thejoint cavity with consequent anchorage of themusculo-tendinous cuff of the shoulder joint to thecompletely rigid fornix humeri, a condition whichwill greatly decrease the range of movements of theupper extremity.

SummaryThe interest of clinical rheumatology for the

periarticular tissues of the shoulder joint, together

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ANATOMY OF THE SHOULDER JOINT

with the fact that current textbooks of anatomy failto give satisfactory descriptions of these tissues, hasled the authors to investigate this region anew. Thefollowing account is based on dissecting-roommaterial.A description has been given of the capsule of the

shoulder joint and its relation to the fornix humeri(coraco-acromial ligament and acromion). Thefornix humeri is part of a much larger fibroussystem, the subdeltoid fascia. This fascia anteriorlyfuses with the subscapularis fascia, posteriorlywith the infraspinous fascia, and laterally to theperiosteum of the surgical neck of the humerus.Tendon-fibres of the short head of the biceps fanout into this fascial sheet, whereas muscular fibresof the deltoid muscle insert into it in the disto-proximal direction. Both may serve to stretchthis fascial sheet during movements of the shoulder,thus preventing it from becoming enfolded underthe fomix humeri. Between the capsule of theshoulder-joint on the one hand, and the fornixhumeri and its lateral extension (the subdeltoidfascia) on the other, a bursa has developed-thesubacromial bursa. A description has been givenof the relation of this bursa to the surroundingtissues. A suggestion is made as to the role of thesubdeltoid fascia and subacromial bursa in move-ments of the shoulder.

The authors wish to thank Mr. E. Bollee, Departmentof Anatomy, Leiden, for the accompanying photographs,and Mr. E. Brandli, Institute of Anatomy, Zurich, for thedrawings which illustrate this paper. They are alsoindebted to Dr. J. J. Siemelink, Utrecht, for valuablecriticism during the preparation of the paper.

REFERENCESFrohse, F. and Fraenkel, M. (1908). " Die Muskeln des

menschlichen Armes." In " Handbuch der Ana-tomie des Menschen." K. von Bardeleben. II,2, 2. Gena.

Henke, K. (1874). "Ein Beitrag zur Pathologie desSchultergelenke." Inaug. diss. Marburg.

Kahlmeter, G. (1941). Z. Rheumaforsch., 4, 251.McGregor, A. Lee. (1943). "Synopsis of Surgical

Anatomy." Bristol.Pfuhl, W. (1934). Morph. Jahrb., 73, 300.Poirier, P. (1904). "Traite d'Anatomie Humaine."

Paris. Battaille et Cie.Rouvi6re H. (1945). " Anatomie Humaine, descriptive

et topographique." Paris. Massonet Cie.

L'Anatomie Macroscopique des TissusPeriarticulaires de l'Epaule

RESUM9L'interet du probleme de la periarthrite humero-

scapulaire, specialement dans un sens rhumatologique,a conduit les auteurs a une recherche anatomique nouvellesur la r6gion scapulaire. La capsule de l'articulationhumero-scapulaire et ses relations a l'egard du fornixhumeri sont decrites. Le fornix humeri (ligamentcoraco-acromial et acromion) fait part d'un systemeaponevrotique plus etendu, c'est a dire, l'aponevrosesous-deltoidienne. Cet apon6vrose se confond ant6rieurement avec l'apon6vrose sous-scapulaire, post6-rieurement avec l'apon6vrose du sous-epineux, laterale-ment avec le periosteum du col chirurgical de l'hum6rus.Des fibres tendineuses de la courte portion du biceps sediversent dans l'aponevrose sous-deltoidienne, tandis quedes faisceaux musculaires s'attachent sur celle-ci dans unedirection disto-proximale. Il est bien s&r que les deuxradiations font un dispositif d'un appareil de tensionpour l'aponevrose pendant les mouvements de l'epaule.Entre la capsule de l'articulation humeroscapulaire et lefornix hum6ri et son extension laterale se trouve unebourse sereuse, c'est 'a dire, la bourse sous-acromiale.Les auteurs donnent une description de cette bourse et deses relations a l'egard du revetement aponevrotique del'epaule. L'attention est fixee sur l'interet de la fonctionde la bourse sous-acromiale et de l'aponevrose sous-deltoidienne pour les mouvements l'paule.

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THE GROSS ANATOMY OF THE PERI-ARTICULAR TISSUES … › content › annrheumdis › 7 › 3 › 164.full.pdfchanges underlying disorders of the shoulder mechanismare not, in anumberofcases,