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Tendons, ligaments, and capsule of the rotator cuff. Gross and

microscopic anatomy
JM Clark and DT Harryman
J Bone Joint Surg Am. 1992;74:713-725.

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Tendons, Ligaments, and Capsule of the Rotator Cuff

GROSS AND MIcRoscoPIc ANATOMY*t

BY J. M. CLARK. MI).. PH.D4. AND D. T. HARRYMAN. II. M.D4. SFAFFI,F. WASIIIN(IION

In vestigatio,i /)e’rtor,nec/ at the A (hilt Reconstructioii (111(1 S/ioulder .Servic(’s, U,iiversit’ of tVas/iiii,t’tcoi .S’e/iool of Itleilici,ie, Seattle

ABSTRACT: We investigated the structure of the myo- configurations ofthe myotendinous cuffand the capsular
tendinous rotator cuff in thirty-two grossly intact cuffs and ligamentous components can withstand physiologi-
from thirty fresh cadavera of subjects who had been cal loading and minimize concentrations of stress. The
seventeen to seventy-two years old at the time of death. normal anatomical features that enable the rotator cuff
We studied the gross anatomy of the capsule and liga- to function effectively throughout life and the features
ments of the cuff, as well as histological sections of the that may he important in the development of localized
tendons of the subscapularis, supraspinatus, and infra- lesions ofthe cuff have received relatively little attention.
spinatus muscles. The tendons were found to splay out Most gross anatomical studies have dealt primarily with
and interdigitate to form a common, continuous inser- pathological changes observed in randomly selected spe-
tion on the humerus. The biceps tendon was ensheathed cimens at autopsy4 ‘.

by interwoven fibers derived from the subscapularis and

Materials and Methods
supraspinatus tendons. The anterior margin and bursal
surface of the supraspinatus tendon were enveloped by Eighty shoulders from seventy-eight cadavera were
a thick sheet of fibrous tissue derived from the coraco- obtained within twenty hours after death. Forty-eight of
humeral ligament. Fibers from the coracohumeral and the eighty shoulders were excluded because of gross
glenohumeral ligaments were found concentrated in a pathological changes in the myotendinous cuff. such as
plane between the capsule and the tendons of the cuff. tears or thinning of the rotator cuff. that were not recog-
Microscopically, in the region of the supraspinatus and nized until the cuff had been dissected.
infraspinatus tendons, the cuff was composed of five In thirty-two shoulders from thirty cadavera, the
layers defined by the attachments and orientations of myotendinous cuff was intact. In two cadavera of men,
the fibrous elements in each of these layers. both shoulders were studied; the ages at the time of death
CLINICAL RELEVANCE: In the rotator cuff, which is had been twenty-one and sixty years. There were twelve
a composite of the capsule, the ligaments, and the ten- cadavera of men and sixteen cadavera of women, and the
dons around the shoulder, the supraspinatus tendon is age at the time of death ranged from seventeen to sev-
reinforced by fibers of the coracohumeral ligament and enty-two years.
fibers from adjacent tendons. Therefore, lesions in the The entire scapula and proximal one-third of the
area of the supraspinatus tendon may involve one or humerus with the attached soft tissues was removed en
more of these elements, and the evolution of a tear in bloc in order to keep the shoulderjoint intact.The en bloc
this area may be determined by the location ofthe initial Specimens were then evaluated by various methods.
lesion. Thirteen of the thirty-two specimens were fixed in
buffered formalin with the shoulderjoint in the adducted
Tears of the rotator cuff typically begin in the su- position. after the skin and the deltoid muscle had been
praspinatus tendon4. The vulnerability of that tendon to removed. Following fixation for twenty-four hours. the
tearing and the resultant degeneration of this area are specimens were decalcified in formic acid. The muscles
believed to be related to the avasculanity of the tendon. of the myotendinous cuff were then divided just proxi-
to age-related changes in the collagen.and to mechanical mal to the musculotendinous junctions. The scapula was
tnauma2467’7’52222. It is commonly assumed that the separated by detachment of the glenohumeral capsule
from the glenoid, with the cuff and capsule left attached
to the humerus.
*No benefits in any form have been received or will he received
To prepare blocks of tissue. the cuff and subjacent
from a commercial part\ related directly or indirectly to the subject of
this article. Funds were received in total or partial support of the capsule were cut into strips and one-cubic-centimeter
research or clinical study presented in this article. The funding source blocks of the humerus were removed from the site of
was National Institutes of Health Basic Research Support (Irant
RR0S432.
attachment of the capsule and the various tendons to
tRead in part at the Annual Meeting of The American Academy bone (Fig. 1-A).The strips were approximately one cen-
of Orthopaedic Surgeons. Atlanta. Georgia. February 5. 1988. timeten wide and five centimeters long and included
Department of Orthopaedics. University of Washington. RK-lO.
Seattle, Washington 98195. Please address requests for reprints to Dr.
what was thought to be the tendon of each cuff muscle,
J. Clark. as well as its site of insertion on the humerus. The strips

VOL. 74.A, NO. 5. JUNE 1992 713

714 J. M. CLARK AND D. T. HARRYMAN. II

Fu;. I-A
Figs. I-A through I-l):The dissections used in the study.
Fig. I -A: Frontal section through a fixed and decalcified specimen of an adducted shoulder during preparation for microscopic examination.
The segment of the rotator cuff that is to be trimmed and embedded in paraffin is the portion between the black lines. The inset shows the
three planes in which sections of the cuff were cut: longitudinal (L), transverse (Tr). and tangential (Th). The specimen shown was cut
longitudinally.

were trimmed, embedded in paraffin. and sectioned at a of the fibers, and a horizontal plane tangential to the
thickness of eleven micrometers in one of three planes: articular surface of the humenal head (Fig. b-A). From
a longitudinal plane in the direction of the tendon fibers this group of thirteen myotendinous cuffs, one prepara-
and perpendicular to the articular surface of the humenab tion from each of the four individual tendons was 5cc-
head. a transverse plane perpendicular to the direction tioned tangentially.

FIG. I-B
Complete myotendinous cuff and capsule spread out after they were removed from the humeral head and scapula and were incised through
the axillary pouch. The anterior (left). superior (top). and posterior (right) aspects of the cuff, as seen from above, are shown before fixation.
The humeral attachments are below,and the divided muscle bellies are above.The structures shown are the subscapularis (SC),the osteotomized
coracoid process (C) with the attached coracohumeral ligament (chl), the supraspinatus (SP). the infraspinatus (IS). and the teres minor (i’M).
Note the fleshy portions of the teres minor and subscapularis that have been detached from the humerus.

l’IIE JOtJRNAL OF BONE AND JOINT SURGERY

 TENDONS. LIGAMENTS, AND CAPSULE OF THE ROTATOR CUFF 715

The remaining specimens were divided equally into sin and Masson tnichnome and were studied under a
those that were cut longitudinally and those that were microscope (model BHT2; Olympus, Tokyo, Japan) that
cut transversely. The tangential and longitudinal sections was equipped with polarizing filters. Particular attention
extended from the musculotendinous junction to the was paid to the orientations of the collagen fibers, the
bone of the humerus. The longitudinal sections were cut vascular anatomy, and degenerative changes such as calci-
both from the center and from the two edges of each fication, hyaline necrosis of collagen, and acellular areas.
of the cuff tendons that were studied. Multiple trans- Another ten of the thirty-two fresh specimens were
verse sections for histological study were cut, at three- prepared for histological study with use of the dissection
millimeter intervals, from the tendinous region of each technique that was described by Brewer. The cuff, includ-
cuff. The tissue in the interval between the subscapulanis ing the ligaments and the attached capsule, was removed
and supraspinatus tendons also was trimmed, embedded, by sharp dissection from its attachments to both the
and sectioned transversely at five-millimeter intervals, humerus and the scapula, and the resultant tube of ten-
with the biceps tendon kept in place. don, ligament, and capsule was divided longitudinally
The sections were stained with hematoxylin and eo- through the region of the axillany pouch. The tube was
then spread out flat, pinned to a slab of dental wax, and
fixed by immersion in 2 pen cent glutaraldehyde for
twenty-four hours (Figs. 1-B and 2-A). After fixation,
these flat preparations were cut into one-centimeter-
wide longitudinal strips and were processed for micro-
scopic examination in one of two ways. In seven of the
ten specimens, paraffin sections, similar to those pre-
pared from the first thirteen shoulders, were made in the
three planes and various locations that have been de-
scribed. For the other three shoulders, the entire strip was
immersed in liquid nitrogen for sixty seconds and then
was broken open longitudinally, along the muscle-ten-
don axis, with a steel chisel to direct the fracture. The
surfaces of the fracture were then critical-point-dried.
gold-coated, and studied with a scanning electron micro-
scope (model JSM 35c: JEOL, Tokyo, Japan)”'.
The remaining nine shoulders were dissected while
still fresh to study the gross relationships of the tendons,
ligaments, capsule, and overlying tissue, including the
subdeltoid bunsa. Each muscle with its attached tendon
was detached from the scapula and was meticulously
separated from the peniarticulan structures - notably,
the capsule - and then reflected laterally. leaving the
insertion ofthe muscle on the humerus intact (Fig. 1-C).
The relationships of the tendons, capsule, and overlying
tissue were recorded and photographed at each step of
the sharp dissection. The separated tendons and capsule
of the cuff were pinned out flat and prepared for light
microscopy in the manner already described (Fig. 1-D).

FIG. 1-C
Results
Photograph of the superior aspect of a specimen from a left shoul- Gross Examination
der after the myotendinous cuff muscles (SC, SP. and IS) have been
dissected off the shoulder capsule and reflected laterally. with their
The tendons of the rotator cuff were seen to fuse into
attachments to the humerus left intact. The acromion (A) and the one structure at or near their insertions into the tuber-
coracoacromial ligament were removed with the specimen. Shown are osities of the humerus (Figs. 1-B and 2-A). This fusion
the superior aspects of the capsule and of the coracohumeral ligament
(chl), which, in the intact shoulder, extends from its humeral attach-
was apparent when the two surfaces of the intact cuff
ment to the lateral border of the coracoid process (C) in the interval were exposed by removal of the overlying bursa and the
between the subscapularis and supraspinatus tendons. The posterior
underlying capsule (Figs. 1-C and 1-D). The supnaspi-
portion of this ligament. which normally crosses over the supraspi-
natus tendon, has been incised along the line indicated by the curved natus and infraspinatus tendons join about fifteen milli-
arrow and then reflected posteriorly together with the supraspinatus meters proximal to their insertions on the humerus and
tendon. A thinner layer of transversely oriented fibers (X) extends
cannot be separated by additional blunt dissection (Figs.
posteriorly from the ligament. passes deep to the supraspinatus and
infraspinatus. and terminates approximately at the border between
1-D, 3-A, 3-B, and 3-C). Although there is an interval
the infraspinatus and the teres minor (see Figs. 2-A, 2-B. and 6). between the muscular portions of the teres minor and

VOL. 74-A, NO. 5. JUNE 1992

716 J. M. CLARK AND D. T. HARRYMAN. II

FIG. 1-U

Photograph of the under (capsular) surface of the cuff after it has been dissected off the shoulder capsule and detached from its insertion
on the humerus. The tendons of the subscapularis (SC), supraspinatus (SP). infraspinatus (IS). and teres minor (TM) are fused to form a
continuous tendinous ring that normally encircles the humeral head. The scissors indicate the location of the biceps tendon where it would
normally pass over the blended insertions of the subscapularis and supraspinatus tendons in the bicipital groove. The areas enclosed within
the lines of black ink indicate where the tendons had been firmly adherent to the capsule and were separated by sharp dissection. The portions
of the tendons central to the outlined areas had been dissected off the humerus and hence were the insertions of the cuff tendons on the
tuberosities.

infnaspinatus,these muscles merge insepanablyjust pnox- infraspinatus tendons to the humerus (Fig. 4-A). This
imab to the muscubotendinous junction (Figs. 1-D and band also sends slips along the surface of the capsule into
3-A). The tenes minor and the subscapularis have mus- the interval between the subscapulanis and supraspi-
cuban insertions on the surgical neck of the humerus, natus tendons that attach to both tuberosities deep to the
which extends approximately two centimeters inferior to insertions of the cuff tendons (Figs. 1-C, 4-A, and 4-C).
their tendinous attachment onto the tuberosities. These slips that run from the conacoid process into the
The subscapulanis and supraspinatus tendons fuse to interval between the subscapubanis and supraspinatus
form a sheath that surrounds the biceps tendon at the tendons correspond to the structure referred to as the
proximal end of the bicipitab groove (Figs. 1-D, 2-A, 2-B, coracohumenab ligament”’’3.
3-A, 3-B, and 3-C). A tendinous slip extends antenolater- Additional components of the conacohumeral biga-
ally from the supraspinatus tendon to form the roof of ment are revealed when the tendons of the rotator cuff
the sheath, and the superior pant of the subscapularis are dissected from the underlying capsule of the shoulder
tendon passes under the biceps tendon tojoin with fibers and reflected laterally (Fig. 1-C) or when the cuff and
from the supraspinatus tendon to form the floor of the capsule are nesected together and their deep surfaces are
sheath. The deep portion of the sheath runs adjacent examined (Figs. 2-A and 2-B). When viewed from these
to the bone and forms a fibrocartilaginous lining for perspectives, the tendons are seen to be tightly adherent
the bicipitab groove, which extends approximately seven to the joint capsule near their insertions on the humerus,
millimeters. as previously described3. The capsule beneath the su-
The tendons of the cuff are reinforced near their praspinatus and infraspinatus tendons is thickened by a
insertions on the tuberosities of the humerus by fibrous strip of fibrous tissue, one centimeter wide, that runs
structures that are located both superficial and deep to posteriorly in a direction perpendicular to the fibers of
the tendons. The superficial aspects of the infraspinatus the tendons. The strip extends to the posterior edge of
and supraspinatus tendons are covered by a thick sheet the infnaspinatus tendon and appears to be a deep exten-
of fibrous tissue that lies directly beneath the deep layer sion of the conacohumeral ligament. which runs in an
of the subdebtoid bunsa but is not part of the bursa itself. interval between the capsule and the tendons of the cuff.
When this sheet is sharply dissected from the tendons of The coracohumeral ligament and capsule also form
the cuff, it is seen to be a fan-bike postenobatenab extension part of the roof of the sheath of the biceps tendon in the
of a broad, thick, fibrous band extending from the lateral interval between the infraspinatus and subscapulanis ten-
edge of the conacoid process oven the supraspinatus and dons (Figs. 4-A, 4-C, and 5-C). Along the lateral margin

THE JOURNAL OF BONE AND JOINT SURGERY

 TENDONS. LIGAMENTS. AND CAPSULE OF THE ROTATOR CUFF 717

FI;. 2-A
Figs. 2-A and 2-B: The deep (capsular) aspect of the rotator cuff, showing the capsule overlying the cuff.
Fig. 2-A: Photograph of the deep (articular) aspect of the cuff-capsule complex of a specimen composed of the shoulder capsule and attached
rotator cuff after the cuff-capsule complex was dissected off the humerus (top) and the scapula (bottom). The cuff muscles have also been
divided near their musculotendinous junctions (see drawing [Fig. 2-B] for explanation). A band of fibers (X) extends posteriorly as a branch
of the coracohumeral ligament into the plane between the capsule and tendons where it ends or blends with the capsule approximately at the
superior edge of the teres minor.

of that interval, the capsule blends with the extension of nohumeral ligament merges with the anterior edge of the
the supraspinatus tendon where it crosses the biceps conacohumeral ligament beneath the superior edge of
tendon and its groove. The superior and middle gleno- the subscapubanis tendon. Once all of the capsule and
humenal ligaments and the coracohumerab ligament are ligament have been meticulously nesected, the muscu-
firmly attached to the outer, non-anticular surface of the botendinous units, which are now cleanly visible, are all
joint capsule. The humeral insertion of the superior gle- that remain of the cuff.

Fii. 2-B
Drawing of the deep surface of the rotator cuff-capsule complex after it has been detached from the humerus, as shown in Figure 2-A. The
diagram in the inset is a cross section of the bicipital groove and related structures. Note the relationships of the capsule (C), subscapularis
(SC). supraspinatus (SP), infraspinatus (IS). and teres minor (TM) tendons, as well as the confluence of the supraspinatus and subscapularis
tendons proximal to their insertions on the lesser (I-L) and greater (I-G) tuberosities. In the inset, the complex sheath surrounding the biceps
tendon (B) is shown diagrammatically in cross section. The deep portion of this sheath is formed by the subscapularis tendon, and a slip (E)
from the supraspinatus tendon forms a roof over the biceps tendon. Also shown is the pericapsular band (X) seen in Figures 1-C and 2-A.

VOL. 74-A, NO. 5. JI.JNE 1992

718 J. M. CLARK AND D. T. HARRYMAN. II

FIG. 3-A
Figs. 3-A, 3-B, and 3-C: Photograph and diagrams of a dissection of the cuff tendons, showing how the tendons converge as they insert on
the humerus.
Fig. 3-A: Photograph of the lateral aspect of the proximal end of the humerus and of the outer aspects of the attached muscles of the cuff,
which have been separated from each other and dissected off the capsule, with their insertions on the humerus left intact. In the intact shoulder,
the cuff forms a solid sleeve of fibrous tissue that surrounds the proximal end of the humerus. The supraspinatus (SP) and infraspinatus (IS)
tendons blend together about 1 .5 centimeters proximal to their insertions on the humerus. and the tendon of the teres minor (TM) is inseparable
from that of the infraspinatus. Fibers of the supraspinatus tendon intermingle with those of the subscapularis tendon (SC) to form a tunnel for
the biceps tendon (B) as diagrammed in Figure 3-B.

Histological Examination that had been cut from the regions of the subscapulanis,
Sections were made in the tangential, longitudinal, supraspinatus, and infraspinatus tendons. These sections
and transverse planes from the one-centimeter strips were studied to (1) determine the orientation and extent

Fo. 3-B FIG. 3-C

Fig. 3-B: Diagram of the specimen shown in Figure 3-A, illustrating the relationships of the subscapularis (SC), biceps (B), supraspinatus
(SP), and infraspinatus (IS) tendons and of the bicipital groove (BG) at the level of the insertion of the cuff on the greater (GT) and lesser
(LT) tuberosities. The portion of the biceps tendon that is normally in the bicipital groove has been removed to expose the bed of the tendon.
This bed (small arrows) is formed by the blending of fibers from the adjacent cuff tendons. Note the lateral extension (E) of the supraspinatus
tendon. This extension normally forms the roof over the groove (see text and Figure 2-B).
Fig. 3-C: Diagrammatic representation of Figures 3-A and 3-B showing the normal interweaving of the fibers (arrows) from the subscapularis
(SC), supraspinatus (SP), and infraspinatus (IS) tendons in the region of the rotator cuff. The fibers from the subscapularis and supraspinatus
tendons form the floor of the sheath of the biceps tendon (BT) within the bicipital groove (BG).

THE JOURNAL OF BONE AND JOINT SURGERY

 TENDONS. LIGAMENTS. AND CAPSULE OF THE ROTATOR CUFF 719

of the various fiber groups within the cuff-capsule com- spinatus tendons, where they blend with the peniosteum.
plex. (2) assess the blood supply of different pants of the Large arterioles are commonly present throughout this
cuff, and (3) identify early evidence of degeneration, if layer.
any. in the various pants of the cuff-capsule complex. The Layer 2: The second layer, three to five millimeters
sections from specimens that had been pinned flat were thick, is composed of closely packed. parallel tendon
the most satisfactory, because the direction and location fibers grouped in large bundles. These bundles, one to
of the sections could be controlled more reliably; also, two millimeters in diameter, extend directly from the
because these specimens were not decalcified, the histo- supraspinatus on infraspinatus muscle belly to the hu-
logical detail was better. In cuffs that had not been menus. Fibers from this layer also form the previously
exposed to formic acid, the collagen fascicles within the described extension of the supraspinatus tendon that is
tendons were more compactly grouped, had a more uni- part of the roof oven the biceps tendon within its groove.
form crimp pattern (periodic weave pattern in normal Arterioles from the first layer cross into this second layer
tendon collagen), and stained more intensely. Altenna- between the fascicles.
tively, in the thirteen en bloc preparations, study of the Layer 3: The third layer, which is three millimeters
interface between bone and cuff was possible. Regard- thick, has a tendinous structure in which the fascicles are
less of the method of preparation, the density of the smaller than those in Layer 2 but lack a uniform onien-
tendons made it difficult to obtain transverse sections. tation. In the longitudinal sections made for scanning
electron microscopy (Fig. 5-C) and in the sections that
Supraspinatus and Infraspinatus were made parallel and perpendicular to the line of force
The sections through the supraspinatus and infraspi- of the supraspinatus and then studied by polarized light
natus tendons and the subjacent ligaments and capsule microscopy, the tendon fascicles in this layer crossed one
showed that the cuff-capsule complex is composed of five another at an angle of45 degrees. The individual fascicles
layers at this site (Figs. 5-A, 5-B, and 6). are smaller than those in Layer 2 and are not as tightly
Layer I: The most superficial layer is thin (one milli- packed. Blood vessels are also present in this layer, but
meter thick) and is composed of fibers of the conaco- they are smaller than those in Layers 1 and 2. Larger
humenal ligament, obliquely oriented with respect to the arteries that pass through the first and second layers turn
axis of each muscle (Figs. 5-A and 5-B). These fibers and run in the interval between the second and third
extend to the greater tuberosity of the humerus in the layers.
interval between the subscapulanis tendon and the supra- Layer 4: The fourth layer is composed of loose con-

FI;. 4-A FIG. 4-B FI1. 4-C

Figs. 4-A, 4-B, and 4-C: Drawings showing the relationships of the coracohumeral ligament (chl).
Fig. 4-A: Lateral aspect of the shoulder. The coracohumeral ligament (chl) extends laterally from the coracoid process (C) and covers the
biceps tendon (B) in the interval between the subscapularis (SC) and supraspinatus (SP) tendons. The attachments of the coracohumeral
ligament and of the capsule to the humerus lie deep to these tendons. A sheet of the coracohumeral ligament fans out posteriorly over the
supraspinatus tendon, extending as far as the infraspinatus (IS). and merges laterally with the periosteum of the greater tuberosity. Note the
positions ofthe acromion (A) and bicipitalgroove (BG).The inset shows a diagram ofa transverse section through the coracohumeral ligament.
the cuff tendons, and the humeral head (HH). The ligament is depicted in black: the capsule is not shown.
Fig. 4-B: The lateral aspect of the shoulder with the coracohumeral ligament removed. (The site of attachment of the ligament on the coracoid
[C] is the hatched area.) The supraspinatus (SP) and subscapularis (SC) tendons meet and interdigitate in the floor of the bicipital groove
(BG). An extension (E) of the supraspinatus tendon runs over the biceps tendon (B) and bicipital groove but is deep to the coracohumeral
ligament. A = acromion.
Fig.4-C: Diagram ofa cross section through the shoulderjoint.parallel to the surface ofthe glenoid. Note the relationships ofthe subscapularis
(SC) and biceps (B) tendons, the glenoid (G), the glenoid labrum (GL), and the supraspinatus (SP) and infraspinatus (IS) tendons. Also shown
in cross section is the coracohumeral ligament (chl). The coracohumeral ligament is superficial to the shoulder capsule (cap) and overlies the
biceps tendon (B). and its superficial and deep branches envelop the anterior part of the supraspinatus tendon.

VOL. 74-A, NO. 5. JUNE 1992

720 J. M. CLARK AND D. T. HARRYMAN. II

\J_&.’_

- . j;;.”.2 . .

(; c_;1f:.\__.

-I
1

‘.t\

FIG. 5-A
Figs. S-A through S-D: Histological sections made vertically through the rotator cuff and capsule of the shoulder in various locations.
Layer I is composed of fibers of the coracohumeral ligament obliquely oriented with respect to the axis of each muscle. Large arterioles are
commonly present throughout this layer. Layer 2 is composed of closely packed parallel tendon fibers grouped in large bundles. Arterioles
from the first layer cross into this second layer between the fascicles. Layer 3 has a tendinous structure in which the fascicles are smaller than
those in Layer 2. but they lack a uniform orientation. The individual fascicles are smaller than those in Layer 2 and are not as tightly packed
together. Blood vessels are also present in this layer but are smaller than those in Layers 1 and 2. Larger arteries that pass through the first
and second layers turn and run in the interval between the second and third layers. Layer 4 is composed of loose connective tissue in which
there are thick bands of collagen fibers. The only blood vessels in this layer are capillaries. found adjacent to the extra-articular surface of the
capsule of the shoulder. Layer S is a thin. continuous sheet of interwoven collagen fibrils which usually insert on the humerus as Sharpey fibers
within the bone.
The photomicrographs were made with a 1/4 lambda filter. The collagen fibers are blue and red, the vessels are red, and the loose areolar
tissue is blue. The use of the filter enhances the detail.
Fig. S-A: Composite photomicrograph of a vertical, longitudinal section through the supraspinatus tendon and joint capsule near the insertion
of the tendon. The open arrowhead in Layer 4 identifies one of the transverse fibers in this layer. At this location, Layer 1 is relatively thick
and the fibers in Layer 4 are attenuated (hematoxylin and eosin. x 19).
 TENDONS. LIGAMENTS. AND CAPSULE OF THE ROTATOR CUFF 721

-=
I,
I . - ‘r2.
..-‘

7’_,.l,
,L’ , a.
, . ..
, I%u_..

IMPIIIVWIP;;::;:.._:.. -I,I .-_

: ‘ T- ‘

‘- -.-- - 2 - -
J

_;_“p,..’ -
-

j__’_#{149}

. , --
-
; -‘.
, _ - - ,:___

, -

Fi;. S-B

Vertical, transverse section through the supraspinatus tendon and capsule. midway between the musculotendinous junction and insertion of
the tendon. The thick fibers of Layer 2 are cut perpendicular to their long axes. and their rounded profiles are evident. Layer 1 is thin at this
level, and the fibers in Layer 4 (arrows) are numerous.

VOL. 74-A. NO. 5. JUNE 1992

722 J. M. CLARK AND D. T. HARRYMAN. , II

_., f(.:’

1:-. -
- ._..t ‘ #{149}

FIG. 5-C
Vertical. transverse section through the biceps tendon and its sheath near the proximal opening of the hicipital groove (Masson trichrome.
x 38). The section, made after these structures had been dissected off the bone, shows the thick fibrous tissue that encircles the tendon (BT).
In this segment of the sheath, the floor is formed primarily by a slip from the subscapularis (SC) and has the appearance of fibrocartilage (fc)
where it lies close to the bone. The fibers crossing horizontally over the tendon are an extension (E) from the supraspinatus tendon.

?-‘ -

Scanning electron micrograph showing the cryofractured surface of a supraspinatus tendon after it was fractured in the vertical longitudinal
plane (x 320). The fascicles shown are in Layer 3. The fascicles form distinct layers due to variations in their orientations. The fascicles that are
not parallel to the plane of fracture project from the surface (arrows). The bar indicates 100 micrometers.

THE JOURNAL OF BONE AND JOINT SURGERY

 TENI)ONS, LIGAMENTS. AND CAPSULE OF THE ROTATOR CUFF 723

2.0 millimeters thick), continuous sheet of interwoven

collagen fibrils (Fig. 5-A). This layer, which is the capsule
of the shoulder joint, extends from the glenoid lahnum
medially to the humerus laterally where the fibnils insert
on the humerus as Sharpey fibers within the hone.
In the regions of the supraspinatus and infnaspinatus,
the tendinous segment of the cuff is thickened along the
axes of the principal muscubotendinous units. The cuff is
thinner (three to five millimeters thick) in the interval
between the supraspinatus and infraspinatus tendons.
because Layer 2, composed of the fibers that extend
directly from the two muscle bellies to the humerus. is
not present.
The grossly apparent fusion of the tendons of the
supraspinatus and infraspinatus muscles (Figs. 1-B and
I -D) is due to the extensive interdigitation of the tendon
fibers in the third layer (Figs. 3-A, 3-B, and 3-C). This
cross-over is best appreciated in the tangential sections
that were cut through the third layer in the specimens
that had been fixed while pinned flat. It is apparent that
Fii. 6
both tendons splay as they approach their insertions into
Schematic diagram of a dissection sectioned transversely at various
sites in the supraspinatus and infraspinatus tendons and capsule of the the greater tuherosity.
shoulder, comparable with that shown in Figures S-A and S-B. The
orientations of the fascicles in the numbered layers are indicated by Subscapularis
the lines on their upper surfaces. Layer I is composed of superficial
fihers that overlie the cuff tendons and extend from the coracoid The portion ofthe cuff-capsule complex in the region
process to the greater tuherosity. These fibers form an extension of of the subscapulanis tendon is composed of four to six
the coracohumeral ligament (chl). Layers 2 and 3 contain the fibers
thick bundles of collagen fibers that extend from the
of the supraspinatus (SP) and infraspinatus (IS) tendons. The fibers
in Layer 2 are oriented parallel to the axes of the supraspinatus and muscle belly to the lessen tuherosity. These bundles run
infraspinatus tendons. the fibers of Layer 3 are smaller and are parallel to one another but splay before they insert on
obliquely oriented with respect to the fibers of Layer 2. Within Layer
the lessen tuberosity. They are tightly packed in the su-
3, the fibers of the supraspinatus tendon fan out and intermingle with
the fibers of the adjacent infraspinatus and subscapularis tendons. perficial part of the tendon, hut the deeper bundles
i’his intermingling between the infraspinatus and supraspinatus crc- adjacent to the capsule are separated by loose connective
ates the variation in alignment of the fibers observed in Layer 3 and
tissue. The most proximal group of bundles passes under
shown here diagrammatically. In Layer 4. the fibers make up the deep
extension of the coracohumeral ligament (Fig. 4-A). These fibers the biceps tendon to form the floor ofthe bicipital groove
branch off the main body of the ligament at the anterior border of the together with fibers from the supraspinatus. However,
supraspinatus tendon and then course between the tendon and cap- most of the fibers that make up the floor of the groove
sule as far as the junction between the infraspinatus and supraspi-
natus. Layer S is the true joint capsule of the shoulder, which forms a are derived from the subscapulanis (Figs. 2-C and 5-C).
continuous fibrous cylinder extending from the glenoid labrum to the Within the groove, these intermingled tendinous dc-
neck of the humerus. The synovial lining of the capsule is in direct
ments became fibnocantilaginous, and cuboidal cells and
contact with the articularsurface ofthe humeral head.The orientation
of the fibers within the capsule is quite variable and is not identified metachromatic ground substance are dispensed among
in this diagram. thick collagen fascicles. In all tendon insertions into the
tuberosities, there is a fibrocartilaginous zone compara-
nective tissue in which there are thick bands of collagen ble with the one that Benjamin et al. described in the
fibers. These hands, for the most part, are located on the supraspinatus.
external (extra-articulan) surface of the capsule. How- Fibers of the superior and middle glenohumeral liga-
ever, along the anterior edge of the supnaspinatus, they ments, which can be identified histologically as separate
merge with those of the coracohumeral ligament and structures, run along the superficial, non-anticular aspect
form a ligamentous envelope that encases the anterior of the capsule. Located along the proximal and distal
part of the supraspinatus tendon (Fig. 4-B). The pre- edges of the subscapulanis tendon. these fibers pass be-
viously described fibrous band that is visible beneath the tween the tendon and the capsule on their way to insert
supraspinatus (Figs. 2-A and 2-B) is composed of fibers into the lessen tubenosity of the humerus. In these boca-
that branch off from the body of the conacohumeral tions, the configuration of the cuff is similar to that
ligament at the anterior edge of the supraspinatus ten- observed in Layer 4 in the region of the supraspinatus.
don. The only blood vessels in this layer are capillaries Fibers of the superior and middle glenohumeral liga-
found adjacent to the extra-articularsurface ofthe shoul- ments can he identified primarily by their location on the
der capsule. superficial aspect of the capsule. In sections through the
Lover 5: The fifth and deepest layer is a thin ( I .5 to capsule, from specimens in which the capsule had been

VOL.. 74.A. NO. ;. JUNE 1992

724 J. M. CE.ARK AND D. T. HARRYMAN. II

separated from the tendons of the cuff, the collagen frequent use of magnetic resonance imaging, ultrasonog-
fibers had a diverse orientation. naphy. and anthroscopy in the diagnosis of shoulder le-
sions makes it imperative that the interpretation of the
General Histological Observations findings he based on a detailed knowledge of normal
In the thirty-two shoulders. there was little micro- anatomy. It is especially important to know that tears of
scopic evidence of degeneration of tendons because only a cuff tendon may be obscured by the coracohumenal
specimens that had grossly intact myotendinous cuffs ligament on the superficial surface or by the capsule on
had been selected. Small foci ofcalcification and areas of the deep surface. Simple sutures seem to hold well in the
acellulanity were present in the tendons from about half rotator cuff, perhaps because of the heterogeneous an-
of the cuffs. Also. in the specimens from cadavena of nangement of the collagen fibers in the tissue. This study
subjects more than fifty-five years old, the cuffs were is unique because it involved normal specimens and
generally thinner, although this thinning could not be because microscopic examination and dissection were
attributed to attenuation of one or more of the specific employed together as a means of tracing individual fi-
components of the cuff. The appearance of the collagen brous elements.
fibers and the blood vessels of the tendinous portion of When tendons are interwoven and are surrounded
the cuffs were similar in all specimens and did not appear by capsule and ligaments. simple dissection with a scalpel
to be affected by age or sex. Signs of degeneration of the does not show their precise relationships. Furthermore,
cuff, such as hyaline necrosis of collagen, microscopic because the cuff curves over the humeral head. it is
tears in fibers, calcific deposits, and intimal changes in difficult to trace the various elements of the cuff in serial
arterioles, were not exclusively characteristic of one age- histological sections. In our study. the tendons were sepa-
group. In general, the diameter of the arteries in the rated from adventitial tissues in stages. Some specimens
cuff decreased as the distance from the muscubotendi- were examined grossly and microscopically while they
nous junctions increased. In the transverse sections, the were still attached to hone and then were compared with
vessels on the outer surface of the cuff followed the specimens that had been pinned flat before fixation, with
longitudinal intenvals between the heavy fiber bundles in and without the adjacent tissues in place. Histological
Layer 2 and branched into the interface between Layers studies confirmed that apparent expansions of the liga-
2 and 3. ments and tendons were in fact direct fibrous continu-
ations of these elements. Dissection of the tendons off
Discussion the bone before sectioning eliminated the need for de-
In most anatomy textbooks. the supnaspinatus. in- calcification, thus avoiding distortion of cells and colla-
fraspinatus, and teres minor tendons are shown as con- gen fibers that occur during decalcification.
tiguous but distinct structures, with the subscapulanis In contrast with other histological studies. few obvi-
separated from the others by an interval that contains the ous pathological changes were observed in the tendons
bicipital tendon and groove”’4”. Our study showed of the cuff. Uhthoff et al. studied a group of shoulders
that all four tendons of the rotator cuff fuse to form a that had partial tears or no tears of the tendons of the
common insertion on the tuberosities of the humerus. cuff and reported that fibrillation. necrosis, and so-called
Fibers from the subscapulanis anteriorly and the infraspi- microtears were common on histological examination.
natus posteriorly interdigitate with those ofthe supraspi- Similarly, Brewer noted that the tendons of the rotator
natus. The intendigitation of fibers occurs primarily in the cuff from olden subjects showed more signs of degenera-
deep layers. On gross inspection. the tendons appear to tion than those from younger ones and concluded that
have discrete insertions because the superficial fibers are the cuff deteriorates with age. Brewer included only
concentrated along lines that are parallel to the axes of three shoulders, from cadavera of people who had been
individual muscles and go directly to their insertions. The twenty, fifty, and seventy years old at the time of death.
tendinous portion of the cuff is also confluent with the so it is questionable whether the changes in the older
capsule of the shoulderjoint and with the coracohumeral cadavera could he termed representative. These histo-
and glenohumeral ligaments. Therefore, at any point, the logical abnormalities are commonly believed to result
cuff is composed of layers that can he cleanly identified from hypovascularity, particularly in the deeper layers of
by the orientations and attachments of the constituent the supraspinatus tendon’7’. We found that vessels in
fibers. the third layer of the cuff were relatively small compared
Initially, defects of the cuff seem to occur in different with those in the more superficial layers, but we saw
layers. Codman originally described deep-surface (an- no associated evidence of degeneration and concluded
ticular side) failure of fibers. Fukuda et al.”’ described that the blood supply was adequate for the metabolic
tears limited to the superficial (bursal) side: more ne- needs of the tissue. This concept is supported by the
cently. Tabata and Kida described several patterns of observation of Moseley and Goldie’ that vascular pat-
interstitial tears. Without knowledge of the normal anat- terns within the cuff do not change with age. In seventy-
omy of the fibers and of the arrangement of the layers, it two shoulders that were studied after injection. those
is difficult to explain the different lesions. The more authors found no avascular area in the supraspinatus and

IIIE JOURNAL. OF BONE AND JOINT SURGERY

 tENDONS. LIGAMENTS. AND CAPSULE OF TIlE ROTATOR (tIFF 725

concluded that “the tendinous portion is well vascular- causal events in failures of the cuff. Part of this effort is
ised and remains so throughout life.’ Although Rathbun to describe a more detailed picture of normal functional
and Macnab maintained that there is an avascular zone anatomy.
in the supraspinatus when the shoulder is adducted, they The normal rotator cuff has structural features that
also noted that the extent of avascularity was greater should improve its resistance to failure under load. The
when the tendons of the cuff were attenuated. Thus, insertion of the cuff on the tuberosities is wide and
microscopic tears of either the tendons or the capsule continuous. The areas of insertion of the individual ten-
may actually cause ischemia or necrosis by secondary dons are large because they each splay and then inter-
disruption of vessels. digitate with each other. Therefore, tension in any one
As Codman first showed. the prevalence of tears in musculotendinous unit is distributed. directly or mdi-
the rotator cuff increases with age. No specific reason has rectly. oven a wide area. Benjamin et al. have proposed
emerged from subsequent studies. Cleanly. age alone that the splayed insertions protect tendons from exces-
does not determine the condition of the tendons: we sive stresses induced by bending. DePalma et al.”’7 and
found no striking age-related differences among our Gagey et al. described the coracohumeral and gleno-
specimens. which were selected because they showed no humenab ligaments as checkreins which become taut in
gross evidence of tears. Generalized thinning of the ten- specific positions. Those authors postulated that the liga-
dons may reflect the atrophy that is pant of normal ments could therefore resist stresses that would other-
senescence and subsequent disuse. Some pathological wise fall exclusively on the tendons of the cuff. In this
observations, such as microscopic tears and calcification. study, the coracohumeral ligament appeared to reinforce
suggest that biochemical changes may alter the mechani- the supraspinatus tendon. to which it is parallel and
cal properties of the tendons. Rather than simply dis- firmly adherent. The actual function of these structural
counting this as related to aging. we should continue to features can be established only by mechanical testing of
perform research studies to delineate the sequence of normal specimens.

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Vol.. 74.A, NO. 5. JtJNE 1992