Dog Labrum

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    Comparative MedicineCopyright 2009by the American Association for Laboratory Animal Science

    Vol 59, October

    Pages 465

    In the elds of orthopedic and trauma research, animals areused frequently to model human pathologic conditions. The mostimportant criteria for the choice of the appropriate animal modelare anatomic and physiologic comparability. These fundamentalscontribute to the validity of a model, whereas missing or incom-plete knowledge may lead to results that cannot be extrapolatedto the human condition. The comparability of the biomechanical

    joint function of quadrupedal laboratory animals with that ofupright-ambulating humans is questionable. For instance, in con-trast to that in humans, the shoulder joint in quadrupedal animalshas a crucial weight-bearing function .32,35 However, the anatomi-cal structure and composition of analogous joints from humansand quadrupeds have a great deal in common. In particular, simi-larities in the alterations and lesions of the shoulder joint give riseto the possibility of strong correlation between the anatomicaldesign of the joint and the patterns of disease in these species.

    In a 1980 article,10 the GL is described as the proximal attach-ment of the joint capsule and the lateral glenohumeral ligament.In humans, the humeral head is nearly 4 times larger than theglenoid cavity, and the GL enlarges the joint surface. 30,38 In com-parison, the canine shoulder joint (scapulohumeral joint, articu-

    latio humeri) is a ball-and-socket joint. The canine humeral headis more curved in the sagittal than in the dorsal plane and articu-lates with the obviously smaller glenoid cavity of the scapula.32One study4 reported a surface relation of the glenoid cavity tohumeral head of about 1:3 in dogs, whereas another19 described

    a contact area between scapula and humerus of 47% in the ejoint and of 62% in normal weight-bearing condition.

    The human shoulder joint is highly mobile, typically allowfor abduction of 90, adduction of 20, anteversion of 90, retroversion of 30. Normal values of internal and external rtion of the humerus are each 70. However, the large rangmovement of the human shoulder is increased further by con

    bution from the scapulothoracal, sternoclavicular, and the amioclavicular joints, leading to abduction of 180 and anteexof approximately 170.37 In contrast, the range of motion ofshoulder joint in quadrupeds is limited because of the adjacmuscles and tendons, which lead the joint to function as a ro

    joint.22 Extension and flexion in carnivores typically is grethan 120, with external rotation of up to 45, but internal rotais usually less than 35.41 In a recent study8 angles for abductiodogs without history of shoulder instability were between 3133, according to goniometric measurements and image analy

    The human shoulder has a wide joint capsule with resefolds, which elapse during certain movements. The biceps tdon is covered by a tendon sheath and situated in the supeportion of the joint cavity.30 In all companion animals, the j

    capsule of the shoulder is spacious. In carnivores in particuthe joint space bulges into 2 cranial and an expanded caudolatportion.22 The proximal attachment of the capsule is the GL,distal insertion is located only a few millimeters distal to the jsurface of the humeral head, extending into the periosteum ofhumeral neck.11 In carnivores, the proximal part of the tendonthe biceps muscle is surrounded by the joint capsule to the intubercular groove.

    In humans, ligaments strengthen the anterior wall of shoulder joint capsule in the superior, medial, and inferior ditions.13,17,18,38 In dogs these structures run mainly medially

    The Anatomy of the Glenoid Labrum: AComparison between Human and Dog

    Martin Sager,1,* Monika Herten,2 Stefanie Ruchay,2 Josef Assheuer,3 Martin Kramer,4 and Marcus Jger2

    The anatomy of the glenohumeral joint in humans is characterized by static and dynamic stabilizing structures. In particularglenoid labrum (GL), the proximal attachment of the joint capsule and the lateral glenohumeral ligament, is an important passstabilizer in the human shoulder. Although canine animal models are used frequently to investigate the complex biomechanicthe shoulder, few data regarding the microstructure of the canine GL are available. In this study, the anatomy of the canine GL related structures (n = 20) was investigated and compared with the human anatomic situation (n = 36). In both human and beajoints, the GL consisted of 3 zonesthe transition zone, shifting zone, and meniscoid fold, but not all 3 zones were present injoint segments from canine joints. In particular the peripheral parts of the GL showed rich vascularization in both species. height and width of the GL in the histologic specimens indicated that the GL is of less importance as a passive stabilizer in dAdditional differences between the human and canine CL include the joint ligaments, tendons of the shoulder joint, and lack

    rotator cuff. The structural and biomechanical characteristics of the joints of quadrupedal animals raise the question of theirpropriateness for shoulder research.

    Received: 27 Sep 2008. Revision requested: 25 Nov 2008. Accepted: 25 Jan 2009.1Central Animal Research Facility and 2Orthopaedic Department, Medical School of the Heinrich-Heine-University, Dsseldorf. Germany; 3Institute for Magnetic ResonanceImaging, Kln, Germany; 4Small Animal Clinic, Veterinary School of the Justus-Liebig-University, Giessen, Germany.

    *Corresponding author. Email: [email protected]

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    taminase II as a marker of tissue vascularization.12 Tissue sectwere deparafnized in xylol, dehydrated through an ethanolries, and rehydrated in PBS. Antigen unmasking was perform

    by incubating the slides for 15 min in trypsin (0.05% in PBS; PLaboratories, Pasching, Austria) at 37 C. After slides were rinwith PBS, the activity of endogenous peroxidase was quencwith 0.9% hydrogen peroxide in PBS for 10 min at room tempture, specimens were washed, and nonspecic binding sites w

    blocked by incubation in blocking solution (DakoCytomatHamburg, Germany) for 30 min. Primary antibodies inclumouse monoclonal antibodies to collagen I and II (1:100 dilutChemicon, Hofheim, Germany) and transglutaminase II (1dilution, Acris Antibodies GmbH, Hiddenhausen, Germany),

    bit polyclonal antibody to collagen III (1:100 dilution, Chemicand mouse IgG1 and rabbit IgG (as negative controls) and wapplied to tissue sections in a humidied chamber and incubaovernight at 8 C. Slides were washed in PBS and incubated wsecondary biotinylated antimouse antibody (1:50 dilution, Dafor 60 min at room temperature. Slides again were washePBS, and antibodyantigen complexes were visualized by usa streptavidinperoxidase solution (1:250 dilution, Dako) 3-amino-9-ethylcarbazole as the chromogen (Dako). Slides wcounterstained with hemalaun (Merck, Darmstadt, Germany

    Histomorphometric analysis. Histomorphometrical analyand microscopic observations were performed by a singleperienced investigator blinded to the specic experimental cditions. For image acquisition, a color camera (Color ViewOlympus, Hamburg, Germany) was mounted on a binocular lmicroscope (Olympus BX50, Olympus). Digital images (origmagnication, 200) were evaluated by using a software prog(analySIS FIVE docu, Soft Imaging System, Mnster, German

    For measuring the size of the labrum glenoidale, the calciarea (Figure 2) was used as a reference. The height of this area determined as the distance at a right angle between the refereline to the peripheral limit of the articular cartilage; width w

    obtained by taking the distance between the rst centrally visdemasked bers to the outermost peripheral point of the labrand depth was the distance from the most proximal bers ofinsertion of the labrum in a right angle to the reference line.

    ResultsIn the following description of the labrum glenoidale, dif

    ences in nomenclature between humans and dogs must be csidered. In the present study, the origin of the biceps tendon wtaken as the reference point for the characterization of segmeThe terms used with the incisura in medial or anterior positare dened in Figure 3.

    Macroscopic description of the human shoulder joint. In 35vestigated human specimens, the labrum did not encircle thetire glenoid, and marked differences in size, shape, structure attachment were present (Figure 1); 1 specimen could be evated because of beginning of autolytic changes. In all specimethe long biceps tendon was present in the superior segment,in 34 of 35 joints, it could not be distinguished from the labrand formed a labrumtendon complex. This complex seemto be relocatable and xed in the proximal part at the glencreating a recess (a bulge in the joint capsule) toward the glenThe bers of the biceps tendon were connected to the labrumdifferent ways; in most (83%) cases, the tendon was ancho

    by 2 reins, which led to the posterior and anterior labrum. In

    Histologic preparation. The specimens were xed in 4% neutralbuffered formalin. After removal of soft tissue (cutis, subcutane-ous fat, muscles, nerves, vessels), the joint capsule was incisedcircularly from the middle to proximal part. The anatomy of allshoulder joints was analyzed macroscopically by measurementof distinct parameters (longitudinal and transverse diameter) anddocumented by photography (Figure 1). For histologic prepara-tion, the joints were decalcied in 10% buffered EDTA and em-

    bedded in paraffin or methacrylate (Technovit 7100, HeraeusKulzer, Weinheim, Germany). Each joint socket was divided into7 segments, with the proximal biceps tendon insertion serving asorientation at 12:00 and progressing clockwise for right shoulder

    joints but mirror-inverted for left joints. Segments were cut into3-m circular slices by using a rotating microtome (Autocut 2055,ReichardtJung AG, Heidelberg, Germany). The number of slicesper segment was 54 for human joints and 6 for canine.

    Histochemical staining. Slices were stained with either hema-toxylin and eosin or azan according to Heidenhain15 or, for dis-tinction between reticular collagenous soft tissue and muscle,according to Richardson.26 Both the Heidenhain and Richardsonstaining methods were suitable for polarization microscopy.

    Immunohistochemistry.Canine joints were investigated immu-nohistochemically for collagen types I, II, and III and for transglu-

    Figure 2. Histomorphometric analysis of the canine GL, lateral segment(segment VI). The line of reference is the calcication zone. The height

    was determined by the distance starting at a right angle to the referenceline to the limit of the articular cartilage. The width was measured atthe middle of this distance at a right angle. The distance from the pointof the most proximal bers insertion of the labrum measured perpen-dicular to the reference line was dened as the depth of the labrum. Bar,100 m.

    Figure 3. Nomenclature regarding the right shoulder joint.

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    At the edge of the glenoid cavity of the scapula, the labrum (ifpresent) diverged dramatically in size, shape, and attachmentamong segments. In some segments, the joint lips could not beseparated macroscopically because there was no distinct delimi-tation between the adjacent joint capsule and the glenohumeraltendons.

    The rst segment contained a gap between the biceps tendonand the cranial pole of the glenoid cavity; this gap was lled witha gelatinous-like tissue. This sliding zone was prominent in 11of the 20 investigated joints, protruding above the hyaline carti-lage and attening toward the rim of the biceps tendon. In 8 of 20

    joints, the sliding zone was narrow, presenting a cavity betweenthe cranial glenoid rim and the biceps tendon. In the remaining

    joint, this cavity was enlarged but lacked any soft transitionaltissue.

    The craniomedial part of the joint (segment II) seemed to berather exible and not rmly connected to the glenoid. The me-dial glenohumeral tendon predominated, and a labrum struc-ture could not be dened. Some cavities (recessus subscapularis)could be detected.

    remaining 17% of specimens, the tendon seemed to be anchoredonly posteriosuperiorly, without the additional anterior rein. Ananteriosuperior sublabral recess was present in 50% of specimens,due to partial or complete ablation of the labrum from the gle-noid. The structure of the human labrum was weaker posteriorlythan inferiorly, where it was characterized by recesses betweenthe glenoid and labrum mainly in the superior and anteriosupe-rior regions. Inferiorly and posteriorly, the labrum predominantlywas xed by the glenoid, but numerous bulges in the joint cap-sule were present between the glenohumeral ligaments (Figure 4).

    Macroscopic description of the canine shoulder joint. The bicepstendon served as a central orientation point during preparationand macroscopic description and was used for the arrangementof the glenoid cavity in cranial direction (Figure 1). The origin ofthe tendon from the supraglenoid tubercle could not be detectedmacroscopically. Although the biceps tendon was adjacent to cap-sular tissue and surrounded by lateral rims at the side oppositethe glenoid, it was uncovered near the articular cavity. Only theproximal rim was covered by a sliding zone and separated fromthe cranial pole of the glenoid cavity (Figure 1).

    Figure 4. Summary of ndings from the current study and literature regarding differences between the glenohumeral ligaments of humans6,13,17,18,38 anddogs.10,29

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    morphologically. In 75% of all investigated cases, the supeportion comprised a labrumbiceps complex whereas in the

    maining cases both structures could be differentiated cle(Figure 7). The anchorage zone could be detected in only 2 ojoints. In addition, a deep sublabral recess, a bundle of circubers with bony attachment through Sharpey bers, and a pnounced meniscoid fold dominated. These ndings varied dmatically from those in the rst segment of the dogs, in whthe anchorage zone was well demarcated and the attachmenthe glenoid was nearby. The anchorage zone in canine joints marked by a substance resembling cartilage bers, in whichtexture of the collagen bers differed from the parallel pattof the biceps tendon and displayed marked crossing of com

    The third segment was unique in that the border of the cartilagesurface facing the labrum did not seem to be circumscribed pre-cisely but rather had retractions resembling incisures. The labrumextended into the joint space like a meniscoid fold and could bedetached from the glenoid by using forceps (Figure 1). The extentof the overlapping zones varied among the investigated jointsand seemed to be frayed in some areas of some joints.

    The 2 caudal segments (segments IV and V) were very homog-enous in appearance. There was a smooth transition between thehyaline edge of the cavity and joint capsule, and the connectionseemed to be xed. The capsule wall was very thin, especiallycaudolaterally, and translucent at the adjacent muscles.

    In the sixth segment, the labrum was easily discernable andappeared to have a tough, rm structure that was attached to thehyaline joint area. The labrum arose distinctly from the cartilagesurface and deepened the cavity, which was only minimally de-veloped in this area (Figure 1).

    In the seventh segment, the lateral glenohumeral ligamentwas inserted craniolaterally, reaching from caudal and incliningtoward the labrum. Both structures united in a V cranially in arough strand that precluded macroscopic distinction betweenlabrum and ligament (Figure 1). The joint socket was enlargedand deepened.

    Size and form of the glenoid cavity. The longitudinal diameterof the glenoid cavity (mean 1 SD) was 2.0 0.18 cm in dogs and3.2 0.41 cm in humans, and the transverse diameter at the nar-rowest point (at the incisura glenoidalis) was 0.6 0.1 cm in dogsand 2.4 0.36 cm in humans. The area of the articulating joint sur-face in dog was determined by using the means of the transversediameters at the maximal and narrowest points and assuming anellipsoidal joint surface. For human joints, the areas were 1.6 cm 2for the glenoid cavity and 4.0 cm2 for the caput humeri, resultingin a ratio of 1:2.5. When dened according to Anetzberger,2 thecanine joint cavity (Figure 2) was droplike (type Ia) in shape in12 dogs (60%), lacked incision (type 1b) in 2 (10%), and was oval

    (type II) in 6 (30%).Microscopic investigation of human and canine joints. The la-

    brum glenoidale was divided among as many as 3 segments (Fig-ure 5). In the rst segment, the transition zone, the labrum wasconnected to the hyaline joint cartilage (Figures 3 and 5). Thiszone consisted of filamentous cartilage, in which the collagenbers were readily apparent due to their low amount of matrix(in contrast to hyaline cartilage). In cross section, the bers dis-played a lattice structure. In human joints, this zone was pres-ent predominately in the anterior and anteriosuperior segments,whereas in dogs it spanned the cranial, craniomedial, and cranio-lateral segments.

    The second segment consisted of collagen bers encircling theglenoid (Figure 5). This zone often was connected with and dif-

    cult to differentiate from the rst segment. In addition, the GL inthe second segment often was associated at the bone with Sharp-ey bers, which interlaced in an obtuse angle with subchondral

    bone.The third segment was created by a meniscoid fold (Figure 5),

    consisting predominantly of well-vascularized synovial tissue(Figure 6), which was connected with collagen bers to the re-sidual part of the labrum.

    Comparison of joint segments between humans and dogs.Seg-ment I. In contrast to the other segments, the superior and an-teriosuperior segments of the human joint were highly variable

    Figure 5. Differentiation of the human GL into 3 characteristic zonesman anterosuperior segment (segment II). Left, hyaline cartilage (C

    bottom, subchondral bone (SCB); middle, transition zone (TZ); topbrous zone with circular bers (CF). Right, meniscoid fold (MF). Ty

    variation: folding grid. All 3 zones in this segment occurred in 44.4%specimens. Polarization microscopy; magnication, 12.5.

    Figure 6. Medial segment (segment III) of the canine GL, visualizaof vascularization. CA, articular cartilage; CF, brous zone with circbers; C-MGHL-C, complex of joint capsule and medial glenohumligament; MF, meniscoid fold. Immunohistochemistry for transglutnase II; bar, 200 m.

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    labrum occurred in 47.2% of specimens and was characterizedby a big sublabral recess (the sublabral hole), and the anchoragezone and the bundle of circular bers were missing (Figure 10).A minor, third type of labrum in humans (8.4%) was described as

    miscellaneous.The situation in dogs was similar to the rst type of labrum inhumans, because the transition zone and bundle of circular -

    bers were present in parallel but without any meniscoid fold. Theappearance of a glenohumeral ligament arising distinctly fromother structures was typical in the second segment in dogs. Thisligament seemed to be attached by fatty mesentery-like tissueand was placed like a tongue between the glenoid and the nalligament of the subscapular muscle, separating the subscapularrecess into 2 parts (Figure 11). The medial glenohumeral tendonof dogs consisted mostly of parallel collagen bers, which were

    nent strands. Immunohistochemical staining for collagen II waspositive in this area (Figure 9). The anchorage zone did not exceedthe hyaline cartilage layer, in contrast to the next higher zone,which overtopped the cartilage level and was macroscopicallyidentical to the sliding zone (Figures 8 and 9). This zone was vir-tually triangular in shape and was located between the labrumand the biceps tendon, with the unattached leg extended into the

    joint space. Immunohistochemical staining for the endothelialcell marker transglutaminase II revealed that the anchorage zonelacked blood vessels, unlike the sliding zone which displayed nu-merous positively stained vessels at the rim from the joint spaceto the biceps tendon (Figure 8).

    Segment II. In the second segment of the human joint, 2 pre-dominant types of labrum could be identied. The rst type (gridtype) was present in 44.4% of specimens and was located nextto the transition zone and comprised a prominent bundle of cir-cular fibers and meniscoid fold (Figure 5). The second type of

    Figure 7. Human labrumbiceps tendon complex, superior segment(segment I). Left, hyaline cartilage (CA); right, labrumbiceps tendoncomplex (LBTC) with a visible meniscoid fold (MF). Polarization micro-scopy; magnication, 12.5.

    Figure 8. Overview of the cranial segment (segment I) of the canineGL. CA, articular cartilage; BT, biceps tendon; JC, joint capsule; SCB,subchondral bone; TZ, transition zone. Hematoxylin and eosin stain;

    bar, 2 mm.

    Figure 9. Transition zone of the canine GL and origin of the biceps ten-don, cranial segment (segment I). Immunohistochemistry for collagentype II. Inset, vascularization in the shifting zone (SZ). Immunohisto-chemistry for transglutaminase II. BT, biceps tendon; CA, articular carti-lage; SB, subchondral bone; TZ, transition zone. Bar, 200 m.

    Figure 10. Anterosuperior segment (segment II) of the human GL. Left,hyaline cartilage (CA). Right, circular bers in the labruminferiorglenohumeral ligamentcomplex (L-IGHL-C). This variation (type II),with its large sublabral recess (SL-REC; also known as a sublabral hole)and lack of a transition zone, accounted for 47.2% of specimens. Polari-zation microscopy; magnication, 12.5.

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    prominent in the third segment of dogs and declined caudaSimilarly in humans, this meniscoid fold was present in theterior segment in 70% of all specimens (Figure 13). The humlabrum was very wide in the third and fourth segments, avering 5.1 and 4.5 mm, respectively.

    Segments IV and V. In the fourth segment in dogs, the bro

    tendon-like muscular origin of the caput longum of the tricbrachii muscle predominated. In the caudal segments, the GL similar characteristics to segment III. The circular ber bundwere proximal to the calcification area but did not exceedlevel of the hyaline cartilage layer (Figure 14). The collagen bprotruded into a bulged fold but had lost their triangular shand proceeded only slightly convexly into the joint space. Infourth segment, the joint wall still displayed signs of the cauleg of the medial glenohumeral ligament but did not show

    branching caudolaterally.

    aligned into bundles displaying an oval shape in cross-section(Figure 11). In the craniomedial segment, the canine labrum had a2-layered assembly: the rst part consisted of an anchorage zonecharacterized by positive staining for collagen II (Figure 12) anda grid-like alignment of the bers and the second part compris-ing of circular arranged collagen bers, laterally overlying theanchorage zone.

    Segment III. The medial segment of the canine GL displayedcircular collagen bers without an anchorage area and crossingcollagen ber bundles. Some collagen bers protruded from thefiber bundle and proceeded from lateral to mediosuperficial,creating the base of the third zone, which presented a triangularshape in cross-section and extending into the joint space (Figure 6).Immunohistochemical staining revealed that this structure wasexceedingly vascularized. This so-called meniscoid fold was most

    Figure 11. Craniomedial segment (segment II) of the canine GL. CA,articular cartilage; MGHL, medial glenohumeral ligament; REC, recess;SCB, subchondral bone; TZ, transition zone. Hematoxylin and eosinstain; bar, 1 mm.

    Figure 12. Craniomedial segment (segment II) of the canine GL. CA,articular cartilage; CF, brous zone with circular bers (CF); MGHL,medial glenohumeral ligament; REC, recess; SCB, subchondral bone;TZ, transition zone. Immunohistochemistry for collagen type II; bar, 200m.

    Figure 13. Anterior segment (segment III) of the human GL. Left, hline cartilage (CA); center, transition zone (TZ) and meniscoid fold (Mright, brous zone with circular bers (CF). Polarization microscmagnication, 12.5.

    Figure 14. Caudomedial segment (segment IV) of the canine GL. Brly based origin of the triceps muscle. CA, articular cartilage; CF, brzone with circular bers; JC, joint capsule. Hematoxylin and eosin s

    bar, 2 mm.

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    In dogs, craniolaterally in seventh segment the circular berbundle disappeared into the background and was replaced bya strong anchorage zone. The fibers were grid-like and micro-scopically showed the presence of chondrocytes (Figure 15). Thelabrum was closely interwoven with the structures of the lateralglenohumeral ligament (Figure 15).

    The maximal and minimal widths of the GL did not occur inthe same segments in human and dogs (Figure 16). In humanshoulders, the highest values were found in segments I and IIIwhereas the maximal widths in dogs were located in segmentsII and IV. The lowest width for humans was in segment VIIand for dogs in segments III and IV. The height of the labrum(Figure 17) in humans varied less between segments than did thewidth. In humans, this measure corresponded to the height of thecircular ber bundle, which in all segments was more developedin this direction than was the transition zone. In dogs, the maxi-mal height of the labrum occurred in segment VI. Pertaining tothese measurements, the xation procedure led to shrinkage inall specimens.

    Vascular supply In dogs, the transglutaminase method revealedpronounced vascularization of the shifting zone, particularly atthe free edge of the joint space, at the biceps tendon of the cranialsegment, and in the medial segment in the meniscoid fold.

    In humans, both inferior segments had the typical assembly ofthe labrum but with a less-developed transition zone without re-cess formation and only very slightly developed meniscoid folds.The inferior glenohumeral ligament (IGHL) inserted inferiorly atthe prominent circular ber bundle.

    Segments VI and VII. In dog, the caudolateral part of the glenoidwas indicated by a pronounced GL. The circular ber bundlesincreased in height and width and were protruding from the hya-line cartilage surface. The extension above the calcication zonewas greater than the depth of the subchondral anchorage. Thecapsule wall was pervaded by numerous crossing ber bundles,which continued cranial toward the lateral glenohumeral liga-ment. The strength of the ligament and its entire integration intothe joint capsule contributed to a bulky and laterally overhangingappearance.

    The labrum was only weakly developed in the sixth and theseventh segment in humans. Superiorly, the circular ber bundlewas superimposed by the intruding bers of the labrumbicepstendon complex, and the bony base of the labrum was expanded.Between the labrum and glenoid, a recess frequently was foundin the posterior and posteriosuperior segment in humans, butsmall meniscoid folds were only occasionally present.

    Figure 15. Craniolateral segment (segment VII) of the canine GL. Left, the transition zone (TZ) in the area of insertion of joint capsule and lateral gleno-humeral ligament is shown. CA, articular cartilage; C-LGHL-C, capsuleligament complex; SCB, subchondral bone. Bar, 1 mm. Right, Use of increased

    magnication (insets A and B) enabled visualization of demasked bers. Hematoxylin and eosin stain; bar, 100 m (inset A), 20 m (inset B).

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    types of cells, including the endothelium of arteries, veins, lymph vessels. This enzyme also is found in the mesotheliumthe pleura, pericardium, and peritoneum. The presence of traglutaminase in the vascular system has been used for the detion of microvessels during healing processes.7

    In dogs, a rich vascular supply was revealed in the shiftzone, particularly at the free edge adjacent the joint space, at

    biceps tendon of the cranial segment, and in medial segmenthe meniscoid fold. These ndings coincide with descriptionshuman joints,16 in which blood vessels were located between bdles of highly brous avascular connective tissue in the transizone. Other authors9 have described a vascular supply only ofperipheral zone of the labrum; that study revealed scant valarization in the superior and anteriosuperior segments but vascularization in the posteriosuperior and inferior segmeThe possibility of vessels entering the labrum from subchon

    bone was excluded. Age may alter the degree of vascularizaof the GL, in that older subjects showed less vascularization oflabrum in one study.25

    Size and shape of articulation surfaces. In the present stuthe ratio of the joint surface of the canine glenoid cavity to of the humeral head was approximately 1:2.5. In comparison,ratio in humans is approximately 1:4,30,38 indicating high incgruence in this regard between the shoulders of medium-sicanines (that is, beagles) and humans. That is, the surface aof the human glenoid is 4 to 5 times greater than that of beadogs. Further, we were able to conrm 3 known variations inshape of the canine glenoid cavityin humans, these variatihave been described as droplike in shape with incision (typeor without incision (type Ib) and oval (type II).2 The relative inence of these various shapes of the glenoid cavity on the stabof the shoulder joint or xation of the GL is unknown. 38

    Support structures. In regard to the positions of the shoulligaments, the human superior and medial glenohumeral lments were equivalent in position to the 2-component canine

    dial glenohumeral ligament. The inferior glenohumeral ligamwhich was not found in dogs, strengthened the entire caudal csule wall, which was scarcely developed in dogs. In contrast,lateral wall of the canine joint was strengthened primarily bylateral glenohumeral ligament, whereas only a thin capsulpresent in the posterior segment of human shoulders.13 Similto the xation of the canine lateral glenohumeral ligament,human glenohumeral ligaments spread into the GL and onla few cases were accompanied by additional bony xation.addition, the origin of the joint capsule at the scapula was vable in humans, depending on the insertions of the ligaments

    biceps tendon.The shoulder lacks collateral ligaments outside of the jo

    this function is attributed to tendons that work as contrac

    ligaments.22,42 In this regard, the tendon of the subscapularis mcle was present medially, and those of the infraspinatus muand a lateral portion of the supraspinatus muscle were localaterally.32 These muscles form the rotator cuff in humans have great importance as active stabilization mechanisms ofcanine joint.4,5 Additional muscles supporting the stability ofhuman joint include the teres major, teres minor, biceps, tricecoracobrachialis, and deltoideus muscles.10 For dogs, these mcles were not only involved in extension and exion but alslimited rotation, adduction, and abduction of the leg22.

    DiscussionDevelopment of the labrum in the different segments. Com-

    paring the characteristic ndings of the human and canine GLrevealed that this anatomic structure consisted in general of 3different zones in both species, but with distinct differences in thesegments of these zones. The transition zone was identied in allsegments of the human glenoid but could only be distinguishedin the cranial, craniomedial, and craniolateral segments of thecanine labrum. The second zone with its characteristic circularbers was present in all human segments but missing from thecranial and craniolateral canine segments. The third zone, the me-niscoid fold, was present in dogs at an incidence of 70%, mostlyin the medial segment. The incidence for the human joints was100% in the medial and 83% in the superior segment, whereasthis zone was not found in the corresponding canine cranial seg-ment. In this segment, human specimens had a superior labrum

    biceps tendon complex, in which the biceps tendon was woveninto the posterior and interior glenoid in different patterns andhad an osseous origin at the supraglenoid tubercle.6,14,38 Other

    authors40 have described 4 types of insertion in humans, whichwere very often accompanied by a recess within the superiorarea. Within the breed limits of our study, the origin of the bicepstendon of dogs showed predominantly an osseous xation withonly sporadic anchorage bers into the GL. This situation couldcorrelate with the reduced range of movement of the roller jointin dogs.8,22,37,41

    Vascular supply. We assessed vascularization of the canine andhuman GL by use of primary mouse monoclonal antibodies totransglutaminase II. Immunohistochemical studies in guineapigs12 revealed that transglutaminase is expressed by various

    Figure 16. Mean width (mm) above the calcication zone of segments Ithrough VII of the human (h) and canine (c) GL.

    Figure 17. Mean height (mm) above the calcication zone of segments Ithrough VII of the human (h) and canine (c) GL.

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    Biomechanical aspects. One critical feature that must be con-sidered is that the shoulder joint of quadrupedal animals has aweight-bearing function unlike that of humans.35 In this regard,instabilities that would otherwise be minor in the human shoul-der likely would have a major inuence on gait in dogs.33 Thepredominant function of locomotion of the front limb of dogsis associated with limited range of motion in favor of increased

    joint stability.Experiments involving canine models. Several studies have at-

    tempted to identify appropriate animal models to answer variousquestions regarding the human shoulder. Immobilized shoul-der joints of dogs were unsuccessful in providing insight intothe pathogenesis of the stiffness of the human joint.31 In anotherstudy,35 33 animal species (including the dog) were evaluated toidentify a model for rotator cuff disease in humans. The rotatorcuff forms a caplike roof and is assembled from 4 muscles (thesupraspinatus, infraspinatus, subscapularis, and teres minor) andtheir associated tendons extending from the scapula to the greaterand lesser tubercle.37 Apart from some primate species, whichmay be less desirable for experimental purposes for various rea-sons, only the anatomic structure of laboratory rats showed suf-cient analogy to the human shoulder joint: the skeletal structureof rats shows an almost identical development of acromion andclavicula which, together with the acromioclavicular ligament andcoracoids, formed a closed arch over the underlying supraspina-tus tendon.35 However, the dog is used in research addressing the

    blood supply of the human rotator cuff.21 According to an ultra-sonographic description of the shoulder anatomy,20 the canineshoulder joint lacks a true rotator cuff; therefore comparison ofthese structures between humans and dogs is not possible.

    In using the GL of the dog as a model for humans, macroscopicand microscopic differences of this component of the shouldermust be considered together with species-specic differences inthe overall structure of the shoulder joint. Any of these differ-ences could mitigate the utility of the model and the validity ofsubsequent comparison.

    AcknowledgmentThe authors would like to thank the research group of U Knig, T

    Barthel, F Gohlke, and JF Lhr (Bayerische Julius Maximilians,Universitt Wrzburg, Germany) for providing us the excellentspecimens of human glenoid labrum (Figures 1, 5, 7, 10, and 13).

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