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he mode of destruction in shoulders with rheumatoidrthritis based on radiographic findings

iroyuki Tanaka, MD,a Kazuomi Sugamoto, MD, PhD,b Wataru Sahara, MD,b Takeshi Ono, MD,b

etsuya Tomita, MD, PhD,b Jun Hashimoto, MD, PhD,b and Hideki Yoshikawa, MD, PhD,b Osaka, Japan

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he objective of the present study was to elucidate theode of rheumatoid arthritis shoulder destruction. The

tudy included 402 shoulders from 201 patients withheumatoid arthritis. Plain radiographic findings weresed to assess and statistically analyze the severity of thelenohumeral joint destruction (GHD) and greater tuber-sity destruction (GTD).For both GHD and GTD scores, atatistically significant correlation was found between theeft and right sides and also between the GHD and GTDcores within the same shoulder. However, 97 shouldersf 67 patients showed a heterogeneous pattern. An inter-sting finding was that no patients showed a combina-ion of the GHD type plus the GTD type. Shoulders withheumatoid arthritis showed statistically significant sym-etry and uniform destruction. Even if they showed heter-geneous destruction, there were no cases of a differentattern of heterogeneity on the opposite side. The modef destruction was not always definite, however. (J Shoul-er Elbow Surg 2007;16:539-543.)

oint destruction due to rheumatoid arthritis (RA) isell documented, and the shoulder is one of the

oints most often affected.3,11,12,13,18,19 Joint destruc-ion caused by RA is generally bilateral and symmet-ical13,19,8,4,21; however, we have demonstrated thatoint destruction is unilateral in some patients, with aarked left versus right difference in the severity ofestruction. In addition, the homogeneity of destruc-

ion within the same joint can vary.We focused on 2 important areas of the proximal

umerus, the joint surface and the greater tuberosity,ecause destruction of these areas seemed to beelated to clinical symptoms such as joint congruity orotator cuff function. We also wanted to determine therequency and tendency toward heterogeneous or

rom the aDepartment of Orthopedics, Kawasaki Hospital; andbDepartment of Orthopedics, Osaka University Hospital.

eprint requests: Hiroyuki Tanaka, MD, Department of Orthope-dics, Kawasaki Hospital, Sawa 485-1-502, Kaizuka-shi, Osaka,Japan 597-0062 (E-mail: hiro145@rinku.zaq.ne.jp).opyright © 2007 by Journal of Shoulder and Elbow SurgeryBoard of Trustees.

058-2746/2007/$32.00

oi:10.1016/j.jse.2006.11.011

symmetric destruction of the RA shoulder. We, there-ore, initiated a large-scale radiographic study withhe objective of elucidating the mode of RA shoulderoint bone destruction.

ATERIALS AND METHODS

atientsBetween 2001 and 2003, 233 patients visited the De-

artment of Orthopaedics at the Osaka University Hospital.hey satisfied the diagnostic criteria established by themerican College of Rheumatology1 and underwent bilat-ral plain radiography. Of these 233 patients, 32 werexcluded: 5 patients who had undergone joint replacementn both shoulders, 7 who had undergone joint replacementn 1 shoulder, and 20 for whom definitive radiographicndings could not be obtained for 1 or both sides. Conse-uently, 402 shoulders from 201 patients (26 men, 175omen) were included in this study. Their average age was7.0 years (range, 23-84 years).

lain radiographyJoint destruction was assessed from anteroposterior ra-

iographs of the left and right shoulder joints taken at thenal examination. The radiographs were taken by placingach patient in the supine position, tilting the contralateralide 20° relative to the direction of the x-ray tube, position-ng the upper arm into lateral rotation with the palm facingpward, and then taking radiographs perpendicular to thelenohumeral joint.

ssessment of plain radiographsLarsen’s classification system10 was used to classify gle-

ohumeral joint destruction (GHD) into 6 grades (grades-5). The severity of greater tuberosity destruction (GTD)

bone erosion and radiolucency) was assessed by the depthrom the top of the greater tuberosity to the bottom of thesseous lesion and was classified into 3 grades: as milddepth, �5 mm), moderate (:depth, 5-10 mm); and severedepth, �10 mm; see Figure 1).

attern of destructionWe classified the pattern of destruction within a shoulder

nto 4 types at the point of the most severely affected areas follows:

1. GHD type (heterogeneous osseous lesion in a se-

verely eroded glenohumeral joint): GHD grade 4 or

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more, GTD grade mild or moderate (see Figures 2Aand B, 3A)

2. GTD type (heterogeneous osseous lesion in a se-verely eroded greater tuberosity): GHD grade 3 orless, GTD grade severe (Figure 4B)

3. Uniformly mild: GHD grade 3 or less, GTD grademild or moderate (Figures 3B and 4A)

4. Uniformly severe: GHD grade 4 or more, GTDgrade severe

e classified the GHD and GTD types as heterogeneousestruction.

ata analysisPaired comparisons between men and women were

igure 1 The destruction of the greater tuberosity was assessed byts depth from the top of the greater tuberosity to the bottom of thesseous lesion. The depth was classified into three grades: milddark gray) was less than 5 mm; moderate (medium gray) wasetween 5 and 10 mm; and severe (light gray) was 10 mm orore.

igure 2 A and B, Radiographs of the rheumatoid shoulders of a1-year-old woman show bilateral grade 5 glenohumeral jointestruction (GHD), and a mild grade of greater tuberosity destruc-

ion. Both shoulders showed extensive erosive destruction of artic-lar surface, both osseous lesions of the greater tuberosity wereild. The destruction pattern was symmetric GHD type. The destruc-

ion was symmetrical.

erformed with the Mann-Whitney U test for GTD and GHD c

cores. The correlation between age and osseous destruc-ion, between individual left and right sides, and betweenhe GHD and GTD scores within the same shoulder wereade with Spearman rank correlation coefficients.

ESULTSlassification of glenohumeral destruction and greater

uberosity destruction

Glenohumeral destruction. According to a. Larsen’s

igure 3 Radiographs of the rheumatoid shoulders of a 62-year-ld woman. A, The right shoulder was at grade 5, and had mildTD. It showed extensive osseous lesion in the articular surface, but

here was little osseous lesion in the greater tuberosity. The destruc-ion pattern was GHD, uniformly mild type. The destruction wassymmetrical. B, The left shoulder showed no pronounced lesionnd was at glenohumeral joint destruction (GHD) grade 1. It had aild grade of greater tuberosity destruction (GTD).

igure 4 Radiographs of the rheumatoid shoulders of a 52-year-ld woman. A, The right shoulder was at glenohumeral jointestruction (GHD) grade 1 and had a mild grade of greater

uberosity destruction (GTD). It showed no pronounced osseousesion. B, The left shoulder was at GHD grade 2 and a severerade of GTD. It showed an extensive osseous lesion in the greater

uberosity, but the original articular surface had not yet disap-eared. The destruction pattern was uniformly mild/GTD type. Theestruction was asymmetrical.

lassification system, the severity of GHD was classified

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nto 6 grades: grade 0 in 4 joints (1.0%), grade 1 in 94oints (23.3%), grade 2 in 151 joints (37.6%), grade 3n 46 joints (11.4%), grade 4 in 29 joints (7.2%), andrade 5 in 78 joints (19.4%). Thus, 107 (26.7%) of02 joints had a grade of 4 or more (Table I).Greater tuberosity destruction. As described ear-

ier, the severity of the GTD was classified into 3rades: mild in 128 shoulders (31.8%), moderate in98 shoulders (49.3%), and severe in 76 shoulders

18.9%; Table II).

tatistical analysis

A comparison of gender and GHD or GTDcores found no significant difference between mennd women in GHD (P � .26) and GTD scores (P �67).

There was no correlation between age and theHD (r � 0.11; P � .03) or GTD (r � –0.09; P �

able I Radiographic assessment by Larsen method of thelenohumeral joints in 201 patients with rheumatoid arthritis*

Right GHD grade

Total0 1 2 3 4 5

eft GHD grade(No. of joints)

0 2 0 0 0 0 0 21 0 30 17 0 1 3 512 0 10 47 12 1 3 733 0 0 9 9 4 1 234 0 0 3 1 5 4 135 0 3 2 1 5 28 39Total 2 43 78 23 16 39 201

HD, Glenohumeral joint destruction.The number of the left GHD grade for each right GHD grade is presented.he grade of GHD between individual left and right sides is significantlyorrelated (r � 0.69, P � .001).

able II Radiographic assessment of the greater tuberosityestruction in 201 patients with rheumatoid arthritis*

Right GTD grade

Mild Moderate Severe Total

eft GTD grade(No. of joints)

Mild 48 17 4 69Moderate 9 75 14 98Severe 2 8 24 34Total 59 100 42 201

TD, Greater tuberosity destruction.The number of the left GTD grade for each right GTD grade is presented.he grade of the GTD between individual left and right sides is significantlyorrelated (r � 0.65, P � .001).

35) scores. Significant correlations were found G

etween the individual left and right sides (Tables Ind II) for both. GHD (r � 0.69, P � .001) and;TD (r � 0.65, P � .001) and between GHD andTD (r � 0.58, P � .001) within the same shoulder

Table III).

eterogeneous destruction within a shoulder

We showed that there was a significant correlationetween the GHD and GTD scores within the samehoulder. However, we investigated 97 shoulders24.1%) from 67 patients who showed a heteroge-eous pattern within their shoulders of the GHD type64 shoulders in 42 patients) and GTD type (33houlders in 25 patients).

We then assessed the pattern of destruction on thepposite side for these patients (see Table IV). In theHD type, 22 (52.4%) of 42 patients showed a

ymmetrical pattern. In the same manner, in the GTDype, 8 (32.0%) of 25 patients showed a symmetricalattern. No patients presented with heterogeneousatterns in which there was a combination of the

able III The number of the greater tuberosity destruction grade isresented for each glenohumeral joint destruction grade in 402houlders from 201 patients*

GHD grade

Total0 1 2 3 4 5

TD grade (No.of joints)

Mild 4 63 54 6 0 1 128Moderate 0 31 82 22 16 47 198Severe 0 0 15 18 13 30 76Total 4 94 151 46 29 78 402

TD, Greater tuberosity destruction; GHD, glenohumeral joint destruction.There was a significant correlation between the grade of GHD and GTDr � 0.58, P � .001).

able IV The pattern of the opposite side is presented in 67atients with heterogeneity of destruction

Pattern of opposite side

TotalUniformly

mild* SymmetricUniformlysevere†

HD type 13 22 7 42TD type 14 8 3 25

otal 27 30 10 67

HD, Glenohumeral joint destruction; GTD, greater tuberosity destruction.GHD grade �3, GTD grade is severe.GHD grade �4, GTD grade mild or moderate. No case showed asymmet-ic heterogeneous pattern.

HD type and the GTD type.

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ISCUSSION

In general, joint destruction caused by RA is bilat-ral and symmetrical.4,8,13,19,21 One study showedhat the left-right symmetry of the severity of jointestruction was especially pronounced in patientsith severe RA.13 Similarly, in the present study, thereas a statistically significant correlation in the GHDnd GTD scores between the left and right sides. Inddition, a significant correlation was found between

he GHD and GTD scores within the same shoulder.Many studies4,8,13,19,21 have compared the pres-

nce of joint destruction between left and right shoul-ers but did not compare the severity of destructionetween the sides or between different areas within

he same shoulder. Like previous reports on shoulderoint destruction, the present study involved manyatients. Many patients were mildly affected, how-ver, and that may have reduced the probability thate could detect statistically significant differencesetween individual sides or the mode of destructionithin a joint.We believe that the joint surface and the greater

uberosity are clinically important parts of the proxi-al humerus because of their role in joint congruitynd rotator cuff function, respectively. Lehtinen et al13

onfirmed radiographically that the mildest sign in theheumatoid shoulder is marginal erosion on the su-erolateral articular margin of the humerus. We there-ore assessed the presence of osseous lesions of these

areas.The present study assessed,the severity of GHD

nd GTD. There were correlations in the GHD andTD scores between the same sides (Tables I and II)nd between the GHD and GTD scores within theame shoulder (Table III). With respect to GHD, only8 patients (9.0%) showed a clear difference be-

ween their left and right sides (�2 grades separa-ion; Table I). With respect to GTD, only 6 patients3.0%) showed a clear difference between their leftnd right sides (�2 grades separation; Table II).onversely, within the same shoulder, 97 shoulders

rom 67 patients that showed a heterogeneous pat-ern: 64 shoulders from 42 patients for the GHD type,nd 33 shoulders from 25 patients for the GTD type.

n the GHD type, 22 (52.4%) of 42 patients showedsymmetrical pattern. Similarly, in the GTD type, 8

32.0%) of 25 patients showed a symmetrical pattern.n interesting finding was that no patients showed aombination of the GHD type plus the GTD typeTable IV).

This suggests that most patients showed uniformnd symmetrical destruction. Even if the caseshowed heterogeneous destruction within the samehoulder, the opposite side always showed a symmet-ical, heterogeneous pattern or uniform destruction.

his did not seem to be a random occurrence.

We considered 2 factors that might cause thisariety of destruction. First, absorption of the cartilagend bone as a result of the actions of cytokineseleased from the synovial tissue or direct destructionf the marginal bone may have resulted in theseiffering patterns. The second factor was the effectsrom anatomic and mechanical factors. Some studiesave shown that mechanical stress can affect shoul-er destruction. Other studies have found that handominance has no effect on the severity of joint de-truction, suggesting that mechanical stress has littleffect.11-14 Because the shoulder joint is not a weight-earing joint, mechanical stress may have a lesserffect than for weight-bearing joints such as the hip ornee. However, we could not generate a reliableypothesis in this study to explain our results ade-uately. Ochi et al18 reported that even in the same

oint, the mechanism of destruction varies widelyepending on the disease subset.The condition of the bone and cartilage may

ffect the progression of bony destruction. This maye further affected by several factors, such as age,ender, medication, and the duration of the dis-ase.2,5-8,15,18,20 In this study, the severity of bothTD and GHD types did not seem to be affected

ignificantly by gender or age in the statistical anal-sis. All of the present patients received some form ofedication, but the drugs used and the time course ofdministration varied widely, making it difficult tossess the effects of drug-induced bone destruction.urthermore, the disease durations were not assessedecause of a lack of information from the patients.egrettably, we could not assess other factors, suchs laboratory data or the condition of the rotator cuff,

oint cartilage, or bone marrow. Further studies areequired to determine the mechanism of joint destruc-ion using magnetic resonance imaging or more de-ailed clinical data.

In conclusion, shoulders with RA showed statisti-ally significant symmetry and uniform destruction onlain radiographs. Even if the shoulders showed het-rogeneous destruction, no patients presented with aifferent pattern of heterogeneity on the oppositeide. The mode of destruction was not always defi-ite, however: some subjects showed heterogeneousestruction within a joint, and a few showed unilat-ral destruction or a difference in the degree ofestruction between left and right sides.9,16,17

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