Annals of the Rheumatic Diseases 1997;56:85–90 85 Ann Rheum Dis: first published as 10.1136/ard.56.2.85 on 1 February 1997. Downloaded from EXTENDED REPORTS Bone formers: osteophyte and enthesophyte formation are positively associated Juliet Rogers, Lee Shepstone, Paul Dieppe Abstract phenomenon, unrelated to any joint disease.4 Objective—To test the hypothesis that New bone can form at individual entheses in enthesophyte formation and osteophyte response to a seronegative spondarthritis.5 growth are positively associated and to More commonly, they are seen in several sites look for associations between bone forma- as part of the condition first described in the tion at diVerent sites on the skeleton so spine by Forrestier and Rotes-Querol6 and now that a simple measure of bone formation known as diVuse idiopathic skeletal hyperost- could be derived. osis (DISH).7 Methods—Visual examination of 337 adult The presence of periarticular osteophytes skeletons. All common sites of either has been noted by Resnick and Niwayama in enthesophyte or osteophyte formation DISH1 but the relation of enthesophyte and were inspected by a single observer who marginal osteophytosis in this condition has graded bone formation at these sites on a not been specifically investigated. This study 0-3 scale. The total score for each feature tests the hypothesis that some individuals have was divided by the number of sites exam- a greater tendency to form bone at both joint ined to derive an enthesophyte and an margins and entheses than others. The osteophyte score. Cronbach’s á and hypothesis has been derived from the observa- principal components analysis were used tion in skeletal studies of striking osteophyte to identify groupings. formation in a subgroup of skeletons, including Results—Enthesophyte formation was those with DISH, and from the reports quoted associated with gender (M>F) and age. above. The latter suggests that a variable There was a positive correlation between amount of bone formation occurs at these two http://ard.bmj.com/ enthesophytes and osteophytes (r = 0.65, sites as a result of a mixture of age, a systemic 95% confidence interval, 0.58 to 0.71) predisposition, and local biomechanical which remained after correction for age factors. and gender. Principal components analy- Radiographs provide an insensitive and sis indicated four diVerent groupings of inadequate way of assessing osteophyte forma- enthesophyte formation. By choosing one tion and enthesophyte changes.8 In contrast, site from each group a simple index of the visual examination of skeletons allows all total skeletal bone formation could be aspects of the joint margin and several different on September 26, 2021 by guest. Protected copyright. derived. ligament and tendon insertion sites to be Conclusions—Osteophytes and entheso- examined in detail, and graded for the amount phytes are associated, such that a propor- of bony change. We have therefore system- tion of the population can be classified as atically examined a number of skeletons for “bone formers”. Enthesophyte groupings evidence of bony changes at several joint mar- provide some clues to aetiopathogenesis. gins and enthesophyte sites, and examined the Bone formation should be investigated as data for associations. a possible determinant of the heterogene- The unique opportunity of visual examina- ity of outcome and of treatment responses tion of whole skeletons also allowed us to in common musculoskeletal disorders. document enough enthesis sites to investigate the data for possible groupings, which might Rheumatology Unit, (Ann Rheum Dis 1997;56:85–90) Department of provide insights into the aetiopathogenesis of Medicine, University Musculoskeletal disorders are associated with enthesopathy as well as developing a method of of Bristol, Bristol the formation of new bone at two main sites: quantifying the phenomenon and thus Royal Infirmary, the joint margin (osteophytosis) and ligament Bristol BS2 8HW, allowing us to derive a simple measure of United Kingdom and tendon insertions (enthesophyte forma- “bone formation”. The development of a J Rogers tion).12 Osteophytes are strongly associated working definition is necessary before any L Shepstone with osteoarthritis, probably forming in clinical implications can be investigated. P Dieppe response to abnormal stresses on the joint 3 Correspondence to: margin. However, the degree of osteophytosis Methods Dr Juliet Rogers. in osteoarthritis varies considerably, and there Three hundred and thirty seven adult skeletons Accepted for publication is some evidence that small marginal from routine studies of the skeletons from 24 October 1996 osteophytes can also develop as an age related three separate archaeological sites were 86 Rogers, Shepstone, Dieppe Table 1 Osteophyte and enthesophyte locations all skeletal elements surviving, including the Ann Rheum Dis: first published as 10.1136/ard.56.2.85 on 1 February 1997. Downloaded from spine and the main long bones. Missing bones Osteophytes: spinal and peripheral joint sites Enthesophytes: ligament insertion sites were assumed to be missing at random. There Odontoid Distal interphalangeal joints Rotator cuV were 202 male skeletons, 129 female, and six Cervical facet joints Hip Olecranon—ulna were unsexed. The age ranges were young Thoracic facet joints Knee: medial compartment Deltoid tubercle—humerus Lumbar facet joints Knee: lateral compartment Bicipital tuberosity—radius adult (20-25 years) to old adult (more than 60 Temporomandibular joint Knee: patellofemoral joint Greater trochanter—femur years), as aged by standard anthropological Acromioclavicular joint Ankle Lesser trochanter—femur 910 Sternoclavicular joint Tarsal joints Linear aspera—femur techniques. The skeletons were dated from Glenohumeral joint Metatarsophalangeal joints Tibial tubercle between the 9th century and the 16th century; Elbow Interphalangeal joints Soleal line—tibia 91 were from excavations at Wells Cathedral, Wrist Quadriceps insertion—patella Thumb base Iliac crest—pelvis 165 from St Oswald’s priory in Gloucester, and Other carpal metacarpal Ischial tuberosity—pelvis 81 from St Peter’s Church, Barton-on- joints Posterior spur—calcaneum Humber. All available skeletons from the sites Metacarpophalangeal joints Inferior spur—calcaneum Proximal interphalangeal at Wells and St Oswalds were used, and a fur- joints ther group from Barton-on-Humber was added to increase the power of the study. The selected for entry into this project. All the data skeletons were observed for osteophyte around were collected according to our standard the margins of vertebral bodies and at 23 protocols and were acquired before deciding to peripheral joint sites, and enthesophyte at 14 use them to examine the hypothesis addressed ligament insertion sites (table 1). The joint in this paper. Each skeleton had at least half of sites were selected to include most synovial http://ard.bmj.com/ on September 26, 2021 by guest. Protected copyright. Figure 1 (A) Knees showing marked osteophytes grade III and enthesophytes at the Figure 1 (A) Knees showing marked tibial tubercle grade II. (B) Grade III osteophyte osteophytes grade III and enthesophytes at the around the carpo-metacarpal joint of the thumb. tibial tubercle grade II. (B) Grade III (C) Calcaneum with grade II enthesophyte and osteophyte around the carpo-metacarpal joint of patellae with grade III enthesophyte. (D) Radius the thumb. (C) Calcaneum with grade II with grade II enthesophyte at occipital enthesophyte and patellae with grade III protuberance and grade I osteophyte at enthesophyte. (D) Radius with grade II radioulnar articulation. Ulna humeral joint has enthesophyte at occipital protuberance and grade grade II osteophyte. (E) Hip joint showing I osteophyte at radioulnar articulation. Ulna greater trochanter of femur with grade II humeral joint has grade II osteophyte. (E) Hip enthesophyte and lesser trochanter with grade I joint showing greater trochanter of femur with enthesophyte. The iliac crest also has grade II enthesophyte and lesser trochanter with enthesophytes, grade I, and the ischial tuberosity grade I enthesophyte. The iliac crest also has enthesophytes grade II. enthesophytes, grade I, and the ischial tuberosity enthesophytes grade II. Correlation of osteophyte and enthesophyte formation 87 articulations around the skeleton. The between sexes). A general linear model was Ann Rheum Dis: first published as 10.1136/ard.56.2.85 on 1 February 1997. Downloaded from odontoid peg was observed separately from the used to assess the strength of the relations rest of the cervical facet joints. In the spine the between enthesophyte scores and osteophyte presence of osteophyte at any cervical, scores while allowing for other potential thoracic, or lumbar facet joint was deemed to confounding variables. A square root transfor- be positive for that segment. The three mation was taken of the enthesophyte score compartments of the knee joint were observed (the dependent variable) in order to achieve as individual joints and the thumb base was normally distributed residuals. Statistical treated separately from the rest of the significance was set at the 5% level. carpal-metacarpal joints. The presence of An attempt was made to find a small number osteophyte in any metacarpal-phalangeal of enthesophyte sites that could be used to (MCP) joint, a proximal interphalangeal joint- construct an enthesophyte score with little loss (PIP), or a distal interphalangeal joint counted of information (referred to as the