The Association Between Ulnar Length and Forearm Movement in Patients With Multiple Osteochondromas

The Association Between Ulnar Length and Forearm Movement in Patients With Multiple Osteochondromas Adam C. Watts, MD, J. Andrew Ballantyne, MD, Maria Fraser, BA, A. Hamish R. W. Simpson, MD, Daniel E. Porter, MD From the Edinburgh University Department of Orthopaedic Surgery, New Royal Infirmary, Little France, Edinburgh, United Kingdom and Nuffield Department of Orthopaedic Surgery, Nuffield Orthopaedic Centre, Headington, Oxford, UK.

Purpose: To determine the relationship between the length of the ulna as a proportion of height (proportional ulnar length [PUL]), forearm and wrist ranges of motion, and degree of observable deformity in people with hereditary multiple exostoses. Methods: One hundred forty-two people with hereditary multiple exostoses were examined; 35 were under the age of 15 years and therefore were presumed to be skeletally immature. Elbow, forearm, and wrist motion were measured, and the radius and ulna were palpated for osteochondromas. Ulnar length was estimated as a proportion of height (PUL) in skeletally immature subjects. The relationships between total active motion, number of palpable osteochondromas, and proportional length were examined for one randomly selected limb from each subject. Results: A negative correlation was found between the number of palpable osteochondromas and range of forearm rotation. The degree of forearm motion in those under the age of 15 years was directly related to PUL and indirectly related to the number of palpable osteochondromas. Children whose PUL is within the normal range have a normal range of motion. Conclusions: In a child with hereditary multiple exostoses affecting the forearm, the PUL is associated with the range of movement and deformity, and it can be a useful adjunct in deciding the appropriate management. (J Hand Surg 2007;32A:667– 673. Copyright © 2007 by the American Society for Surgery of the Hand.) Key words: Deformity, forearm, movement, hereditary multiple exostoses, multiple osteochondromas.

ereditary multiple exostoses (HME) is an autosomal dominant condition with 100% penetrance but great variability in phenotypic expression1 that affects 1 in 50,000 people.2 It is characterized by bony lumps and osteochondromas that appear at the metaphysis of long bones during development.3 The genes responsible for the condition can be localized in approximately 80% of patients.4 – 6 The development of an osteochondroma can affect the longitudinal growth of a bone.7 Where there are paired bones (the forearm and the leg) there is particular risk of joint deformity, because discrepancies in rate of longitudinal growth can cause distortion of the anatomy. In the leg this leads to a characteristic

H

valgus deformity of the ankle due to relative shortening of the fibula,8 which is symptomatic in 18% and limits recreational activities in up to one third of patients with HME.9 Noonan et al9 also found that this disruption of the normal anatomy could lead to premature osteoarthrosis. The involvement of upper-limb bones by HME is associated with greater loss of function than elsewhere in the body,10 but even here the loss of function may be limited.11 Shortening of the ulna is commonly seen in the forearms of patients with HME, and most researchers recognize that ulnar shortening is an important consideration in planning treatment for forearm deformity.12–16 Current methods of assessing the degree of shortening rely on The Journal of Hand Surgery

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comparing the tip of the distal ulna with the ulnar border of the distal radial articular surface13,16 –18 on an anteroposterior radiograph of the wrist. This will tend to underestimate the degree of ulnar shortening, because tethering of the distal radius results in radial bowing, differential longitudinal growth on the radial and ulnar border resulting in an increase in the distal radial articular angle, and ultimately in radial head dislocation.19 Using ulnar length as a proportion of height circumvents this problem. The constant relationship between height and ulnar length has long been recognized in forensic medicine and is used to calculate the stature of an individual when only the ulna is available.20 Although it is known that individuals with HME may not attain their predicted adult height because of longitudinal growth retardation of the long bones in the lower limb or vertebral involvement,7 this growth retardation is not thought to occur until the individual is nearing skeletal maturity.21 We examined the relationship between the length of the ulna as a proportion of height (proportional ulnar length [PUL]) and the forearm and wrist ranges of movement in a population with HME. In addition, the relationship between the number of palpable exostoses, PUL, range of movement, and degree of deformity in individuals with HME was examined. The application of a biometric constant, PUL, improves the clinical assessment of the true extent of ulnar shortening in people who are skeletally immature.

Materials and Methods Proportional Ulnar Length The length of the ulna is known to be proportional to the height of a healthy individual. Proportional ulnar length can vary with ethnicity but in a largely white population has been shown to be 15%.22 To determine the PUL in the healthy population where the study was performed, 32 healthy adult volunteers were examined. Measurements were made of the standing height (in centimeters) and ulnar length, from the tip of the olecranon to the tip of the ulna styloid (in centimeters). From these measurements a biometric value was calculated—PUL—that was defined as the ulnar length in centimeters divided by the height in centimeters multiplied by 100. Thirty-two healthy children from the ages of 2 to 14 years were examined, and the PUL was calculated in the same way. The Forearm in Hereditary Multiple Exostoses Two hundred eighty-four upper limbs from 142 individuals with HME with bilateral upper-limb in-

volvement were available for study with local ethical committee approval. Sixty-four patients (45%) were male and 78 (55%) were female, with a mean age of 32 years (range, 3–76 y). Thirty-five patients were under the age of 15 years. The right or left upper limb was selected for each patient by computerized random number generation, leaving 142 limbs for inclusion in the study.23 The right limb was selected in 72 patients (51%) for whom an odd number was generated and the left for the 70 (49%) patients with an even number. Demographic data such as age, gender, and height were recorded for linear regression analysis. By clinical examination, the ulnar length was measured (tip of the olecranon to the tip of the ulna styloid). This enabled calculation of the PUL as described, expressed as a percentage of each patient’s height (measured ulnar length [cm]/height [cm] ⫻ 100). The PULs of the skeletally immature healthy and HME populations were compared. The number of palpable osteochondromas within the forearm was recorded according to anatomic location (proximal or distal half of radius or ulna). This has been shown to correlate with radiographic assessment of the number of osteochondromas.7 Radiographs that had been required on clinical grounds were available for 44 subjects with HME. An observer blinded to the number of osteochondromas palpable by clinical examination recorded the number of osteochondromas present radiographically on the proximal and distal halves of the radius and ulna. Nonparametric correlation was performed to compare the results. With a goniometer the ranges of active elbow flexion/extension, forearm pronation/supination, and wrist flexion/extension were quantified in degrees. The movement was defined as poor according to the criteria of Morrey et al24 if there was more than 30° of fixed flexion of the elbow, less than 130° of active elbow flexion, and less than 50° of active pronation or supination. The degree of forearm deformity was assessed, without the use of radiographs, by 2 observers by inspection and palpation and was categorized on a subjective 4-point clinical scale: 1, no visible deformity; 2, isolated ulnar shortening; 3, shortened ulna and bowing of the radius; and 4, shortened ulna, bowed radius, and dislocation of the radial head. Statistical Analysis Statistical analysis was performed using software (SPSS for Windows, version 13.0; SPSS Inc., Chicago, IL). The mean PULs for healthy skeletally

Watts et al / Forearm Movement in Multiple Osteochondromas

The Forearm in Hereditary Multiple Exostoses In eighty-eight of 142 limbs (62%) there was no clinical forearm deformity on examination, 29 limbs (20%) had isolated ulnar shortening, 17 limbs (12%) had bowing of the radius, and 8 limbs (6%) had, in addition a dislocated radial head.

14

12

Number of individuals

669

10

8

6

4

Std. Dev = .56

2

Mean = 15.01 0 13.75

14.25 14.00

14.75 14.50

15.25 15.00

15.75 15.50

16.25 16.00

Proportional Ulnar Length (%)

Figure 1. Histogram of the relative ulnar length of a series of healthy volunteers.

immature volunteers and individuals with HME were compared with the Student t test. Ranges of movement for those with a PUL within the normal range and for those whose PUL was below the normal range were compared with the Mann-Whitney U test. Mean ranges of movement were compared between deformity categories using 1-way analysis of variance. Correlations between the PUL, number of palpable osteochondromas, and range of movement were tested with the Spearman correlation coefficient. Linear regression analysis was used to analyze the influence of gender, age, number of palpable exostoses, and PUL on range of movement. The results were considered statistically significant if p was less than .05.

Anatomic Distribution Eighty-four of 142 limbs (58%) had palpable involvement of the distal ulna, and 106 (75%) had palpable involvement of the distal radius. Palpable involvement of the proximal forearm was much lower, with 14 limbs (10%) having osteochondromas on the proximal radius and 4 (3%) having osteochondromas on the proximal ulna, although this may in part reflect the greater muscle bulk of the proximal forearm disguising the presence of an exostoses. Range of Movement Elbow. The median arc of elbow movement was 140° (interquartile range, 135°–150°). No patient had fixed flexion of more than 30°. In 16 of 142 limbs (11%) there was poor elbow flexion (⬍130° as defined by Morrey et al24). Forearm pronation/supination. The median arc of forearm pronation/supination was 165° (interquartile range, 135°–176°) with a slightly greater loss of supination. In 21 of 142 limbs (15%) a poor range of pronation (⬍50° as defined by Morrey et al24) was recorded, and 24 (17%) had poor supination (⬍50°). Wrist. The median wrist extension was 85°, median wrist flexion was 80°, and total median wrist arc of motion was 160° (interquartile range, 140°–175°).

Results

Estimation of the Number of Osteochondromas by Palpation There was a significant correlation between the number of palpable osteochondromas and the number of osteochondromas detected on radiographs on the proximal and distal radius and ulna (␳ ⫽ 0.56, p ⬍ .001). Clinical examination, however, tended to underestimate the number of osteochondromas present (mean by palpation, 2; mean by radiography, 5).

17.0

16.0

Proportional Ulnar Length (%)

Proportional Ulnar Length of Healthy Volunteers A histogram of PUL data shows that the data are normally distributed (Fig. 1). The mean PUL was 15% (SD, 0.55), in agreement with previously published data.22 The PUL remained constant in childhood (r ⫽ – 0.1, p ⫽ .95) (Fig. 2). The lower limit for the normal PUL was therefore taken as 14% (mean – 2 SDs).

15.0

14.0

13.0

12.0

11.0

10.0 2

4

6

8

10

12

14

Age in Years

Figure 2. Scatterplot of PUL by age for control children.

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Proportional Ulnar Length (%)

16.0

14.0

12.0

Age

10.0 15 Years +

No Clinical Deformity

<15 Years

Isolated Ulnar Shortening Short Ulna/Radial Bow DEGREE OF CLINICAL DEFORMITY

Dislocated Radial Head

Figure 3. Boxplot of the PUL by clinical deformity classification categorized by age (⬍15 y or ⱖ15y).

The only significant relationship was an indirect correlation with age (␳ ⫽ – 0.51, p ⬍ .001). There was no significant correlation in the whole study group between wrist arc of movement and PUL and number of palpable osteochondromas (␳ ⫽ 0.14, p ⫽ .94 and ␳ ⫽ – 0.12, p ⫽ .15, respectively). Proportional Ulnar Length (Pediatric Population) The mean PUL in the limbs of the 35 individuals with HME under the age of 15 years was significantly lower than that in the control pediatric population (14% [SD, 1.2], p ⬍ .001). Proportional ulnar length correlated indirectly with the 4-point deformity scale (␳ ⫽ – 0.50, p ⫽ .002) such that with increasing severity of deformity there was a reduction in mean PUL (Fig. 3). A positive correlation was found between deformity and number of palpable forearm osteochondroma (␳ ⫽ 0.48, p ⫽ .004). In the 35 individuals under the age of 15 with poor range of active elbow flexion, the PUL was significantly lower (mean, 12%; SD, 0.8) and the number of palpable exostoses was significantly higher (n ⫽ 8; SD, 1) compared with those with an acceptable range of elbow flexion (mean, 14%; SD, 1.2 and n ⫽ 3; SD, 2, respectively) (p ⬍ .02). Likewise, those with a poor range of pronation/ supination had a significantly lower PUL (mean, 13%; SD, 1.1) than those with an acceptable range

of movement (mean, 14%, SD, 1.1) (p ⬍ .05) and significantly more palpable osteochondromas (mean, n ⫽ 6; SD, 3 vs mean, n ⫽ 3; SD, 2 in those with a good range of motion) (p ⫽ .01). Based on linear regression analysis, the PUL and number of palpable osteochondromas were found to have the strongest independent relationship with forearm arc of motion (R ⫽ 0.61, ␤ ⫽ 0.4 for palpable osteochondromas; PUL, ␤ 0.3; p ⬍ .05). When ranges of movement at the major joints were compared, there was a significant correlation between the PUL and the arc of pronation/supination (␳ ⫽ 0.50, p ⫽ .002). Those with a PUL below 14% had more palpable forearm osteochondromas and a smaller arc of pronation/supination (Table 1). The proposed application of PUL assumes that in HME recognizable stature retardation does not occur until late adolescence. In this study the 35 individuals with HME under the age of 15 years had normal stature, with 60% of the 35 patients over the 50th percentile and 3% under the 3rd percentile for their ages (Fig. 4).

Discussion There are 2 main limitations to this study. Radiographic measurement of the number of osteochondromas present should be viewed as the gold standard. Radiographs were available for only a few of our subjects based on clinical need, and more radio-

Watts et al / Forearm Movement in Multiple Osteochondromas

Table 1. Comparison of Range of Motion at the Elbow, Wrist, and Forearm for Individuals With Hereditary Multiple Exostoses PUL Age

<14%

>14%

p

Over 14 years Mean age, y Average no. of palpable forearm osteochondromas Elbow arc of motion, ° Forearm supination/ pronation, ° Wrist arc of motion, ° Mean PUL, %

n ⫽ 37 37

n ⫽ 70 40

.26

4 135

2 140

<.001 .64

108 138 13

163 154 15

<.001 .002 <.001

Under 14 years Mean age, y Average no. of palpable forearm osteochondromas Elbow arc of motion, ° Forearm supination/ pronation, ° Wrist arc of motion, ° Mean PUL, %

n ⫽ 13 9

n ⫽ 22 8

.36

4 138

2 146

.02 .06

146 172 13

168 173 15

.06 .75 <.001

NOTE. Boldface indicates significance.

graphic data would have strengthened the findings. Given the association between x-ray exposure and chondrodysplasia,25 it seemed unreasonable to take x-rays for this study. A previous study has reported that “although palpation results in some missed exostoses, a simple clinical count will quantify osteochondromas in such a way that reliably reflects the variation in exostoses numbers from patient to patient.”7 Second, the use of the PUL assumes normal stature of the individual. In skeletally mature individuals with HME, in whom height may be reduced, this value may not be valid. It should be highlighted, however, that in those of short stature the calculation would tend to underestimate rather than exaggerate the degree of ulnar shortening. The forearm is affected in up to 60% of patients with HME.12,19 The proportion with clinically obvious forearm deformity is lower than this— one third of patients in a previous report26—and our data agree with this. Why the longitudinal growth of bones such as the ulna and fibula should be more severely affected in HME has not been explained. Some researchers13 have suggested that osteochondromas remove chondrocytes from the physis and hence reduce

Percentage of Subjects Under 15 Years

70.0%

60.0%

50.0%

40.0%

30.0%

20.0%

10.0%

0.0% <3rd

3rd to 10th

671

10th to 25th

25th to 50th

>50th

Percentiles Figure 4. Height percentiles for individuals with HME under the age of 15 years.

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its growth potential, arguing that the ulna is more severely affected by this phenomenon because it has a smaller cross-sectional area. The current concept of osteochondromas as neoplastic lesions would suggest that this is not the case.27 An alternative theory is that ulnar length is affected more because, compared with the radius, a greater proportion of growth occurs at the distal ulnar physis and that osteochondromas are more commonly seen at the distal end of these bones.3,14 In this series over 84/142 (58%) of limbs had osteochondromas palpable on the distal half of the ulna or radius compared with less than 14/142 (10%) on the proximal half, although the difficulty of palpating osteochondromas under the larger muscle mass of the proximal forearm may bias these data. The current study found a direct association between range of movement and the length of the ulna. On average, those under the age of 15 years with a PUL within 2 SDs of the mean for a sample pediatric population had no clinically relevant loss of elbow flexion or wrist flexion/extension, supination, or pronation. With progressive reduction in the PUL, there is a decrease in the range of pronation/supination. Those with a PUL less than 14% had a smaller arc of pronation/supination than those whose PUL was 14% and higher. This difference was not statistically significant in this group. This supports the study by Mader et al28 that empirically chose shortening of 2 cm (1.5% reduction in PUL for a 10-year-old boy of average height) as one indication for surgery to lengthen the ulna in patients with HME. Other indications were symptomatic loss of wrist, forearm, or elbow movement; 50% ulnar displacement of the carpus, and a radial articular angle greater than 40°. Mader et al28 showed good outcomes with the use of an external fixator for lengthening and found that there was spontaneous improvement of the radial articular angle with lengthening without the need for osteotomy, in agreement with the observation of Pritchett.14 Calculation of the PUL in those of shortened stature would underestimate ulnar shortening. At the time when intervention to restore ulnar length is most likely to be effective, however, this study shows that individuals with HME have the same distribution of height for age as the rest of the population. Therefore, the use of the PUL to estimate true ulnar shortening up to the age of 15 years remains valid. Some researchers11,12,29 have concluded that surgery only serves to improve appearance and not function. A study of the natural history of the forearm in HME found little disability in a cohort of

patients with HME who had not had any previous surgery18 and reported that there was little evidence of premature joint degeneration. In the present study, however, a significant association was found between increasing age and deterioration in the arc of wrist flexion and extension. This warrants further investigation to determine whether early osteoarthrosis occurs in the wrist joint of individuals with HME. This study suggests that motion in the forearm in patients with HME is dependent on the length of the ulna and the number of palpable osteochondromas in the forearm. The use of a biometric constant (PUL), we believe, reflects the true degree of ulnar shortening in children under the age of 15 years. Removal of solitary osteochondromas can be useful where they are causing pain or pressure effects,13 but it has not been shown that this is an effective technique for preserving ulnar length. Previous literature suggests that lengthening of the ulna in the growing child may halt or even reverse some of the anatomic changes in the forearm and wrist associated with HME,13,16 but there is as yet no evidence that this will improve function.11 The current data suggest that PUL within 2 SDs of the mean for the normal population (⬎14%) is associated with more forearm rotation. This may be used as an additional factor in the decision model when considering management options in a child with multiple osteochondromas. Received for publication April 19, 2006; accepted in revised form February 15, 2007. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Corresponding author: A. C. Watts, MD, Edinburgh University Department of Orthopaedic Surgery, New Royal Infirmary Edinburgh, Little France, Old Dalkeith Road, Edinburgh, EH16 4SU, UK; e-mail: [email protected]. Copyright © 2007 by the American Society for Surgery of the Hand 0363-5023/07/32A05-0013$32.00/0 doi:10.1016/j.jhsa.2007.02.008

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