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1 Department of Radiology, Stanford University School of Medicine, Medical
Center S056, Stanford, CA 94305-5105.
2 Department of Radiology, University of Vienna, Austria, Wahringer Gurtel
18-20, Vienna A-1090, Austria.
3 Institute of Anatomy, University of Vienna, Austria, Wahringer Strasse 13,
Vienna A-1090, Austria.
Received April 11, 2002;
accepted after revision August 22, 2003.
Address correspondence to A. M. Herneth.
Abstract
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MATERIALS AND METHODS. The study cohort comprised 32 children who had undergone unenhanced radiography, CT, or MRI for reasons other than bone disorders and who presented with enlarged ischiopubic synchondroses. In these children, the distribution of enlarged ischiopubic synchondrosis and foot dominance were evaluated either retrospectively (n = 11) or prospectively (n = 21).
RESULTS. In this cohort, 78% of patients were right-footed and 22% were left-footed. Nine of the 32 children presented with unilateral enlarged ischiopubic synchondrosis (left, seven [78%] of nine; right, two [22%] of nine). All children with enlarged left ischiopubic synchondrosis were right-footed, and all children with enlarged right ischiopubic synchondrosis were left-footed.
CONCLUSION. Unilateral enlarged ischiopubic synchondrosis is closely correlated with foot dominance. The asymmetric ossification pattern of the ischiopubic synchondrosis indicates delayed ossification of this anatomic structure due to asymmetrically applied mechanical forces to the nondominant limb.
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The enlarged ischiopubic synchondrosis is an anatomic structure that occurs in all children during skeletal maturation, and its distinctive closure sequence shows a strong age dependency [1, 810]. In younger children, the enlarged ischiopubic synchondrosis is frequently observed bilaterally, indicating that its fusion begins symmetrically in both hemipelves. However, in older children, before complete ossification of this synchondrosis, unilateral enlarged ischiopubic synchondrosis is seen more commonly [1]. We have previously reported that this age dependency was evident on MRI in 17 healthy children with ischiopubic synchondrosis [17]. However, in this cohort, a nonstochastic, left-sided predominance (86%) of unilateral enlarged ischiopubic synchondrosis was observed, which, to our knowledge, has not been described.
Several reports in the literature indicate that the ischiopubic synchondrosis is susceptible to mechanical stress, which may cause delayed ossification of this temporary joint [9, 11, 15, 17]. During certain athletic activities, such as jumping or kicking, mechanical forces exerted on the ischiopubic synchondrosis of the weight-bearing standing leg are increased compared with those of the swinging leg. The standing leg is in general the nondominant leg, which is the left leg in most humans, according to Peters [18] and Annett [19]. Thus, unevenly applied mechanical forces during common athletic activities may cause the prolonged persistence of the enlarged ischiopubic synchondrosis in the non-dominant limb. The purpose of this study was to correlate foot dominance with the distribution of unilateral enlarged ischiopubic synchondrosis in prepubertal children.
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In the second cohort, foot and hand dominance was evaluated prospectively. To maintain consistency between these two cohorts, we used the same age range and exclusion criteria as those used for the retrospective cohort. In 29 children, 18 girls (62%) and 11 boys (38%), foot and hand dominance was evaluated before imaging by asking the children to kick a ball, then to throw a ball to the examiner, and finally to draw his or her favorite animal with a pencil. The arm and leg used for these tasks were documented. Twenty-one (72%) of these 29 children presented with enlarged ischiopubic synchondrosis (bilateral, n = 14; unilateral, n = 7).
Age, foot dominance, hand dominance, and distribution of enlarged ischiopubic synchondrosis were evaluated for each study cohort separately and for all 32 children included. Differences in age, foot dominance, and distribution between the two cohorts were calculated with the Student's t test, and differences were considered significant with a p value of less than 0.05. Descriptive statistics and the Student's t test were calculated with a commercially available software package (SYSTAT 8.0, Statistical Package for the Social Sciences, Chicago IL).
Informed consent was obtained before the investigation from the parents of all included children. According to our national and institutional guidelines for ethical review, institutional review board approval was not necessary.
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In the 32 children who presented with either bilateral or unilateral enlarged ischiopubic synchondrosis, foot dominance and hand dominance were evaluated. No discordance between foot and hand dominance was observed in either the retrospectively or the prospectively evaluated cohort; thus, we decided to concentrate on foot dominance only. Twenty-five (78%) of the 32 children were right-footed and seven children (22%) were left-footed. The distribution of foot dominance between the prospectively and retrospectively evaluated cohorts was 17 (81%) of 21 versus four (19%) of 21 and eight (72%) of 11 versus three (27%) of 11, respectively. This difference was not statistically significant.
Nine (28%) of these 32 children presented with unilateral (Fig. 1A, 1B, 1C) and 23 (72%) with bilateral enlarged ischiopubic synchondrosis (Fig. 2A, 2B). Of these nine children with unilateral enlarged ischiopubic synchondrosis, seven (78%) presented with left-sided and two (22%) with right-sided enlarged ischiopubic synchondrosis. All seven children with left-sided enlarged ischiopubic synchondrosis were right-footed, and both children with right-sided enlarged ischiopubic synchondrosis were left-footed. Of the 23 children with bilateral enlarged ischiopubic synchondrosis, 18 were right-footed and five were left-footed.
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The nonstochastic predominant persistence of unilateral enlarged left ischiopubic synchondrosis in healthy children was unexpected and, to date, unexplained. The data of the current study provide evidence that unilateral enlarged ischiopubic synchondrosis is related to the foot dominance of the individual and that it emerges in the weight-bearing, nondominant leg.
Since its first description in 1924 [2], the enlarged ischiopubic synchondrosis has been the subject of controversy because it resembles a tumor and because of its doubtful origin. In children with pain in the groin, van Neck [2] and Odelberg [3] described a radiolucent swelling of the ischiopubic fusion zone and referred to this new entity as "osteochondritis ischiopubica." Because this finding occurred frequently in healthy and asymptomatic children and seemed to disappear after skeletal maturation, other terms, such as "osteochondrosis ischiopubica" and "osteochondropathia ischiopubica," were introduced [4, 5, 79, 12, 15, 16, 2123]. The benign nature of this tumorlike finding was then suggested by researchers who evaluated ischiopubic synchondrosis in larger cohorts [1, 9, 11].
Our hypothesis is based on the premise that ischiopubic synchondrosis is susceptible to mechanical stress. This susceptibility was first mentioned by Duben [11], who suggested that callus is formed as a physiologic answer to increased mechanical strain, which leads to the distinct fusiform enlargement of ischiopubic synchondrosis [26]. This hypothesis was strongly supported by Pratje [1] and Hubner [9], both of whom described the typical ossification pattern in healthy children. The detailed histologic examinations of Hubner are a cornerstone for understanding this physiologic ossification process. Hubner found that the enlarged ischiopubic synchondrosis is formed by hyaline cartilage originating from the adjoining rami of the ischiic and the pubic bones. Before fusion of these chondral anlagen, the cell layers decline in height toward the smoothly shaped surface, leaving a small cleft. This configuration and the strong enhancement of the cell layers close to the surface (i.e., tangential layer) on H and E staining are typical for joints and jointlike structures, which are subject to mechanical stress [9]. Thus, Keats [15] considered the ischiopubic synchondrosis to be a "temporary joint." In addition, typical findings on MRI in children with ischiopubic synchondrosis strongly emphasize this hypothesis because in the absence of infection, tumor, or trauma, the edema in the ischiopubic synchondrosis and the surrounding tissues is most likely caused by mechanical irritation [17].
The pattern of mechanical forces applied to the pelvis when the hip joint is flexed and extended is complex and has been well shown in functional models [9, 27]. In addition to the adductor group, which strains the ischiopubic synchondrosis to the greatest degree, the iliopsoas and gemellus muscles are the main contributors to mechanical stress in this area. Mechanical stress causes constant movement in this temporary joint, which would prolong fusion of the adjoining cartilage layers and would then delay ossification of these synchondroses [26]. Unequally distributed forces may then lead to asymmetric closure, as has been observed in this and previously reported studies [9, 17, 20].
Physiologically, asymmetric muscle action occurs during skilled motor activities such as jumping or playing ball games [28, 29]. Although these activities are performed with the dominant leg (i.e., the swinging leg), the major strain is sustained by the weight-bearing, nondominant leg (i.e., the standing leg). In the prepubescent pelvis, these unequally distributed forces may then cause delayed closure of the enlarged ischiopubic synchondrosis on the nondominant side. This theory is strongly supported by the data of our study, indicating that in right-footed children, unilateral enlarged ischiopubic synchondrosis occurs in the left hemipelvis and vice versa.
Furthermore, this theory is fortified by the studies of Hubner [9] and Pratje [1], who described asymmetric ossification of enlarged ischiopubic synchondrosis in children with unilateral hip luxation, coxitis, congenital coxa vara, and Legg-Perthes disease. Whenever unilateral enlarged ischiopubic synchondrosis was present in these children, the enlarged ischiopubic synchondrosis was seen in the healthy hemipelvis opposite the affected hip. In these children, uneven mechanical straining of the ischiopubic synchondrosis occurred after immobilization of the affected limb due to pain or treatment or both over a substantial course of time. Thus, delayed ossification of the enlarged ischiopubic synchondrosis in the hemipelvis opposite the affected hip can be explained by regular or even increased muscle strain compared with the reduced muscle strain at the ischiopubic synchondrosis of the immobilized limb. In addition, Hubner found that the ossification of the ischiopubic synchondrosis ipsilateral to the hip abnormality occurred at an earlier age than it occurred in healthy children, indicating that reduction of mechanical stress results in more rapid ossification of these synchondroses.
The predominance of enlarged left ischiopubic synchondrosis in our study corresponds to other anthropometric parameters, which, in turn, are determined by function and laterality. Increased diameter of the bones in the left foot has been reported by several authors [3032]. Furthermore, Pretterklieber [33] reported better vascularization and higher density of the sesamoid bones of the left human hallux. Because body weight is distributed over the bones of the legs, particularly over the bones and sesamoid bones of the first metatarsal ray, these asymmetries in size, density, and vascularization indicate that higher ground reaction forces are exerted on the left foot and result in increased mechanical straining of the left lower limb [34].
Our study is limited by the number of left-footed children with unilateral enlarged ischiopubic synchondrosis. However, this small number can be explained by the fact that in the average population, the frequency of left-footed individuals is approximately 1320% [18, 19]. Furthermore, according to our exclusion criteria, only a fraction of surveys were applicable for this study; thus, a prolongation of the study for an acceptable time would not have increased substantially the number of left-footed children with unilateral enlarged ischiopubic synchondrosis. However, according to the demographic data published to date, the study cohort can be considered representative for this purpose.
In conclusion, our data provide further evidence that the distinct appearance of this temporary joint is a physiologic reaction of the human body to mechanical strain, and the observed laterality can be explained by increased ground reaction forces exerted on the nondominant limb (i.e., the standing leg) during certain kinds of physical exercise. Thus, the nonstochastic predominance of unilateral enlarged ischiopubic synchondrosis in the left hemipelvis can be correlated to foot dominance.
Acknowledgments
We thank Michelle Prior for her valuable help in preparing and editing the
manuscript.
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