Cadaveric and MRI Study of the Musculotendinous Contributions to the Capsule of the Symphysis Pubis

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1 Robinson et al. MRI of the Capsule of the Symphysis Pubis Musculoskeletal Imaging Original Research Philip Robinson 1 Fateme Salehi 2 ndrew Grainger 1 Matthew Clemence 3 Ernest Schilders 4 Philip O Connor 1 nne gur 2 Robinson P, Salehi F, Grainger, et al. Keywords: anatomy, MRI, musculoskeletal imaging, pelvic imaging, sports medicine DOI: /JR Received September 19, 2006; accepted after revision December 6, M. Clemence is employed by Philips Medical Systems as a clinical scientist providing research support to academic areas of MR systems. MRI supported by grants from the Football ssociation and the ritish Society of Skeletal Radiology. 1 Department of Radiology, Leeds Teaching Hospitals, Musculoskeletal Centre, Chapel llerton Hospital, Leeds LS7 4S, United Kingdom. ddress correspondence to P. Robinson (p.robinson@leedsth.nhs.uk). 2 Division of natomy, Department of Surgery, University of Toronto, Toronto, ON, Canada. 3 Clinical Science Department, Philips Medical Systems, Surrey, United Kingdom. 4 Department of Orthopedic Surgery, radford Royal Infirmary, radford, United Kingdom. WE This is a Web exclusive article. JR 2007; 188:W440 W X/07/1885 W440 merican Roentgen Ray Society Cadaveric and MRI Study of the Musculotendinous Contributions to the Capsule of the Symphysis Pubis OJECTIVE. The purpose of this article is to define the relations of the symphysis pubis and capsular tissues to the adductor and rectus abdominis soft-tissue attachments on cadaver dissection and correlate with MRI of the anterior pelvis. SUJECTS ND METHODS. Seventeen cadavers (8 males and 9 females; mean age, 80 years) were dissected bilaterally. Rectus abdominis and adductor muscles were traced to the pubis and further attachments to the pubic symphysis were defined. Ten asymptomatic (mean age, 17; age range, years) male athletes underwent 1.5-T MRI of the anterior pelvis with two surface microcoils (each 42 mm in diameter). n axial T2-weighted turbo spin-echo (TSE) sequence (TR/TE, 2,609/106; voxel size, 0.4 mm) was obtained. xial and sagittal 3D T1-weighted fastfield echo (FFE) sequences (25/4.9; voxel size, 0.3 mm) were obtained. Sequences were repeated incorporating fat suppression and IV gadolinium. The relation of the symphysis pubis, disk, and capsular tissues to the insertions of the rectus abdominis, adductor muscles, and gracilis were independently evaluated by two experienced radiologists blinded to all clinical details. RESULTS. In all 17 cadaver specimens, the adductor longus and rectus abdominis attached to the capsule and disk of the symphysis pubis, whereas the adductor brevis had an attachment to the capsule in seven specimens and the gracilis in one. ll adductor tendons attached to the pubis. In all 10 athletes, the adductor longus and rectus abdominis bilaterally contributed to the capsular tissues and disk. This was only the case for the adductor brevis in four athletes. No other tendons involved the capsular tissues. CONCLUSION. Cadaver and MRI findings show an intimate relationship between the adductor longus; rectus abdominis; and symphyseal cartilage, disk, and capsular tissues. ubalgia or chronic exertional groin P pain is a condition that can result in significant morbidity for professional athletes. Sports especially affected tend to involve repetitive kicking and change of direction and include soccer, ustralian rules football, rugby, and ice hockey [1 5]. It is thought that the chronic stresses produced during these forced single-stance maneuvers can result in overuse injuries of the anterior pelvic soft tissues and symphysis pubis [5 7]. thletes with this condition can have relatively poorly localized symptoms and clinical tenderness involving the symphysis pubis, medial inguinal canal, and adductor and lower abdominal muscles [2, 5, 8 10]. lthough a number of surgical series have described soft-tissue abnormalities involving all of these areas, to date MRI series have largely described abnormalities of the symphysis pubis and anterior parasymphyseal soft tissues [6, 10 14]. The symphysis pubis is a nonsynovial diarthrodial joint between the pubic bodies, with each articular surface covered by hyaline cartilage and separated by an intervening fibrocartilaginous disk [15 17]. Classically, the adductor group and rectus abdominis tendons and the inguinal soft tissues are described as having well-defined attachments onto the pubic bones and adjacent rami [15, 18]. The authors hypothesize that there is a pathophysiologic relationship between osteitis pubis and adductor enthesopathy. natomic description of the symphyseal and parasymphyseal soft tissues represents a vital step in defining any relationship between pubalgia, adductor enthesopathy, intrinsic symphyseal joint degeneration, or rectus abdominis tendinopathy and microtears. The aim of this study was to define the relations of the symphysis pubis articular cartilage, fibrocartilage disk, and capsular tissues to the surrounding adductor and rectus abdominis soft-tissue attachments on cadaver dissection W440 JR:188, May 2007

2 MRI of the Capsule of the Symphysis Pubis and correlate these findings with MRI of the anterior pelvis (in athletes). Subjects and Methods Cadaver Dissection Two clinical anatomists with 2 and 28 years of experience, respectively, dissected the anterior pelvic soft tissues in 17 cadavers (8 males and 9 females; mean age, 80 years; age range, years) following institutional ethical guidelines. Fourteen of the specimens were formalin embalmed, and there were three fresh male specimens (ages 58, 67, and 81 years). Using a dissection microscope, the skin and subcutaneous tissue were removed to expose the anterior abdominal wall and the medial and anterior thigh as far distally as the knee. The fascia lata was C Fig. 1 Male cadaver dissection, normal anatomy., Photograph of anterolateral view. sterisks mark center of symphysis pubis. Tendinous attachment of adductor longus (L) to tissue overlying anterior symphysis pubis is elevated by pin (thin white line) and inferiorly outlined with arrows. Pyramidalis (P) is reflected to reveal rectus abdominis (R). Medial margin of adductor brevis () can be seen medial to L., Photograph of same specimen as in with L reflected. Pins (thin white lines) demarcate tendinous attachments of L and to tissue overlying anterior symphysis pubis. sterisks mark center of symphysis pubis. C, Photograph of fresh specimen axial section shows trabeculae of pubic bones (P) with interdigitating hyaline cartilage (large arrows) and fibrocartilage disk (D). Disk and cartilage merge with anterior aponeurotic tissues (small arrows). Right adductor longus (between asterisks) is elevated by pin and is seen contributing to anterior soft tissues. D, Line diagram shows relative position of tendinous attachments with direction (arrows) of involvement over symphyseal capsular tissues. removed to reveal the anterior and medial thigh muscles. The anterior rectus sheath and aponeurotic extensions of the external oblique overlying the pubic area were removed. The pyramidalis and underlying rectus abdominis muscles were exposed and the insertions defined. The adductor longus, adductor brevis, adductor magnus, and gracilis were traced (from superficial to deep) along their attachments to the pubic bone, and then further attachments to the pubic symphysis capsular tissues were defined. ny attachment to the pubic symphysis was carefully exposed, documented, and photographed. The relative tendon and muscle composition of the proximal attachments was noted [18]. The three fresh specimens were also axially sectioned through the pubic symphysis with a slice thickness of mm. D MRI fter institutional ethical board approval was secured for this study, 10 asymptomatic (no pubalgia symptoms > 3 months) professional athletes (all male; median age, 17 years; age range, years) underwent MRI of the anterior pelvis. ll athletes were recruited from three professional soccer teams and completed a symptom questionnaire that recorded any previous injuries and surgery. thletes with a history of groin pain were not excluded. thletes were followed for 6 months by telephone questionnaire to determine any subsequent pubalgia. MRI Protocol ll MRI examinations were performed on a 1.5- T system (Intera, Philips Medical Systems) using a 4-channel flexible array coil (Microcoil, Philips Medical Systems). Two padded elements, each consisting of a 42-mm-diameter surface microcoil, were placed on either side of the pubic symphysis. n axial T2-weighted turbo spin-echo (TSE) multislice sequence (TR/TE, 2,609/106; 24 slices; 5 averages; field of view, mm) with a final voxel size of 0.4 mm in-plane and 3.0 mm through-plane was obtained. Two high-resolution 3D acquisition axial and sagittal T1-weighted fast-field echo (FFE) sequences (25/4.9; 2 averages; 60 slices; field of view, mm) with a final voxel size of 0.3 mm inplane and 1.5 mm through-plane were obtained. These sequences were repeated incorporating spectral inversion recovery fat suppression and IV dimeglumine gadopentetate (Magnevist, Schering-Plough). Image nalysis ll examinations were independently and prospectively evaluated by two radiologists (each with 7 years of musculoskeletal experience) who were unaware of the dissection findings. The radiologists were also blinded to all clinical details and were not aware of the athletes previous history or that they were currently asymptomatic. The anatomy of the symphysis pubis was independently recorded regarding the extent of the pubis articular cartilage, fibrocartilaginous disk, and capsular tissues. The muscles and tendons of the adductor, gracilis, rectus abdominis, and pyramidalis muscle groups were identified and their osseous and soft-tissue origins recorded. bnormal areas of edema or enhancement were recorded. ny discrepancies were resolved by consensus. Results Cadaver Dissection Pubic symphysis capsular attachments ll (17/17) of the adductor longus and rectus abdominis specimens and 41% (7/17) of the adductor brevis specimens had bilateral attachments to the pubic symphysis capsular tissues (Fig. 1 and Table 1). In contrast, only one gra- JR:188, May 2007 W441

3 Robinson et al. TLE 1: Proximal ttachment of dductor Longus and revis to the Pubic Symphysis Capsular Tissues Incidence and Gender Variation on Cadaver Dissection ttachment to Pubic Symphysis No. (%) of Total Specimens (n = 17) No. (%) Female (n = 9) No. (%) Male (n = 8) dductor longus: tendon and muscular 9 (53) 6 (67) 3 (38) dductor longus: only muscular 8 (47) 3 (33) 5 (62) dductor brevis 7 (41) 3 (33) 4 (50) C D Fig. 2 Sequential axial T1-weighted fast-field echo (TR/TE, 25/4.9) spectral inversion recovery fat-suppressed MR images in 28-year-old male athlete with no previous pubalgia and normal anatomy., Image at level just superior to pubic tubercle shows pubic bodies (P) with intervening disk (arrow) and rectus abdominis tendon (arrowheads) closely applied to anterior capsular tissues., Image at level of pubic tubercle shows continuation of rectus abdominis tendon centrally (arrowhead) with contributions from two adductor longus tendons (arrows) lying medial to tubercle on this occasion. Right pubic subchondral cysts (asterisks) are noted. C, Image inferior in relation to shows rectus abdominis condensation is now quite faint (arrowhead) with more definite adductor longus tendons visualized (arrows). D, Image inferior in relation to C shows fully formed low-signal adductor longus tendons (arrows). cilis specimen was found to attach to the pubic symphysis capsular tissues, and the adductor magnus had no symphyseal attachments. ll of these tendons attached to the pubic bone. xial sectioning of the fresh cadavers showed the fibrocartilaginous disk and hyaline carti- W442 lage merging with the capsular tissues and aponeurosis of the adductor longus and rectus abdominis anteriorly (Fig. 1C). Rectus abdominis The pyramidalis was found to attach to a ridge on the superior aspect of the pubic bone and superior ramus, whereas the adductor longus attached inferiorly to this ridge of bone, the pubic tubercle, and the pubic symphysis capsular tissues (Figs. 1 and 1). The rectus abdominis attached to the pubic crest and pubic symphysis capsular tissues continuous with the adductor longus. There was no sex variation with the pyramidalis and rectus abdominis. dductor group ll the adductor longus muscles were found to have a superficial tendinous and deeper muscular component at their proximal attachment. Two patterns of attachment were recognized. In the first group, both the tendon and the muscle attached to the capsular tissues of the pubic symphysis. In the second group, the tendon attached to the pubic tubercle, whereas the muscular component inserted predominantly into the capsular tissues. This latter pattern of attachment was seen more commonly in males (Table 1). The proximal attachment of the adductor brevis was entirely bone (to the pubic bone) in 59% (10/17) of specimens, whereas the remaining 41% (7/17) of specimens had bone and pubic symphysis capsular tissue attachments (Fig. 1). The proximal attachment of the adductor brevis was predominantly muscular, with no significant tendon seen. In specimens in which both the adductor longus and brevis attached to the pubic symphysis capsular tissues, the former attached more inferiorly in the anatomic position. MRI No athletes had undergone previous pelvic surgery, but three had experienced previous pubalgia. No athletes developed pubalgia within 6 months of MRI. The only discrepancy between the reviewing radiologists occurred when trying to differentiate a discrete adductor brevis tendon from the normal adjacent muscle fascia. Rectus abdominis The distal pyramidalis and rectus abdominis muscles and tendons were defined in all cases, with the rectus abdominis tendon lying deep in relation to the pyramidalis at the level of the superior pubis (Figs. 2 and 3). The rectus abdominis tendon was then seen to merge with the pubic symphysis capsular tissues and extend inferiorly in a sheet of tissue that was continuous with the origin of both adductor longus tendons. dductor group The adductor longus was defined as having a superficial tendon and deeper muscular component proximally in all cases (Fig. 3). t its attachment, the muscle and more superficial tendon were seen to merge with the pubic symphysis capsular tis- JR:188, May 2007

4 MRI of the Capsule of the Symphysis Pubis Fig. 3 Sagittal T1-weighted fast-field echo (TR/TE, 25/4.9) MR images in 29-year-old male athlete who had experienced previous pubalgia show normal anatomy., Image shows edge of fibrocartilaginous disk (D) with interdigitating hyaline cartilage and pubic bone (black arrowheads). nteriorly, capsular tissues (white arrowheads) merge with disk and rectus abdominis tendon (arrow). Pyramidalis is present anteriorly (asterisk)., Image lateral to shows pubic marrow and cortex (P) with thin layer of intermediate-signal hyaline cartilage (small arrowheads) closely applied to anterior capsular tissues (between large arrowheads). Merging with this tissue are rectus abdominis muscle (Rb), pyramidalis (asterisk), superficial adductor longus tendon (arrows), deeper muscle (L), and adductor brevis (r) muscle. C Fig. 4 xial T1-weighted fast-field echo (TR/TE, 25/4.9) spectral inversion recovery fat-suppressed IV gadolinium-enhanced MR images in 23-year-old male athlete who had experienced previous pubalgia show lateral adductor longus tendon insertion., Image at level just superior to pubic tubercle pyramidalis (small arrow) and rectus abdominis tendon (arrowhead) shows they are applied to capsular tissues. There is right-sided pubic bone marrow enhancement and edema (large arrows)., Image inferior in relation to and just inferior in relation to pubic tubercle shows adductor longus tendons (arrows) before attachment to tubercle. They have more lateral course in comparison with those in Figure 2. Rectus abdominis tendon is seen anteriorly (arrowhead). C, Image inferior in relation to shows rectus abdominis tissue (arrowheads) closely applied to anterior capsular tissues but also merging with adjacent adductor longus tendons (arrows). sues in all 10 cases, although in four cases, the tendon attached to the pubic tubercle at the lateral capsular margins with muscle lying more medially over the main capsular tissues (Figs. 2 and 4). proximal adductor brevis tendon could not be defined on MRI except in two cases in which a faint low-signal condensation was identified. The proximal muscle attached to the pubis in all cases and to the pubic symphysis capsular tissues inferiorly to the adductor longus in four cases (Fig. 3). The adductor magnus and gracilis attached to the pubis and JR:188, May 2007 inferior pubic ramus but did not merge with the pubic symphysis capsular tissues. Symphysis pubis MRI showed variation in the appearances of the pubic bones dependent on the athlete s age. n apophysis, with islands of enchondral ossification, applied across the anteromedial pubis was seen in all seven athletes who were under 21 years old, whereas this condition was not evident in the three athletes who were above this age (Fig. 5). When present, the apophysis extended from the anteromedial pubis to the lateral limit of the capsular tissues and was closely applied to the fibrocartilaginous disk, capsular tissues, and deeper subchondral bone. It was difficult to define the fibrocartilage disk as a distinct entity where it merged anteriorly with the capsular tissues. Laterally the disk was apposed by hyaline cartilage, and a primary cleft was seen in four of the athletes (ages, years) (Fig. 6). Where present, the areas of cartilage and ossification in the apophysis showed enhancement after gadolinium administration, with vessels extending from the subchondral pubis (Fig. 7). No other tissues showed significant enhancement. W443

5 Robinson et al. Moderate pubic bone marrow edema was seen in four of the athletes, three of whom had suffered from previous pubalgia (Fig. 4). Spurs, subchondral cysts, and cortical irregularity were seen in all athletes (Fig. 2). Discussion lthough the proximal attachments of the hip adductors to the pubic bone have been described, the symphyseal attachment of the rectus and adductor muscles to the pubic symphysis has not been previously presented to our knowledge. n earlier study found that the proximal adductor longus had superficial tendinous and deep muscular fibers proximally, but the exact attachment Fig year-old male athlete with no previous pubalgia who has normal apophysis., xial T1-weighted fast-field echo (TR/TE, 25/4.9) spectral inversion recovery fat-suppressed MR image shows lowsignal subchondral pubic cortex (large arrowheads) with intervening high-signal apophyseal cartilage and areas of enchondral ossification (small arrowheads) merging with capsular tissues and rectus abdominis tendon (arrow)., Sagittal T1-weighted fast-field echo (25/4.9) spectral inversion recovery fat-suppressed MR image lateral to disk shows pubis (P) still with covering of hyaline cartilage (large arrowhead) and low-signal enchondral ossification (between small arrowheads). nterior soft tissues consist of rectus abdominis (small arrow) and adductor longus tendons and fascia (large arrow). Fig year-old male athlete with no previous pubalgia who has primary cleft. xial T1-weighted fastfield echo (TR/TE, 25/4.9) spectral inversion recovery fat-suppressed IV gadolinium-enhanced MR image shows low-signal fibrocartilaginous disk (arrowhead) with high-signal cleft (arrow). Fig year-old male athlete with no previous pubalgia who has apophyseal enhancement. xial T1- weighted fast-field echo (TR/TE, 25/4.9) spectral inversion recovery fat-suppressed IV gadoliniumenhanced MR image shows enhancing vessels (arrows) extending from subchondral bone into apophyseal cartilage and ossification. sites in relation to the symphysis pubis were not examined [18]. In the current study, the proximal adductor longus was found to be divided into superficial tendinous and deep muscular parts on dissection and MRI. On tracing these structures proximally, the adductor longus was found to have attachments to the pubic bone and the pubic symphysis capsular tissues. On high-resolution MRI, the deep muscular and superficial tendinous components of the proximal adductor longus were best seen on sagittal images (Fig. 3). oth axial and sagittal images showed the adductor longus origin involving the symphyseal capsular tissues continuous with the rectus abdominis (Fig. 2). Variation was found in the symphyseal attachment site of the tendinous and muscular parts of the adductor longus. In 53% (9/17) of the cadaver specimens, both the tendinous and muscular parts attached to the pubic symphysis capsular tissues, whereas in the remaining 47% (8/17), only muscular parts had symphyseal attachments (Table 1). In four athletes, the capsular attachment was predominantly muscular with the tendon attaching to the pubic tubercle (Fig. 4). In the other six athletes, the tendon and muscle were more diffusely attached over the capsular tissues. The anatomic and MRI findings also concurred regarding the adductor brevis origin, which attached inferiorly to the adductor longus and also potentially involved the capsular tissues in 30 50% of cases. Previous anatomic texts and review articles have described a common aponeurosis overlying the anterior symphysis pubis [19, 20]. The cadaver and MRI findings for this study confirm continuation of the rectus abdominis tendon and aponeurosis around the anterior symphysis pubis. The tendon was also shown to be applied to the capsular tissues and fibrocartilage disk and to merge with the soft-tissue origin of the adductor longus (Figs. 1 3). These cadaver and MRI findings confirm that the symphysis pubis capsular structures and disk are intimately related to the anterior soft tissues, which receive contributions from the adductor longus, adductor brevis, and rectus abdominis tendons and muscles. This close anatomic relationship may explain why overuse injuries in this region can commonly produce diffuse symptoms radiating into the medial thigh and lower abdomen. The symphysis pubis is a nonsynovial amphiarthrodial articulation with hyaline cartilage lining the pubic bones and an intervening fibrocartilage disk. s weight-bearing forces are applied in infancy, a primary cleft develops in the disk, which is usually superior and posterior [16, 17] (Fig. 6). During growth, the apophyseal cartilage undergoes enchondral ossification with irregular islands developing resulting in ridges along the pubic subchondral surface [21] (Figs. 1, 2, and 5). natomic series have shown that with degeneration there is vascular ingrowth into the disk, and secondary clefts can develop between the disk, capsular tissues, and hyaline cartilage. These clefts can become synovial lined [17]. In athletes, MRI studies have not shown a clear relationship between presumed degenerative remodelling such as pubic spurs, sclerosis, irregularity, and cystic change with symptoms [8, 10, 12, 14]. In W444 JR:188, May 2007

6 MRI of the Capsule of the Symphysis Pubis this study these features were present in all the asymptomatic athletes. MRI series have found a number of changes that correlate with clinical symptoms but can also be seen in asymptomatic athletes [10 12, 22]. In one series, diffuse pubic bone marrow edema did correlate with symptoms, but a recent series has shown this is not a prognostic marker for subsequent development of pubalgia [6, 22, 23]. more reliable indicator seems to be localized subchondral edema and enhancement of the anteromedial pubis and adjacent capsular tissues [6, 12]. In this current study, the MRI findings in asymptomatic athletes showed this region to encompass the original pubic apophysis, capsular, and aponeurotic tissues of the rectus abdominis and adductor muscles. This junction of the pubis, apophysis, and soft tissues might be expected to represent an area of biomechanical weakness that endures considerable forces during athletic single-stance maneuvers. nother study reported a secondary cleft sign, which correlated with linear edema on MRI, and then extravasation of contrast material during symphysis pubis joint injection [11]. This feature could also be explained by overuse injury to this junctional area allowing extravasation from the disk into the disrupted anterior capsular and aponeurotic tissues. lthough microinstability at the pubic symphysis may account for changes around the symphysis seen in athletic pubalgia, our findings offer an alternative possibility. ttachments of the muscles to the capsule and therefore to the fibrocartilaginous disk indicate changes to the cartilaginous structures, including cleft formation along with adjacent bone marrow edema, that may occur by transmission of repetitive stresses from the muscle groups directly to the soft tissues. There are a number of limitations of this study compared with other anatomic and MRI studies. The cadavers were not in the athletic age group and included women, whereas the MRI evaluation only included asymptomatic male athletes. It was not considered relevant to perform MRI on cadavers or elderly agematched volunteers given the particular relevance of this condition in young male athletes. Logistically and ethically, it was not possible to obtain cadaver specimens of young athletes or to perform exact surgical correlation in asymptomatic athletes. Introducing currently symptomatic athletes before surgery could have biased the normal anatomy on MRI. In addition, the surgical procedures performed on these athletes are usually through small incisions targeting specific areas and thus do not allow global evaluation of the regional anatomy [8, 24]. The results of this study do not allow direct translation into the pathophysiology of pubalgia but do define the anatomic contributions to the area commonly seen as abnormal in the most recent MRI series of symptomatic athletes [6, 11, 12, 25]. This study defines the MRI anatomy of the symphysis pubis and anterior soft tissues. Cadaver and MRI findings show an intimate relationship between the anterior parasymphyseal soft tissues consisting of the adductor longus and rectus abdominis with the anteromedial symphyseal articular margins, fibrocartilaginous disk, and capsular tissues. This junctional area represents the center of abnormality detected in MR series of athletic pubalgia. cknowledgments The authors thank Paul rown and Valerie Oxorn for the artwork in Fig. 1D. References 1. Taylor DC, Meyers WC, Moylan J, Lohnes J, assett FH, Garrett WE Jr. bdominal musculature abnormalities as a cause of groin pain in athletes: inguinal hernias and pubalgia. m J Sports Med 1991; 19: Fredberg U, Kissmeyer-Nielsen P. The sportsman s hernia: fact or fiction? Scand J Med Sci Sports 1996; 6: Fricker P. Management of groin pain in athletes. r J Sports Med 1997; 31: Karlsson J, Sward L, Kalebo P, Thomee R. Chronic groin injuries in athletes: recommendations for treatment and rehabilitation. 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