– Written by Sonia Branci, Denmark and Philip Robinson, UK

Athletes involved in cutting- and kicking-movement sports are commonly affected by long-standing groin pain^1-3, which is a complex clinical condition resulting in significant morbidity. Establishing a radiological diagnosis is difficult, as the affected anatomical area is large and characterised by multiple possible aetiological factors that may act together in creating the overall symptom pattern⁴. Groin pain in athletes is now commonly investigated with conventional pelvic radiography, ultrasound and MRI largely replacing modalities that have been used extensively in the past (e.g. isotope bone scan and herniography⁵). The aim of this article is to provide readers with a brief overview of radiological groin anatomy, results from existing radiological studies and MRI protocols that are currently used for diagnostic assessment of athletes with long-standing groin pain.

RADIOLOGICAL ANATOMY OF THE ANTERIOR PELVIS

The pubic symphysis is a non-synovial, amphiarthrodial joint formed by both pubic bodies with an intervening fibro-cartilaginous articular disc. The medial surface of the body forms the articular surface and is ovoid, covered by hyaline cartilage with undulating transversely oriented ridges and grooves^6,7. The pubic apophysis is a relatively thin growth plate covering the anteromedial pubic body separated from the main body by cartilage. This gradually undergoes enchondral ossification and can fuse relatively late (up to mid-20s) appearing irregular on MRI, CT imaging and ultrasound normally because of variation in the degree of ossification (Figure 1)⁸. The pubic crest arises from the upper margin of the body and projects anteriorly and the pubic tubercle arises from the lateral aspect of the crest.

The joint is supported by four ligaments:

1. superior,
2. arcuate (or inferior),
3. anterior and
4. posterior pubic ligaments.

The pubic symphysis is also stabilised by several musculotendinous structures, which attach onto the anterior and superior aspect of the joint, its capsule and margins. These structures include the hip rotators, oblique abdominal, rectus abdominis and adductor group muscles, tendons and aponeuroses (Figures 1 and 2). Anatomically, these structures are continuous with the lower rectus abdominis sheath, also blending with the medial inguinal canal ligaments and aponeuroses. There is also prominent variation in the nerve supply to this region, which may explain the variety in presenting symptoms that can involve the medial thigh, perineum, lower abdomen and inguinal region. In males, it has been described that the medial half of each rectus abdominis continues distally in a ligament that runs over the anterior symphysis to confluence bilaterally with the gracilis and fascia lata⁹. This has been termed the recto-gracilis ligament while in females, the medial half of each rectus abdominis continues also as a ligament but inserts and terminates on to the antero-superior part of the symphysis. The fibres extending from the inguinal ligament also divide the anterior side of the pubis into a lower and upper half. In females this extension runs over the whole anterior side of the pubis and fibres from the left side merge with fibres from the right side. In males, these extensions do not cross the midline, being separated by the recto-gracilis ligament.

OVERVIEW OF PREVIOUS IMAGING STUDIES

Only few original radiological studies investigating groin pain in athletes exist in the scientific literature. Most of them are cross-sectional case or case-control studies. However, upon review, several radiological findings seem to consistently appear:

• degenerative changes at the pubic symphyseal joint,
• pathology at the adductor muscle insertions at the pubic bones,
• pubic bone marrow oedema (BMO),
• the secondary cleft sign and recently,
• the superior cleft sign.

Symphysis pubis

Degenerative changes at the symphysis consist of joint surface irregularities, subchondral sclerosis and cysts, joint space widening or narrowing and central disc herniation (Figure 3). Two radiographic studies^10,11 have reported a higher prevalence and severity of degenerative changes in symptomatic athletes compared with non-athletes, but changes were also visible in non-athletes and their prevalence increased with age. MRI studies have reported higher prevalences (20 to 98%) in symptomatic athletes compared with asymptomatic athletes (0 to 50%)¹².

Bone marrow oedema

BMO is evaluated on fluid-sensitive MRI sequences as diffuse increased signal intensity within the pubic bone marrow in relation to the symphysis (Figure 4). It has been investigated in several recent studies, as its presence has been suspected of correlating with the severity of athletic groin pain¹³. Available studies reported a prevalence of BMO ranging from 28 to 100% of athletes with long-standing groin pain¹². However, BMO was also found in 0 to 65% of asymptomatic athletes and one study reported BMO in 50% of a group of sedentary asymptomatic controls¹⁴. Thus, the significance of BMO in relation to symptoms is still unclear.

Adductor insertion

Pathology at the adductor muscle insertions has not been explicitly defined in any of the available studies. In several papers, adductor enthesis pathology has been evaluated as post-intravenous gadolinium enhancement of the adductor longus enthesis. Adductor tendinopathy may also be seen on MRI as increased signal intensity within the tendon on fluid-sensitive sequences and/or bulging of the adductor tendon (which is normally well-delineated and dark on both T1 and T2-weighted images) (Figure 5). The reported prevalence of adductor enthesis pathology with MRI varied from 46%¹⁵ of a group of recreational athletes and 71%¹⁶ of a group of symptomatic professional athletes with clinical adductor-related groin pain, but no control groups were included for comparison.

Cleft signs

The secondary cleft sign is a curvilinear area with the signal intensity of fluid extending inferolaterally from the inferior aspect of the symphysis on coronal MR images (Figure 6). It has been reported on the symptomatic side of 52%¹⁷, 67%¹⁸ and 88%¹⁹ of athletes with symphyseal groin pain in three MRI studies. Asymptomatic controls in these studies presented no secondary cleft sign, no matter whether they were athletes^18,19 or sedentary¹⁷. The significance of this secondary cleft is debatable, although authors have argued it may represent an indirect sign of a lesion at the adductor muscle attachment site to the pubic bone, indicating microtears in the symphyseal joint capsule. A recent study²⁰ has presented a new radiological sign, called the ‘superior cleft sign’. As opposed to the secondary cleft sign, this superior cleft sign is a line with the signal intensity of fluid that extends parallel to the inferior margin of the superior pubic ramus. It is located more anteriorly and superiorly than the secondary cleft sign, but is likewise interpreted as an indirect sign of a lesion/tear at the rectus abdominis/adductor longus attachment site, although this remains to be confirmed by further studies.

Overall, interpretation of the existing radiological literature on long-standing groin pain in athletes remains a challenging task. Current evidence is based on relatively few studies of varying methodological quality. The studies are heterogeneous in terms of their design (included sports, ages and sexes of study participants) and only few of them document their clinical examination findings, thereby preventing an accurate classification of clinical entities and diagnoses affecting study participants. Moreover, the existing diagnostic terminology is confusing and characterised by a general lack of consensus regarding radiological definitions and diagnostic criteria used by different authors (terms like ‘athletic pubalgia’, ‘osteitis pubis’ and ‘pubic instability’ are ill-defined and used interchangeably among authors). This confusion prevents a straightforward comparison between existing studies, which further complicates the interpretation of reported radiological findings. Even though MRI is commonly used for assessment of pathological changes in the groin area, there exists at present no standardised image evaluation protocol.

Similar problems in methodology affect the limited number of ultrasound studies performed in athletes with chronic groin pain. One study described adductor longus thickening as a sign of symptomatic adductor longus tendinopathy but this has not been reproduced in subsequent series²¹. Two other series have described inguinal canal ballooning (expansion of contents with a convex posterior wall) on straining with conflicting conclusions produced as to its clinical usefulness^22,23. The more recent study with a larger cohort found it to be an unreliable imaging finding (also see ultrasound of the inguinal canal section later).

IMAGING PATTERNS AND APPEARANCES IN LONG-STANDING GROIN PAIN IN ATHLETES

Conventional X-rays and CT do not typically add significant diagnostic information for athletes with long-standing groin pain²⁴. The ‘degenerative changes’ highlighted in the previous overview, pubic body/apophyseal irregularity, marginal spurring and sclerosis are common and non-specific in terms of current or previous symptoms. Herniography and isotope bone scans are now rarely performed with the latter, in particular, superseded by MRI. An overview of our imaging protocol is given in Table 1 with Figure 7 outlining the anatomical alignment for the oblique axial sequences. Relatively few protocols have gadolinium administered routinely and some institutions also include proton density sequences.

Pubic stress fracture

This is the least common condition to present in the spectrum of long-standing groin pain in athletes but is important to confirm as the prognosis for complete recovery (with rest) is much better than other causes. It typically occurs in younger and female athletes. As with a stress reaction elsewhere in the skeleton, MRI is the imaging modality of choice with a higher sensitivity compared to plain film and CT and increased specificity compared to isotope bone scanning (Figure 8). In addition there is no further radiation burden to this young patient group.

The spectrum of MR imaging findings range from stress reaction showing bone marrow oedema to full fracture showing cortical disruption and a low signal fracture line. It is particularly important with pubic stress injury to evaluate the rest of the pelvic ring (especially the sacrum) for concomitant injury which may alter the duration and type of rehabilitation programme.

MRI OF ATHLETES WITH LONG-STANDING GROIN PAIN

There is marked clinical overlap in terminology as shown in the previous overview and the clinical chapters in this issue. As highlighted, this has also spread into the terminology used in radiology studies of athletes with long-standing groin pain.

Oedema, be it in the pubic body bone marrow or parasymphyseal soft tissues, seems to be the most consistent finding in symptomatic athletes^19,25. A secondary cleft sign has also been described which is thought to be a partial soft tissue disruption at the junction of the symphysis pubis joint capsule and the adductor/rectus abdominis tendons and aponeuroses¹⁸.

Two patterns of pubic bone and parasymphyseal oedema are typically seen in elite soccer players.

Pattern 1

In this pattern which, in our experience seems to occur in younger soccer players (aged 14 to 18 years), MRI typically shows moderate to marked bone marrow oedema involving the majority of both pubic bodies and sometimes extending into the rami (Figure 9). There is often high signal fluid in the joint itself with soft tissue oedema diffusely parallel to the pubic bone cortices in the surrounding tendons and muscles fibres but no actual soft tissue disruption. This appearance is less common than the second pattern and differs from that typically seen in long-standing groin pain in athletes in that the oedema is more extensive (both in the bone marrow and soft tissues) and symmetrical (see below).

Pattern 2

This pattern is the most common seen on MRI, particularly in elite soccer players, and is much more localised in comparison to pattern 1. In this pattern, pubic bone marrow oedema is asymmetrical in that one side is affected more than another and can be much more focal with localisation to the subcortical bone marrow in the anteromedial pubis (Figure 4b). There is also oedema involving the adjacent anterior capsule, capsular ligaments and the enthesis of the common aponeuroses of adductor longus and rectus abdominis^18,19,25. These oedematous changes can commonly extend into the adductors inferiorly. Oedematous changes are visualised on the oblique axial T2-weighted images and on the coronal STIR (short tau inversion-recovery) images where the capsular and entheseal change has also been described as the secondary cleft sign when there is associated partial tearing of these capsular structures (Figures 6 and 10).

Occasionally, despite the use of modern scanners and coils, these changes are sometimes best appreciated as enhancement on post gadolinium sequences (Figure 11). This may be explained by the injury process at that time predominantly consisting of granulation tissue which, although not oedematous, is more vascular than normal capsular and entheseal tissue.

Similar to other modalities, symphyseal irregularity, spurring, fatty pubic marrow change, cysts and mild oedematous change are commonly seen in asymptomatic athletes and therefore of limited diagnostic use^25,26.

ULTRASOUND OF THE SYMPHYSIS PUBIS AND ENTHESIS

In our experience, ultrasound rarely adds positive information in this patient group as the osseous, capsular and entheseal oedema present on MRI is not visible on ultrasound. Pubic cortical irregularity is commonly seen and not discriminatory as it can represent the old apophyseal junction or normal degeneration (Figure 1). The obliquity of the adductor tendons also makes it difficult to assess subtle tendinopathy or thickening because of artefact (anisotropy). Although ultrasound is accurate for complete or partial adductor tears in acute injury these are rarely present in these athletes despite marked soft tissue oedema on MRI.

INGUINAL CANAL IMAGING

As already mentioned and highlighted elsewhere, clinical terminology and studies are not universally accepted or agreed. A number of clinical papers have highlighted inguinal canal disruption or dysfunction as a cause of long-standing groin pain in athletes but for the purposes of this article we will describe what abnormalities can be detected by imaging studies.

MRI of the inguinal canal

The inguinal canal and its surrounding muscles and aponeuroses are well-seen on MRI but in the authors’ experience are rarely abnormal in chronic athletic groin pain. Typically the inguinal walls do not show oedema or disruption in athletes with long-standing groin pain, even those with positive clinical signs in the inguinal region. Rarely, there may be acute disruption but this is always accompanied with the relevant history of acute injury rather than insidious onset. Asymmetry of the abdominal wall muscles is not discriminatory as muscular atrophy can occur after surgery or previous injury and is often asymptomatic. Another potential disadvantage of MRI is the lack of reproducible dynamic assessment during straining. However the specificity of ultrasound findings during straining is also not clear.

Ultrasound of the inguinal canal

Ultrasound of the inguinal canal is also usually normal in athletes with long-standing groin pain. Ultrasound is accurate for detecting true inguinal or femoral hernias but these are rare in athletes.

Abnormal posterior wall movement and canal content ballooning has been described in a previous study of Australian Rules footballers. Ballooning was defined as dilatation of the canal (in the sagittal plane) with convex bowing of the posterior wall²². The results suggested that this finding was more specific when it was bilateral and in older athletes. However overall this finding was not sensitive or specific for the entire group and was still present in some asymptomatic athletes after inguinal surgery. Subsequent ultrasound series in athletes and non-athletes have also shown this sign to be non-sensitive and non-specific²³.

CONCLUSIONS

Radiology studies have suffered in terms of the nomenclature and potential referrer clinical bias also seen in clinical studies of long-standing groin pain in athletes. Despite this, the main imaging findings that correlate best with current symptoms in this condition appear to be subjectively assessed moderate to marked oedema of the pubic bone marrow and parasymphyseal soft tissues or partial disruption of the soft tissues involving the anterior joint capsular, adductor and rectus abdominis tendons (‘cleft’). Other series in asymptomatic athletes have already shown that mild to moderate pubic bone marrow oedema in particular can occur normally^14,27. Thus more studies are required to validate the presence and severity of such findings in symptomatic and asymptomatic soccer players. Future imaging studies will also require more structured and rigorous assessment of player examination and symptoms to determine if imaging can have a role in helping differentiate the many clinical entities described. The same will apply for treatment evaluation with little evidence presented to date, using realistic control groups for rehabilitation, image-guided injection therapy and surgical interventions.

Sonia Branci M.D.

Department of Radiology, Rigshospitalet

Copenhagen University Hospital

Copenhagen, Denmark

Contact: sonia.branci.01@regionh.dk

Dr Philip Robinson M.B., Ch.B., M.R.C.P., F.R.C.R.

Consultant Musculoskeletal Radiologist,

Chapel Allerton Hospital,

Leeds, United Kingdom

Contact: philip.robinson@leedsth.nhs.uk

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Image via Jason Milich