Scand J Med Sci Sports 2013: ••: ••–•• doi: 10.1111/sms.12158

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Effect of pubic bone marrow edema on recovery from endoscopic surgery for athletic pubalgia L. Kuikka1, H. Hermunen2, H. Paajanen1 Department of Surgery, Kuopio University Hospital, Kuopio, Finland, 2Department of Radiology, Mikkeli Central Hospital, Mikkeli, Finland Corresponding author: Hannu Paajanen MD, PhD, Department of Surgery, Kuopio University Hospital, 70211 Kuopio, Finland. Tel: +358405263101, Fax: +358 17 173749, E-mail: [email protected]

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Accepted for publication 5 November 2013

Athletic pubalgia (sportsman’s hernia) is often repaired by surgery. The presence of pubic bone marrow edema (BME) in magnetic resonance imaging (MRI) may effect on the outcome of surgery. Surgical treatment of 30 patients with athletic pubalgia was performed by placement of totally extraperitoneal endoscopic mesh behind the painful groin area. The presence of pre-operative BME was graded from 0 to 3 using MRI and correlated to post-operative pain scores and recovery to sports activity 2 years after operation. The operated athletes participated in our previous prospective randomized study. The athletes with (n = 21) or without (n = 9) pubic BME had

similar patients’ characteristics and pain scores before surgery. Periostic and intraosseous edema at symphysis pubis was related to increase of post-operative pain scores only at 3 months after surgery (P = 0.03) but not to longterm recovery. Two years after surgery, three athletes in the BME group and three in the normal MRI group needed occasionally pain medication for chronic groin pain, and 87% were playing at the same level as before surgery. This study indicates that the presence of pubic BME had no remarkable long-term effect on recovery from endoscopic surgical treatment of athletic pubalgia.

The prevalence of chronic groin pain in physically active adults and athletes is between 5% and 10% (Swan & Wolcott, 2007; Nam & Brody, 2008; Litwin et al., 2011). Common causes for athletic pubalgia include tendinopathies from the adductor or rectus abdominis muscles, osteitis pubis associated with bone marrow edema (BME), or disruption of the posterior wall of inguinal canal (so-called sportsman’s hernia). Sometimes a multidisciplinary investigation may reveal more than one of these reasons for chronic groin pain (Smedberg et al., 1985; Paajanen et al., 2011b). Treatment of severe sportsman’s hernia (athletic pubalgia) is aimed toward its specific pathology. First-line management includes rest, muscle strengthening and stretching exercises, physiotherapy, anti-inflammatory analgesics, local anesthetic or corticosteroid injections, and, in resistant cases, operative management (Swan & Wolcott, 2007; Nam & Brody, 2008). Surgical approach includes various open techniques with or without polypropylene mesh, laparoscopic, or totally extraperitoneal techniques (Gilmore, 1991; Genitsaris et al., 2004; Lloyd et al., 2008; Meyers et al., 2008; Minnich et al., 2011; Paajanen et al., 2011b). Endoscopic treatment of chronic groin pain in athletes is a minimally invasive method to treat athletic pubalgia (Lloyd et al., 2008; Paajanen et al.,

2011b). Our previous prospective, randomized trial confirmed that surgical treatment was effective compared with non-operative treatment of athletic pubalgia (Paajanen et al., 2011b). In this study, 60 athletes with sportsman’s hernia and athletic pubalgia were randomized to conservative treatment or endoscopic surgery. Of the 30 athletes who underwent operation, 27 (90%) returned to sports activities after 3 months of convalescence compared with 8 (27%) in the non-operative group (P < 0.001). Various pubalgias at the site of insertion of the adductors, inguinal ligament, conjoint tendon, and rectus abdominis muscles may cause inflammation and subsequent BME in the pubic symphysis in magnetic resonance imaging (MRI) (Verrall et al., 2001; Lovell et al., 2006; Paajanen et al., 2008). Clinical significance of BME is somewhat obscure when operative treatment for athletic pubalgia is planned (Paajanen et al., 2008). In Australian rules footballers, the presence of BME at pubic symphysis was observed in 29 out of 57 asymptomatic players (Verrall et al., 2001). Furthermore, substantial amounts of BME at the pubic symphysis can occur in asymptomatic elite junior soccer players, but it is only weakly related to the development of clinical symptomatic osteitis pubis (Lovell et al., 2006). We and others (Daigeler et al., 2007; Paajanen et al., 2011a) have also previously reported that the MRI examination gives

ClinicalTrials.gov identifier: NCT00966589.

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Kuikka et al. no additional information within the training active period compared with the training-free interval in asymptomatic heavy-training athletes. Furthermore, the presence of BME is a frequent finding in contact sports of asymptomatic athletes (Lovell et al., 2006; Paajanen et al., 2011b), but MRI examination is also extremely useful for detection of symptomatic osteitis pubis (Daigeler et al., 2007). In the present analysis, 30 patients operated for athletic pubalgia from our previous randomized study were reviewed to investigate the role of BME in recovery from endoscopic surgery. Methods The original study was conducted between January 2007 and December 2009 in three hospitals (Paajanen et al., 2011b). In the present analysis, we included only the patients with surgical treatment. The detailed results of 30 patients treated non-operatively were not reported here. The outcome of operative treatment was re-evaluated after a mean follow-up of 24 ± 5 months in 2012. First author (L. K.) assessed the 2-year outcome. He was not the operating surgeon. Our aim was to study the role of BME on long-term recovery from surgery and its role in surgical decision making. Most athletes were at an elite level in national leagues or non-professionals who participated regularly in heavy training (Table 1). The clinical history, details in sports activity, power analysis, and inclusion and exclusion criteria were reported earlier (Paajanen et al., 2011b). The etiology and diagnosis of chronic groin pain was always based on patient history, physical examination, x-ray, and MRI. The location of pain had to be rostral to the

inguinal ligament in the deep inguinal ring at palpation with or without tenderness over the pubic symphysis. The athletes with or without BME in MRI were included in this study. Pain scores (range, 0–10) on a visual analog scale (VAS) during rest and training were carefully recorded pre-operatively and after 1, 3, 6, 12, and 24 months of surgery. Anatomical location of pain scores was asked rostral to the inguinal ligament in the deep inguinal ring and tenderness over the pubic symphysis. Pelvic roentgenograms and MRI studies of the groin region were obtained in all patients to rule out avulsion fractures or other musculo-skeletal abnormalities except sportsman’s hernia (athletic pubalgia) as described earlier. MRI (Siemens Harmony 1.0T, Erlangen, Germany) was performed using routine T1- and T2-weighted and short TI inversion recovery (STIR) sequences (Paajanen et al., 2008; Paajanen et al., 2011a). All abnormal changes in MRI including BME or an increased signal from the insertion of the adductor muscles were recorded (Verrall et al., 2001; Lovell et al., 2006). Pubic BME was graded as 0 (no edema), I (mild), II (moderate), or III (heavy; Fig. 1). MRI scans were reviewed independently by two investigators (one radiologist, one surgeon). A consensus was reached if there was a difference in the scan reports. Both axial and coronal images were evaluated to detect BME. Changes of BME on MRI were based on signal intensity within the bone marrow and the extent of intensity as described earlier (Verrall et al., 2001; Paajanen et al., 2011a). The regional extent of BME at the pubic symphysis was also estimated visually and by an image-processing tool; grade 0 (no increased signal), grade 1 (< 2 cm area at the pubic symphysis), grade 2 (> 2 cm area), and grade 3 (both rami of the symphysis pubic). Other abnormalities in MRI were also recorded (Paajanen et al., 2008). The ethics committee of our hospital approved the study protocol (Clinical Trials NCT00966589).

Table 1. Characteristics of patients with or without pubic bone marrow edema (BME) in magnetic resonance imaging

Number of patients (%)

Males Females Age (years, mean ± SD) Body mass index (kg/cm2, mean ± SD) Duration of symptoms (months, mean ± SD) Type of sport Soccer Running Ice hockey Floorball Others

Pubic BME (n = 21)

No BME (n = 9)

P

17 (81) 4 (19) 30 ± 8.5 24 ± 2.9 11 ± 8.0

8 (89) 1 (11) 28 ± 11 25 ± 3.3 17 ± 16

1.0000

10 (48) 3 (14) 1 (5.0) 3 (14) 4 (19)

4 (44) 3 (33) 1 (11) 0 1 (11)

1.0000 0.6244 0.5172 – 1.0000

0.5930 0.4129 0.1781

SD, standard deviation.

Fig. 1. Magnetic resonance images of pubic bone marrow edema (grade I = mild, grade II = moderate, and grade III = heavy).

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Pubic bone marrow edema in athletic pubalgia Table 2. Clinical information of the patients with or without pubic bone marrow edema (BME) in magnetic resonance imaging

Number of patients (%)

VAS* pain at rest (0–10, mean ± SD) VAS* pain at exercise (0–10, mean ± SD) Total physical impairment† Right-sided pain Left-sided pain Bilateral pain BME Grade I Grade II Grade III Adductor-related pain (tenotomy) Weakness of the posterior wall of inguinal canal

Pubic BME (n = 21)

No BME (n = 9)

P

2.8 ± 2.1 7.6 ± 1.0 15 (71) 6 (28) 5 (24) 10 (48)

2.9 ± 2.8 6.7 ± 1.8 6 (66) 2 (22) 4 (44) 3 (33)

0.9147 0.0886 0.6944 1.0000 0.3888 0.6908

10 (48) 8 (38) 3 (14) 4 (19) 8 (38)

0 0 0 2 (22) 9 (100)

– – – 1.0000 0.0033

*Means visual analog scale (VAS). † Means that the athlete was unable to participate in any sports. SD, standard deviation.

Operative treatment was performed by an endoscopic, total extraperitoneal (TEP) mesh placement behind the pubic bone and posterior wall of the inguinal canal. After dissection, the insertion area was covered with a 10 × 15-cm light polypropylene mesh (Optilene®, B. Braun, Melsungen, Germany), which was fixed with two to three staples (ProTack® stapler, Tyco Healthcare, Norwalk, Connecticut, USA). The staples were put to the aponeurosis of rectus abdominis, conjoined tendon, and Cooper’s ligament. Mesh was placed bilaterally even if the symptoms were unilateral because scarring of the preperitoneal space would most likely prevent a later operation of the non-affected side. Conventional non-steroidal anti-inflammatory drug or paracetamol were used for post-operative pain relief. All patients were evaluated after 1, 3, 6, 12, and 24 months. Recovery and return to sports activity was recorded by evaluating operative complications, preand post-operative pain scores (0–10) during rest and training, use of analgesics and time to resumption of low-level training, full training, and competing. Subjective outcome of athletes was asked and reported as excellent, good, moderate, or poor. The statistical analysis was carried out using Statistical Package for the Social Sciences for Windows, release 20.0 (IBM SPSS®, Chicago, Illinois, USA). Statistical evaluation was performed with Fisher’s exact test between the groups. The comparison between mean pain scores (VAS) was analyzed with Student’s t-test. P < 0.05 was regarded as significant for both tests.

Results All athletes had obscure chronic groin pain rostral to the inguinal ligament with a clinical diagnosis of sportsman’s hernia (athletic pubalgia). The pain area was either near the pubic insertion of inguinal ligament, nonspecifically in the lower abdominal wall, or tenderness of the pubis symphysis. Patient characteristics and the mean pain scores were similar in patients with and without BME at the pubis symphysis (Table 1). In both study groups, pain scores were much greater during exercise than at rest (Table 2). Patients with BME did not have bilateral pain more frequently (48%) than patients without BME (33%). The presence of BME was demonstrated as increased signal intensity on STIR sequences of MRI scans (Fig. 1). The BME was catego-

Fig. 2. Operative view of grade III pubic bone marrow edema. White * indicates pubic symphysis.

rized into three groups in MRI: 10 patients had grade I, 8 grade II, and 3 patients had grade III edema (Table 2). During operation, only grade III BME was observed as irritated, swollen periost of the pubic symphysis, but grades I and II BME were not associated with any visible abnormalities (Fig. 2). The mean pain scores at 3 months after surgery were a little bit higher in the BME group than in the non-BME group (P < 0.05). After 1 and 2 years this difference was not observed anymore (Fig. 3). In the original study group of 30 athletes treated non-operatively, the presence of BME did not effect on recovery from chronic groin pain during 2-year follow-up (data not shown). Seven of the patients initially treated conservatively underwent the TEP surgery during first year of follow-up; three of these patients had BME and four not [not significant (ns)]. Two-year follow-up revealed that three athletes in the BME group and three athletes in the non-BME group had occasionally chronic groin pain that needed pain

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Kuikka et al.

Fig. 3. Mean pre- and post-operative pain scores after endoscopic surgery in athletic pubalgia. White bars indicate the pain scores of patients with pubic bone marrow edema.

medication (Table 3). Some 87% of athletes returned to the same level of sport than before operation. Mean time to return to full sport was 1 month longer in the BME group than in the non-BME group (ns; Table 3). Two patients were re-operated because of recurrent severe groin pain. Both patients had femoroacetabular impingement syndrome. The initial MRI of hip region was normal in both cases. After 2 years of follow-up, patients in both study groups were equally satisfied with the endoscopic surgical treatment (Table 3). Open tenotomy was performed in six patients simultaneously with TEP surgery. All these patients were free of groin symptoms after 2-year follow-up. Four patients with tenotomy had BME and two not (Table 2). Discussion Chronic groin pain is a common presentation in sports medicine. It is most often a problem in those sports that

involve kicking and twisting movements. The main result of this study is that pubic BME observed in MRI has a minor or no effect on patient’s recovery after endoscopic surgery in sportsman’s hernia or athletic pubalgia. The mean pain scores after surgery were quite similar in the BME group compared with non-BME group although at 3 months after surgery the BME group had higher pain scores than non-BME group. The surgical treatment allowed good immediate and long-term relief of pain with low morbidity and fast recovery to full sports activity. Macroscopic swelling of the pubic symphysis in the BME group was clearly seen during operation (Fig. 2), although in the previous study we did not recognize this operative view significant (Paajanen et al., 2011b). The pubic abnormal changes observed in MRI, such as edema in the pubic symphysis or adjacent tendons, had little impact on the long-term operative outcome. Tenotomy performed with TEP surgery did not effect on 2-year outcome of patients. Weakness of our study was that we included only 30 surgically treated athletes in the present post-hoc analysis. This means that our study was to some extent underpowered having type 2 error. Power calculation of our original manuscript indicated that 50–60 athletes are needed to prove that surgical treatment is more effective than conservative treatment in athletes’ pubalgia (Paajanen et al., 2011b). The impact of BME on recovery was not totally negative as the prolonged pain effect of BME was observed at 3 months post-operatively. This indicates that BME can have some minor effect on recovery at the early post-operative period, but late results (after 1–2 years) were negative. The other shortcoming was that our study included many variables related to treatment (tenotomy, gender, different sports, etc.) to compare small study groups. In clinical prospective, controlled study like ours, it is difficult to catch many athletes with pubalgia and negative MRI because MRI is so sensitive to depict edema. In the present study, we excluded many variables such as edema outside

Table 3. Outcome analysis after 2 years of endoscopic operation

Number of patients (%) Pubic BME (n = 21) Pain medication Return to sport At same level At lower level Finished Time to return to full sport (months, mean ± SD) Re-operations to groin pain Operative outcome Excellent Good Moderate Poor BME, bone marrow edema; SD, standard deviation.

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No BME (n = 9)

P

3 (33)

0.3287

19 (91) 0 (0) 2 (9.5) 3.7 ± 2.4 1 (5.0)

7 (78) 1 (11) 0 2.3 ± 0.8 1 (11)

0.5632 0.3000 1.0000 0.1011 0.5172

16 (76) 3 (14) 1 (5.0) 1 (5.0)

7 (78) 2 (22) 0 0

1.0000 0.6220 1.000 1.000

3 (14)

Pubic bone marrow edema in athletic pubalgia pubic bone. The goal of the present study was to investigate the long-term effects and relationship of BME on recovery of patients in our randomized controlled trial study (Paajanen et al., 2011b), and we did not want to include more patients with or without BME in this analysis. Chronic groin pain in athletes often has multiple etiologic factors. The most commonly used theories include adductor and/or rectus abdominis muscle tendinopathies, hip hyperextension injuries, or disruption of the posterior wall of inguinal canal (Gilmore, 1991; Lloyd et al., 2008; Meyers et al., 2008). In athletic pubalgia, physical examination elicits tenderness in the inguinal region rostral to inguinal ligament and around pubic symphysis. Posterior weakness of the inguinal canal (“sports hernia”) is only one component of a chronic groin injury that may include BME in MRI. The other components of athletic pubalgia are conjoint or adductor tendinopathies or osteitis pubis. Thus, the etiology of athletic pubalgia may be diverse, but the common clinical factor is debilitating groin pain that may place an athletic career at risk. There is no evidence-based consensus available to guide decision making in the need for operative treatment of athletic pubalgia (Swan & Wolcott, 2007). Without a clear clinical and pathological diagnosis, the subsequent management of chronic groin pain is difficult. Open and laparoscopic repairs produce good results; the latter may allow earlier return to full sport (Genitsaris et al., 2004; Lloyd et al., 2008; Paajanen et al., 2011b), but comparative studies between open and laparoscopic procedures in athletic pubalgia do not exist. Laparoscopic repair of chronic pubalgia particularly in athletes has many theoretic advantages. The posterior position of mesh behind the conjoint tendon and pubic bone creates theoretically a stronger support than conventional anterior hernioplasty. Furthermore, the preperitoneal technique is less invasive than open techniques. Post-operative pain and wound complications are less frequent after laparoscopic surgery than in open surgery. A novel, open, minimal repair technique may be a promising method to repair sportsman’s groin and challenge endoscopic techniques (Minnich et al., 2011). The origin of BME is presently speculative and obscure. Some reasons can be repetitive stress reaction of periost and attached tendons or subenthesial from avulsive forces. This is supported by the fact that the presence of BME is evident in athletes without pubalgia as well (Lovell et al., 2006). We think that osteoarthritis is a rare reason for athletes BME because most patients are rather young. Subchondral BME in a pattern reminiscent of osteoarthritis is the hallmark MRI finding of osteitis pubis (Mullens et al., 2012). Clinically, osteitis pubis is characterized by diffuse pain, inflammation, and bony changes in the pubic symphysis. We think that an abnormality of the conjoint tendon (Nam & Brody, 2008), tendinopathy of inguinal ligaments (Lloyd et al.,

2008) and, in some patients, incipient osteitis pubis (edema in the pubic bone) (Verrall et al., 2001) may be a manifestation of the same disease entity, i.e., repetitive strain injury or acute disruption of the musculotendinous complex attached to the pubic tubercle. MRI is a highly sensitive diagnostic tool of BME. Pubic edema is not always associated with clinical symptoms and pain because many recent studies with asymptomatic soccer or hockey players have BME in MRI (Lovell et al., 2006; Paajanen et al., 2011a; Silvis et al., 2011). Thus, in many cases increased BME itself is not a contributor to pain. The relevance of BME in the symphysis pubis is of questionable importance when operative treatment is planned for athletic pubalgia. More controlled studies are needed to explore the role of BME in pubic pain reaction. In 2-year follow-up, we had two recurrences of sportsman’s hernia (athletic pubalgia). Both patients had first medially located groin pain typical for “sports hernia.” After surgical repair, immediate recovery was good, but later more lateral hip pain was observed. Both patients had femoroacetabular impingement and they were re-operated by hip arthroscopy. The original MRI of hip joint was normal and clinical examination did not suggest any femoroacetabular injuries. Flexion, inner rotation, and adduction of hip joint were initially normal in both patients. The combination of complex anatomy in the groin area, variability of presentation, and the non-specific nature of the signs and symptoms make the diagnostic process sometimes problematic (Falvey et al., 2009; Larson et al., 2011). It has been recently stressed out that in some patients with athletic pubalgia, both hip and pubic regions are chronically injured. When surgery is addressed only either the athletic pubalgia or the intraarticular hip pathology in this patient population, outcome is suboptimal. Surgical management of both disorders concurrently or in a staged manner leads to improved post-operative outcome scoring and an unrestricted return to sporting activity (Larson et al., 2011). It was also found in the present study that six athletes (20%) used occasional pain medication for groin pain during exercise. This may indicate that the athletes with sportsman’s hernia are more vulnerable to recurrent groin symptoms in the long-term follow-up. To conclude, once the diagnosis of sportsman’s hernia (athletic pubalgia) with or without BME is confirmed and conservative treatment fails, surgical treatment is an efficient method to help patient. In non-professionals, our policy is to wait 4–6 months before suggesting the operative treatment. The proposed operation must fit the patients’ symptoms and signs. The role of MRI is diagnostically useful to exclude other marked pathology of groin region (e.g., tumors, muscle rupture, various bursitis, impingement, or pre-arthrosis of hip joint). The presence of BME had minimal or no effect on recovery from surgery and should not be used as the sole indication or non-indication for operative treatment. It is

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Kuikka et al. necessary to confirm our results with the prospective study of large number of patients to avoid type 2 error.

presence of BME in MRI does not predict a failure in surgical treatment. Key words: Sports hernia, groin pain, sportsman’s hernia, osteitis pubis, surgical treatment.

Perspectives Surgery is not the first-line treatment of athletic pubalgia, but in resistant cases endoscopic surgery heals 90% of athletes with intractable pubalgia. About 70% of athletes suffering from sportsman’s hernia or athletic pubalgia have pubic BME in MRI. The

Author contribution LK: Collecting and analyzing data. HH: Analysis of magnetic resonance images. HP: Planning and conduct, and responsible for the overall content as quarantor, operating surgeon.

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Effect of pubic bone marrow edema on recovery from endoscopic surgery for athletic pubalgia.

Athletic pubalgia (sportsman's hernia) is often repaired by surgery. The presence of pubic bone marrow edema (BME) in magnetic resonance imaging (MRI)...
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