Accepted Manuscript Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review Michael K. Drew, Peter G. Osmotherly, Pauline E. Chiarelli PII:
S1466-853X(13)00106-5
DOI:
10.1016/j.ptsp.2013.11.002
Reference:
YPTSP 582
To appear in:
Physical Therapy in Sports
Received Date: 17 October 2012 Revised Date:
20 September 2013
Accepted Date: 6 November 2013
Please cite this article as: Drew, M.K, Osmotherly, P.G., Chiarelli, P.E., Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review, Physical Therapy in Sports (2013), doi: 10.1016/j.ptsp.2013.11.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Title: Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review. Authors:
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Michael K Drew a b Peter G. Osmotherly a Pauline E. Chiarelli a Institution and affiliations: a
Department of Physiotherapy, School of Health Science, University of Newcastle University Drive, Callaghan, NSW 2308 Australia Department of Physical Therapies, Australian Institute of Sport, Leverrier Cr, Bruce ACT 2617 Australia
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Corresponding author: Name Michael Drew Department Department of Physical Therapies Institution Australian Institute of Sport Address c/o Physical Therapies, Leverrier Cr, Bruce, ACT 2617 Country Australia Tel 02 62141766 (work) Mob +61416048448 Fax +61 26214 1603 Email [email protected]; [email protected]
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Email addresses of co-authors: [email protected]; [email protected]
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Title: Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review of pubic-related structures
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Objectives: To examine the validity of clinical tests and investigations available for the
7
diagnosis of long-standing groin pain in athletes. Design: Systematic review Method: A
8
published search strategy of MeSH terms in MEDLINE, CINAHL, EMBASE, and
9
SportDiscuss. Inclusion criteria: diagnostic studies relating to athletic groin pain, professional or
10
semi-professional athletes, symptoms lasting for more than six weeks, and not limited by age or
11
gender. A priori exclusion criteria were utilised. Outcome Measures: QUADAS tool,
12
sensitivity and specificity, likelihood ratios and predictive values of the reported tests and
13
investigations Results: 577 journal articles were identified. Five studies met all requirements.
14
Sensitivity and specificity of clinical tests ranged between 30-100% and 88-95% respectively
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with negative likelihood ratio of 0.15-0.78 and positive likelihood ratios of 1.0-11.0. Sensitivity
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and specificity of investigations (MRI, herniography, and dynamic ultrasound) ranged between
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68-100% and 33-100% respectively with negative likelihood ratios between 0-0.32 and positive
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likelihood ratios between 1.5-8.1. Conclusion: There is a lack of validated diagnostic clinical
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tests available for clinicians and a lack of symptomology being evaluated. It is recommended
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that a reference standard be used and data be reported in sufficient detail to calculate
21
diagnostic statistics that will be of use to the clinician.
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ABSTRACT
Key words: Groin, athletic injury, diagnosis, systematic review
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INTRODUCTION Groin injuries are common in sports that require cutting and sprinting manoeuvres such as
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soccer, rugby league, rugby union, cricket, ice hockey and Australian Rules football (Brown et
29
al., 2008; O'Connor, 2004; J. Orchard, James, Alcott, Carter, & Farhart, 2002; J. Orchard &
30
Verrall, 2000; Verrall, Slavotinek, & Fon, 2001; Werner, Hägglund, Walden, & Ekstrand,
31
2009). They account for between 4% and 16% of all injuries each season (J. Orchard & Verrall,
32
2000; Werner, et al., 2009) and have an estimated incidence of 0.59-3.5 injuries per 1000 hours
33
of activity (Ekstrand & Hilding, 1999; J. Orchard & Verrall, 2000; Werner, et al., 2009). Groin
34
injuries have a high recurrence rate, reported between 15% and 31% (Werner, et al., 2009). In
35
Australian Rules Football they are the second most common injury behind hamstring muscle
36
strains and have been estimated to be responsible for 11 to 18 competition games per team being
37
missed by players due to injury in a season (J. Orchard & Verrall, 2000). Confusion regarding
38
the clinical presentation of groin pain and inadequate differential diagnosis of groin pathology is
39
likely to result in inappropriate management and consequently ongoing pain or re-injury for the
40
injured athletes.
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The hip joint is a potential source of groin pain and is associated with the development of long-
43
standing groin pain in athletes (C. J. Bradshaw, Bundy, & Falvey, 2008). Sacroiliac joint (SIJ)
44
pathology and degeneration seen on plain X-Ray is also associated with long-standing groin
45
pain (LGP) (Harris & Murray, 1974; Major & Helms, 1997). Entrapment of the obturator nerve
46
has been diagnosed and described in athletic populations with long-standing groin pain (C.
47
Bradshaw & Holmich, 2006; C. Bradshaw, McCrory, Bell, & Brukner, 1997; C. J. Bradshaw, et
48
al., 2008; Brukner, Bradshaw, & McCrory, 1999). Tearing of the external oblique muscle
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aponeurosis has frequently been described in hockey players and has been associated with
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ilioinguinal nerve entrapment (Irshad et al., 2001).
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Within the medial thigh compartment, the adductor longus muscle is commonly implicated in
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long-standing groin pain (Albers, Spritzer, Garrett Jr., & Meyers, 2001; Renstrom & Peterson,
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1980; Robinson et al., 2004). It has been hypothesised that the forces created by the rectus
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abdominis and adductor longus muscles control the shearing force across the anterior pubic arch
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and pubic symphysis (Meyers, Greenleaf, & Saad, 2005). Disruption of this equilibrium is likely
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to impact on these shearing forces. This can occur in adductor longus enthesopathies and rectus
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abdominis tendinopathies, as diagnosed via MRI (Robinson, et al., 2004; Zoga et al., 2008).
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Neutralising these forces surgically by either reinforcing the rectus abdominis enthesis or
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performing an adductor longus tenotomy has been shown to improve function (Meyers, Foley,
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Garrett, Lohnes, & Mandlebaum, 2000; Meyers et al., 2008).
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The inguinal canal is frequently injured and can also exhibit dysfunction under load in athletes
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(Cohen, Turkenburg, & van Dalen, 1990; Kesek, Ekberg, & Westlin, 2002; Smedberg, Broome,
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Gullmo, & Roos, 1985; Taylor et al., 1991; Yilmazlar, Kizil, Zorluoglu, & Ozguc, 1996).
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“Sportsman’s hernia” or posterior inguinal wall deficiency occurs when the posterior wall
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bulges under increased abdominal pressure (J. W. Orchard, Read, Neophyton, & Garlick, 1998).
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It has been reported that direct hernias account for over half of hernias in athletes and can occur
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in combination with indirect hernia and posterior wall weakness (Smedberg, et al., 1985).
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Contradicting this, a later study found unilateral indirect hernias to be the most common type of
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hernia in athletes with longstanding groin pain (Yilmazlar, et al., 1996). Femoral hernias are
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rare in this population (Robinson, et al., 2004; Yilmazlar, et al., 1996).
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It is important to note that many diseases and conditions of non-musculoskeletal origin may
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refer symptoms to this region. These include gynaecological, urological, malignancies, sexually
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transmitted and rheumatological conditions (C. Bradshaw & Holmich, 2006; Ekberg, Persson,
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Abrahamsson, Westlin, & Lilja, 1988; Harris & Murray, 1974; Smedberg, et al., 1985). It is
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therefore important to consider a multidisciplinary approach to both diagnosis and treatment of
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long-standing groin pain in athletes. Additionally, other factors may also influence the patient’s
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experience and outcome from the injury. These include the emotional, social or cognitive in
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origin and should be considered in a biopsychosocial assessment framework. It is therefore
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important to consider a multidisciplinary approach which includes physical and psychological
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aspects to both the diagnosis and treatment of long-standing groin pain in athletes.
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Several approaches to the diagnosis of LGP have been proposed including patho-anatomical
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models (Falvey, Franklyn-Miller, & McCrory, 2008) and the clinical entity approach (Holmich,
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2007). Physical examination can be reliable (Holmich, Holmich, & Bjerg, 2004; Malliaras,
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Hogan, Nawrocki, Crossley, & Schache, 2010) however, while reliable many tests have not
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been evaluated for their diagnostic accuracy. Physical tests have been used to classify groin pain
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into three main pathological entities; adductor-related, iliopsoas-related and rectus abdominis
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related dysfunctions. Holmich et al (2007) studied 207 athletes and found 119 (57.5%) had
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adductor-related dysfunction as their primary entity followed by iliopsoas-related (36%) and
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rectus abdominis-related (10%) dysfunctions. Notably, multiple pathologies were found in 69
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(33%) patients, with 16 (7.7%) having all three pathological entities and rectus abdominis-
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related dysfunction rarely occurring in isolation (Holmich, et al., 2004).
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Falvey et al. (2009) systematically considered the anatomical structures that are located within
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or around the “groin triangle”. Structures were classified by their region; pubic tubercle region,
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medial to the triangle, superior to the base, lateral to the triangle and within the triangle. This
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systematic approach allows the clinician to consider all the structures potentially implicated.
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This patho-anatomical approach provides an intuitively meaningful framework when diagnosing
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the source of LGP, the clinical entity approach as demonstrated by Hölmich et al. (2004) has
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merit when considering conservative clinical examination and treatment options.
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However, a lack of evaluation of clinical tests for the purpose of diagnosis is evident.
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There may be several reasons for this; poor consensus on pathology and terminology,
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lack of specific tests implicating individual structures, absence of an accepted and
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available reference standard against which test performance may be assessed. The
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complexity of this region with its overlapping anatomy and interdependence of structure means
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that a specific tests and/or imaging is challenging to develop and difficult to evaluate. There is
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also a deficiency of literature on the symptomology of athletes with longstanding groin pain
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with reference to diagnoses.
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The purpose of this review is to evaluate the current literature pertaining clinical tests,
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symptomology and investigations available to the clinician working with athletes with
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longstanding groin pain and to examine their validity.
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METHODS
A search was performed using published strategies for searching diagnostic studies (Deville et
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al., 2002). Databases searched included MEDLINE, CINAHL, EMBASE, and SportDiscuss (to
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August 2009) using the MeSH terms: groin, athletic injuries, abdominal muscles, sportsm* and
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hernia, abdominal pain, pelvis pain, athletic pubalgia, pubalgia, rheumatic diseases,
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enthesopathy, inguinal canal, hockey groin syndrome, Gilmore’s groin, adductor longus, rectus
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abdominis, pubic bone, pubic symphysis, enthesis, osteitis pubis, pain, adductor related,
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inguinal hernia, abdominal wall hernia, groin pain, tendinopathy, posterior inguinal wall
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deficiency, and enthesitis. Results were limited to “human” and the English language. Reference
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lists from retrieved studies were examined for any studies not retrieved by the database
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searches. One investigator (MD) screened the titles and abstract of studies without blinding to
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results, authors or journals.
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For studies to be included in the review, they had to pertain to the diagnosis of long-standing
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groin pain (symptoms lasting more than six weeks) in professional or semi-professional athletes
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across any sport, not limited by age or gender and could be of any investigation type. Studies
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had to include enough data to allow derivation of sensitivity and specificity if it had not been
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reported in the paper. A priori exclusion criteria included: articles on treatment without
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describing the diagnostic methodology, if data on sensitivity and specificity data was unreported
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and could not be derived, studies not using a reference standard, hip related groin pain studies
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since this systematic review concentrates on the structures around the pubic area that can cause
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pain, case studies, case series, reviews, prognostic studies, letters, comments and cadaver
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studies. Two investigators (MD, PC) independently assessed the eligibility of the studies for
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inclusion in the review. Discrepancies were settled by discussion and if a consensus could not
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be reached a third investigator (PO) adjudicated. See Box 1 for the review outline.
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Methodological quality of the diagnostic papers were judged using the QUADAS tool (Whiting,
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Rutjes, Reitsma, Bossuyt, & Kleijnen, 2003). This tool has been modified and used in a
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previous systematic review of groin pain (Jansen, Mens, Backx, & Stam, 2008). Articles are
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scored as “yes”, “no” or “unclear” across 14 criteria. The QUADAS tool does not recommend
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to calculate a score as this has no consideration for the individual quality of the item and may
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introduce potential biases and therefore missing potential associations (Whiting, et al., 2003).
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The QUADAS tool criteria are 1.Was the spectrum of patients representative of the patients
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who will receive the test in practice? 2. Were selection criteria clearly described? 3. Is the
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reference standard likely to correctly classify the target condition? 4. Is the time period between
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reference standard and index test short enough to be reasonably sure that the target condition did
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not change between the two tests? 5. Did the whole sample or a random selection of the sample,
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receive verification using a reference standard of diagnosis? 6. Did patients receive the same
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reference standard regardless of the index test result? 7. Was the reference standard independent
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of the index test (i.e. the index test did not form part of the reference standard)? 8.Was the
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execution of the index test described in sufficient detail to permit replication of the test? 9. Was
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the execution of the reference standard described in sufficient detail to permit its replication?
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10. Were the index test results interpreted without knowledge of the results of the reference
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standard? 11. Were the reference standard results interpreted without knowledge of the results
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of the index test? 12. Were the same clinical data available when test results were interpreted as
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would be available when the test is used in practice? 13. Were un-interpretable/ intermediate
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test results reported? 14.Were withdrawals from the study explained? The specificity,
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sensitivity, predictive value and likelihood ratios were also assessed and calculated from the
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published data where they were not reported.
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RESULTS
The database search retrieved 577 journal articles of which five met the inclusion criteria.
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Figure 1 indicates the flow of studies. Results of the QUADAS tool evaluation are presented in
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Table 1. The compliance to individual items in the QUADAS tool varied with all studies
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compliant with items 1, 3, and 7. Items 6, 11 and 14 had the poorest compliance with only one
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study per item satisfying the relevant measurement.
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Figure 1. Flow of studies through the review.
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Table 1. Compliance of individual studies with items of the QUADAS tool
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The five studies considered six different pathologies with four physical assessments and five
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diagnostic imaging techniques being evaluated. This is summarised in Table 2. Three of the five
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included studies reported multiple pathologies in athletes with LGP (Brennan et al., 2005;
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O'Connell, Powell, McCaffrey, O'Connell, & Eustace, 2002; Zoga, et al., 2008). Table 2
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summarises the information from the patient interview. None of these findings were compared
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to the reference standard. Table 2 provides a summary of the data for each test including
185
sensitivity, specificity, likelihood ratios and predictive values. Sensitivity of diagnostic imaging
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ranged from 68% to 100%. The sensitivity of physical assessments was lower (30-86%) with
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the exception of palpation of inguinal hernias which, in a small sample, had a sensitivity of
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100%. Specificity of diagnostic imaging ranged from 0-100% and physical assessments had a
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specificity of 88-100%. With the exception of MRI of adductor tendon pathology (+LR=8.07; -
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LR 0.15) and “bilateral adduction” (+LR=11.0), the tests evaluated in this systematic review
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would fail to substantially increase the post-test probability of the diagnosis under question.
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DISCUSSION While accurate and timely diagnosis of long-standing groin pain is imperative for professional
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athletes, a diagnostic test, even with good diagnostic statistics, is only important if it impacts
196
positively on the outcome of the patient (Ferrante, Hyde, McCaffery, Bossuyt, & Deeks, 2012).
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It is unknown whether the tests highlighted in this systematic review improve either treatment
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choices or outcomes. However, as multiple structures can be implicated diagnosis can be
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difficult. Many of the clinical assessments used by sports physicians and physiotherapists have
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not been evaluated against a reference standard. The results from this systematic review reflect
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the lack of validation of clinical tests in current use. This is reflected by the fact that only five
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studies met our a priori inclusion criteria. Currently there has been no cost benefit analyses
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undertaken related to diagnostic imaging in this population. Future studies may be warranted.
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Reports from athletes with LGP during patient interview can give insight into the pathology
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(Harris & Murray, 1974; Kunduracioglu, Yilmaz, Yorubulut, & Kudas, 2007; Major & Helms,
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1997; J. W. Orchard, et al., 1998; Smedberg, et al., 1985; Verrall, Slavotinek, Barnes, & Fon,
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2005). However, such reported symptoms are not exclusive to any particular pathology and
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have not been evaluated against a reference standard. This is an area for future research.
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Clinicians can be confident in the reliability of clinical assessment of patients with LGP (Hogan
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& Lovell, 1997; Holmich, et al., 2004; Malliaras, et al., 2010; Slavotinek, Verrall, Fon, & Sage,
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2005; Verrall, et al., 2005). However, there needs to be a clear delineation between tests that are
213
clinically useful and those who have been evaluated for their diagnostic accuracy. Verrall et al
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(2005) examined three resisted adduction pain provocation tests on Australian Rules footballers
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with and without groin pain. These athletes subsequently underwent MRI of their groin region.
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In the presence of all three positive pain provocation tests there is a high likelihood of having
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pubic bone marrow oedema (BMO) detected by MRI. Tenderness on the symphysis pubis
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and/or superior pubic rami in addition to the three positive provocation tests further improves
219
the predictive ability of the examination(Slavotinek, et al., 2005; Verrall, et al., 2005). This
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provides useful guidelines in the clinic if BMO is suspected and MRI is unavailable.
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221 Whilst clinically useful assessments have been published which can assist the clinician in the
223
management of the long-standing groin pain, these were excluded from the systematic review as
224
they failed to meet the inclusion criteria for assessment against a reference standard. Clinically
225
useful measures such as strength of the “squeeze test” (isometric adduction in crooked lying) are
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both clinically and statistically significantly less in athletes with long-standing groin pain
227
(Malliaras, et al., 2010) but this may not be entirely related to adductor pathology (Mens,
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Inklaar, Koes, & Stam, 2006). Lovell et al (2012) evaluated six clinical tests for the adductors.
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Their findings showed that the tests cannot discriminate between the muscles that form the
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adductor group(G. A. Lovell, Blanch, & Barnes, 2012). Mens et al. (2006) applied a pelvic belt
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and increased the strength of adduction and decreased difficulty in lower limb tasks (Mens, et
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al., 2006) indicating that there is either reflex inhibition occurring and/or an inability to stabilise
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the pelvic ring when transferring loads from the lower limbs across the SIJ to the spine. This
234
suggests that there may be multiple co-existing pathologies and conditions and the examiner
235
should consider the entire lumbo-pelvic-hip complex prior to diagnosis. Mens et al. (2006) did
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not describe whether there was tenderness over the adductor enthesis and/or pubic symphysis, a
237
common finding in athletes with adductor-related longstanding groin pain (Robinson, et al.,
238
2004; Schilders et al., 2007). This may guide the clinician in deciding the value of applying the
239
pelvic stabilisation test. Pain in the groin without adductor entheseal/pubic bone tenderness is
240
considered a separate entity (Verrall, et al., 2001). Palpation was included in the cluster of
241
fourteen clinical tests proposed by Hölmich, Hölmich and Bjerg (2004). Hölmich et al (2004)
242
was excluded from this systematic review as it did not have a reference standard and therefore
243
did not evaluate the diagnostic ability of the described tests. Their recommendation for
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assessing athletes with groin pain included palpation, stretching, pain provocation and strength
245
tests. Good reliability and inter-observer agreement (κ>0.60) was achieved between examiners
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for 11 of 14 tests. While clinically useful in assessment and reassessment, these findings do not
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definitively diagnose the source of groin pain in the athletes. Zoga et al. (2008) utilised physical
248
assessment results as a reference standard in their study. Unfortunately the details of these
249
assessments were not reported.
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This systematic review highlights that MRI can be used as part of the diagnostic procedure.
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Abnormalities of the anterior pubis and adductor enthesis on MRI have been shown to
253
correspond to the side of presenting symptoms (Robinson, et al., 2004). Oedema in pubic bone
254
marrow, pubic symphysis and periarticular region is associated with an earlier stage of injury
255
(Kunduracioglu, et al., 2007). Subchondral sclerosis and resorption, symphysis pubis margin
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irregularities and tendon injuries to the adductors, iliopsoas and gluteus maximus have a
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significant correlation (p
S1466-853X(13)00106-5
DOI:
10.1016/j.ptsp.2013.11.002
Reference:
YPTSP 582
To appear in:
Physical Therapy in Sports
Received Date: 17 October 2012 Revised Date:
20 September 2013
Accepted Date: 6 November 2013
Please cite this article as: Drew, M.K, Osmotherly, P.G., Chiarelli, P.E., Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review, Physical Therapy in Sports (2013), doi: 10.1016/j.ptsp.2013.11.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Title: Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review. Authors:
RI PT
Michael K Drew a b Peter G. Osmotherly a Pauline E. Chiarelli a Institution and affiliations: a
Department of Physiotherapy, School of Health Science, University of Newcastle University Drive, Callaghan, NSW 2308 Australia Department of Physical Therapies, Australian Institute of Sport, Leverrier Cr, Bruce ACT 2617 Australia
SC
b
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M AN U
Corresponding author: Name Michael Drew Department Department of Physical Therapies Institution Australian Institute of Sport Address c/o Physical Therapies, Leverrier Cr, Bruce, ACT 2617 Country Australia Tel 02 62141766 (work) Mob +61416048448 Fax +61 26214 1603 Email [email protected]; [email protected]
AC C
EP
Email addresses of co-authors: [email protected]; [email protected]
ACCEPTED MANUSCRIPT
1 2 3 4 5
Title: Imaging and clinical tests for the diagnosis of long-standing groin pain in athletes. A systematic review of pubic-related structures
6
Objectives: To examine the validity of clinical tests and investigations available for the
7
diagnosis of long-standing groin pain in athletes. Design: Systematic review Method: A
8
published search strategy of MeSH terms in MEDLINE, CINAHL, EMBASE, and
9
SportDiscuss. Inclusion criteria: diagnostic studies relating to athletic groin pain, professional or
10
semi-professional athletes, symptoms lasting for more than six weeks, and not limited by age or
11
gender. A priori exclusion criteria were utilised. Outcome Measures: QUADAS tool,
12
sensitivity and specificity, likelihood ratios and predictive values of the reported tests and
13
investigations Results: 577 journal articles were identified. Five studies met all requirements.
14
Sensitivity and specificity of clinical tests ranged between 30-100% and 88-95% respectively
15
with negative likelihood ratio of 0.15-0.78 and positive likelihood ratios of 1.0-11.0. Sensitivity
16
and specificity of investigations (MRI, herniography, and dynamic ultrasound) ranged between
17
68-100% and 33-100% respectively with negative likelihood ratios between 0-0.32 and positive
18
likelihood ratios between 1.5-8.1. Conclusion: There is a lack of validated diagnostic clinical
19
tests available for clinicians and a lack of symptomology being evaluated. It is recommended
20
that a reference standard be used and data be reported in sufficient detail to calculate
21
diagnostic statistics that will be of use to the clinician.
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ABSTRACT
Key words: Groin, athletic injury, diagnosis, systematic review
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25 26
INTRODUCTION Groin injuries are common in sports that require cutting and sprinting manoeuvres such as
28
soccer, rugby league, rugby union, cricket, ice hockey and Australian Rules football (Brown et
29
al., 2008; O'Connor, 2004; J. Orchard, James, Alcott, Carter, & Farhart, 2002; J. Orchard &
30
Verrall, 2000; Verrall, Slavotinek, & Fon, 2001; Werner, Hägglund, Walden, & Ekstrand,
31
2009). They account for between 4% and 16% of all injuries each season (J. Orchard & Verrall,
32
2000; Werner, et al., 2009) and have an estimated incidence of 0.59-3.5 injuries per 1000 hours
33
of activity (Ekstrand & Hilding, 1999; J. Orchard & Verrall, 2000; Werner, et al., 2009). Groin
34
injuries have a high recurrence rate, reported between 15% and 31% (Werner, et al., 2009). In
35
Australian Rules Football they are the second most common injury behind hamstring muscle
36
strains and have been estimated to be responsible for 11 to 18 competition games per team being
37
missed by players due to injury in a season (J. Orchard & Verrall, 2000). Confusion regarding
38
the clinical presentation of groin pain and inadequate differential diagnosis of groin pathology is
39
likely to result in inappropriate management and consequently ongoing pain or re-injury for the
40
injured athletes.
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27
41
The hip joint is a potential source of groin pain and is associated with the development of long-
43
standing groin pain in athletes (C. J. Bradshaw, Bundy, & Falvey, 2008). Sacroiliac joint (SIJ)
44
pathology and degeneration seen on plain X-Ray is also associated with long-standing groin
45
pain (LGP) (Harris & Murray, 1974; Major & Helms, 1997). Entrapment of the obturator nerve
46
has been diagnosed and described in athletic populations with long-standing groin pain (C.
47
Bradshaw & Holmich, 2006; C. Bradshaw, McCrory, Bell, & Brukner, 1997; C. J. Bradshaw, et
48
al., 2008; Brukner, Bradshaw, & McCrory, 1999). Tearing of the external oblique muscle
49
aponeurosis has frequently been described in hockey players and has been associated with
50
ilioinguinal nerve entrapment (Irshad et al., 2001).
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Within the medial thigh compartment, the adductor longus muscle is commonly implicated in
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long-standing groin pain (Albers, Spritzer, Garrett Jr., & Meyers, 2001; Renstrom & Peterson,
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1980; Robinson et al., 2004). It has been hypothesised that the forces created by the rectus
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abdominis and adductor longus muscles control the shearing force across the anterior pubic arch
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and pubic symphysis (Meyers, Greenleaf, & Saad, 2005). Disruption of this equilibrium is likely
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to impact on these shearing forces. This can occur in adductor longus enthesopathies and rectus
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abdominis tendinopathies, as diagnosed via MRI (Robinson, et al., 2004; Zoga et al., 2008).
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Neutralising these forces surgically by either reinforcing the rectus abdominis enthesis or
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performing an adductor longus tenotomy has been shown to improve function (Meyers, Foley,
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Garrett, Lohnes, & Mandlebaum, 2000; Meyers et al., 2008).
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The inguinal canal is frequently injured and can also exhibit dysfunction under load in athletes
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(Cohen, Turkenburg, & van Dalen, 1990; Kesek, Ekberg, & Westlin, 2002; Smedberg, Broome,
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Gullmo, & Roos, 1985; Taylor et al., 1991; Yilmazlar, Kizil, Zorluoglu, & Ozguc, 1996).
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“Sportsman’s hernia” or posterior inguinal wall deficiency occurs when the posterior wall
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bulges under increased abdominal pressure (J. W. Orchard, Read, Neophyton, & Garlick, 1998).
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It has been reported that direct hernias account for over half of hernias in athletes and can occur
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in combination with indirect hernia and posterior wall weakness (Smedberg, et al., 1985).
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Contradicting this, a later study found unilateral indirect hernias to be the most common type of
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hernia in athletes with longstanding groin pain (Yilmazlar, et al., 1996). Femoral hernias are
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rare in this population (Robinson, et al., 2004; Yilmazlar, et al., 1996).
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It is important to note that many diseases and conditions of non-musculoskeletal origin may
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refer symptoms to this region. These include gynaecological, urological, malignancies, sexually
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transmitted and rheumatological conditions (C. Bradshaw & Holmich, 2006; Ekberg, Persson,
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Abrahamsson, Westlin, & Lilja, 1988; Harris & Murray, 1974; Smedberg, et al., 1985). It is
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therefore important to consider a multidisciplinary approach to both diagnosis and treatment of
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long-standing groin pain in athletes. Additionally, other factors may also influence the patient’s
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experience and outcome from the injury. These include the emotional, social or cognitive in
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origin and should be considered in a biopsychosocial assessment framework. It is therefore
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important to consider a multidisciplinary approach which includes physical and psychological
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aspects to both the diagnosis and treatment of long-standing groin pain in athletes.
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Several approaches to the diagnosis of LGP have been proposed including patho-anatomical
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models (Falvey, Franklyn-Miller, & McCrory, 2008) and the clinical entity approach (Holmich,
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2007). Physical examination can be reliable (Holmich, Holmich, & Bjerg, 2004; Malliaras,
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Hogan, Nawrocki, Crossley, & Schache, 2010) however, while reliable many tests have not
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been evaluated for their diagnostic accuracy. Physical tests have been used to classify groin pain
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into three main pathological entities; adductor-related, iliopsoas-related and rectus abdominis
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related dysfunctions. Holmich et al (2007) studied 207 athletes and found 119 (57.5%) had
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adductor-related dysfunction as their primary entity followed by iliopsoas-related (36%) and
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rectus abdominis-related (10%) dysfunctions. Notably, multiple pathologies were found in 69
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(33%) patients, with 16 (7.7%) having all three pathological entities and rectus abdominis-
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related dysfunction rarely occurring in isolation (Holmich, et al., 2004).
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Falvey et al. (2009) systematically considered the anatomical structures that are located within
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or around the “groin triangle”. Structures were classified by their region; pubic tubercle region,
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medial to the triangle, superior to the base, lateral to the triangle and within the triangle. This
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systematic approach allows the clinician to consider all the structures potentially implicated.
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This patho-anatomical approach provides an intuitively meaningful framework when diagnosing
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the source of LGP, the clinical entity approach as demonstrated by Hölmich et al. (2004) has
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merit when considering conservative clinical examination and treatment options.
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However, a lack of evaluation of clinical tests for the purpose of diagnosis is evident.
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There may be several reasons for this; poor consensus on pathology and terminology,
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lack of specific tests implicating individual structures, absence of an accepted and
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available reference standard against which test performance may be assessed. The
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complexity of this region with its overlapping anatomy and interdependence of structure means
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that a specific tests and/or imaging is challenging to develop and difficult to evaluate. There is
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also a deficiency of literature on the symptomology of athletes with longstanding groin pain
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with reference to diagnoses.
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The purpose of this review is to evaluate the current literature pertaining clinical tests,
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symptomology and investigations available to the clinician working with athletes with
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longstanding groin pain and to examine their validity.
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METHODS
A search was performed using published strategies for searching diagnostic studies (Deville et
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al., 2002). Databases searched included MEDLINE, CINAHL, EMBASE, and SportDiscuss (to
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August 2009) using the MeSH terms: groin, athletic injuries, abdominal muscles, sportsm* and
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hernia, abdominal pain, pelvis pain, athletic pubalgia, pubalgia, rheumatic diseases,
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enthesopathy, inguinal canal, hockey groin syndrome, Gilmore’s groin, adductor longus, rectus
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abdominis, pubic bone, pubic symphysis, enthesis, osteitis pubis, pain, adductor related,
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inguinal hernia, abdominal wall hernia, groin pain, tendinopathy, posterior inguinal wall
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deficiency, and enthesitis. Results were limited to “human” and the English language. Reference
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lists from retrieved studies were examined for any studies not retrieved by the database
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searches. One investigator (MD) screened the titles and abstract of studies without blinding to
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results, authors or journals.
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For studies to be included in the review, they had to pertain to the diagnosis of long-standing
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groin pain (symptoms lasting more than six weeks) in professional or semi-professional athletes
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across any sport, not limited by age or gender and could be of any investigation type. Studies
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had to include enough data to allow derivation of sensitivity and specificity if it had not been
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reported in the paper. A priori exclusion criteria included: articles on treatment without
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describing the diagnostic methodology, if data on sensitivity and specificity data was unreported
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and could not be derived, studies not using a reference standard, hip related groin pain studies
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since this systematic review concentrates on the structures around the pubic area that can cause
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pain, case studies, case series, reviews, prognostic studies, letters, comments and cadaver
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studies. Two investigators (MD, PC) independently assessed the eligibility of the studies for
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inclusion in the review. Discrepancies were settled by discussion and if a consensus could not
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be reached a third investigator (PO) adjudicated. See Box 1 for the review outline.
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Methodological quality of the diagnostic papers were judged using the QUADAS tool (Whiting,
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Rutjes, Reitsma, Bossuyt, & Kleijnen, 2003). This tool has been modified and used in a
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previous systematic review of groin pain (Jansen, Mens, Backx, & Stam, 2008). Articles are
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scored as “yes”, “no” or “unclear” across 14 criteria. The QUADAS tool does not recommend
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to calculate a score as this has no consideration for the individual quality of the item and may
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introduce potential biases and therefore missing potential associations (Whiting, et al., 2003).
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The QUADAS tool criteria are 1.Was the spectrum of patients representative of the patients
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who will receive the test in practice? 2. Were selection criteria clearly described? 3. Is the
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reference standard likely to correctly classify the target condition? 4. Is the time period between
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reference standard and index test short enough to be reasonably sure that the target condition did
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not change between the two tests? 5. Did the whole sample or a random selection of the sample,
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receive verification using a reference standard of diagnosis? 6. Did patients receive the same
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reference standard regardless of the index test result? 7. Was the reference standard independent
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of the index test (i.e. the index test did not form part of the reference standard)? 8.Was the
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execution of the index test described in sufficient detail to permit replication of the test? 9. Was
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the execution of the reference standard described in sufficient detail to permit its replication?
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10. Were the index test results interpreted without knowledge of the results of the reference
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standard? 11. Were the reference standard results interpreted without knowledge of the results
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of the index test? 12. Were the same clinical data available when test results were interpreted as
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would be available when the test is used in practice? 13. Were un-interpretable/ intermediate
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test results reported? 14.Were withdrawals from the study explained? The specificity,
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sensitivity, predictive value and likelihood ratios were also assessed and calculated from the
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published data where they were not reported.
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RESULTS
The database search retrieved 577 journal articles of which five met the inclusion criteria.
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Figure 1 indicates the flow of studies. Results of the QUADAS tool evaluation are presented in
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Table 1. The compliance to individual items in the QUADAS tool varied with all studies
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compliant with items 1, 3, and 7. Items 6, 11 and 14 had the poorest compliance with only one
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study per item satisfying the relevant measurement.
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Figure 1. Flow of studies through the review.
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Table 1. Compliance of individual studies with items of the QUADAS tool
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The five studies considered six different pathologies with four physical assessments and five
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diagnostic imaging techniques being evaluated. This is summarised in Table 2. Three of the five
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included studies reported multiple pathologies in athletes with LGP (Brennan et al., 2005;
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O'Connell, Powell, McCaffrey, O'Connell, & Eustace, 2002; Zoga, et al., 2008). Table 2
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summarises the information from the patient interview. None of these findings were compared
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to the reference standard. Table 2 provides a summary of the data for each test including
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sensitivity, specificity, likelihood ratios and predictive values. Sensitivity of diagnostic imaging
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ranged from 68% to 100%. The sensitivity of physical assessments was lower (30-86%) with
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the exception of palpation of inguinal hernias which, in a small sample, had a sensitivity of
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100%. Specificity of diagnostic imaging ranged from 0-100% and physical assessments had a
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specificity of 88-100%. With the exception of MRI of adductor tendon pathology (+LR=8.07; -
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LR 0.15) and “bilateral adduction” (+LR=11.0), the tests evaluated in this systematic review
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would fail to substantially increase the post-test probability of the diagnosis under question.
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DISCUSSION While accurate and timely diagnosis of long-standing groin pain is imperative for professional
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athletes, a diagnostic test, even with good diagnostic statistics, is only important if it impacts
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positively on the outcome of the patient (Ferrante, Hyde, McCaffery, Bossuyt, & Deeks, 2012).
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It is unknown whether the tests highlighted in this systematic review improve either treatment
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choices or outcomes. However, as multiple structures can be implicated diagnosis can be
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difficult. Many of the clinical assessments used by sports physicians and physiotherapists have
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not been evaluated against a reference standard. The results from this systematic review reflect
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the lack of validation of clinical tests in current use. This is reflected by the fact that only five
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studies met our a priori inclusion criteria. Currently there has been no cost benefit analyses
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undertaken related to diagnostic imaging in this population. Future studies may be warranted.
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Reports from athletes with LGP during patient interview can give insight into the pathology
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(Harris & Murray, 1974; Kunduracioglu, Yilmaz, Yorubulut, & Kudas, 2007; Major & Helms,
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1997; J. W. Orchard, et al., 1998; Smedberg, et al., 1985; Verrall, Slavotinek, Barnes, & Fon,
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2005). However, such reported symptoms are not exclusive to any particular pathology and
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have not been evaluated against a reference standard. This is an area for future research.
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Clinicians can be confident in the reliability of clinical assessment of patients with LGP (Hogan
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& Lovell, 1997; Holmich, et al., 2004; Malliaras, et al., 2010; Slavotinek, Verrall, Fon, & Sage,
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2005; Verrall, et al., 2005). However, there needs to be a clear delineation between tests that are
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clinically useful and those who have been evaluated for their diagnostic accuracy. Verrall et al
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(2005) examined three resisted adduction pain provocation tests on Australian Rules footballers
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with and without groin pain. These athletes subsequently underwent MRI of their groin region.
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In the presence of all three positive pain provocation tests there is a high likelihood of having
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pubic bone marrow oedema (BMO) detected by MRI. Tenderness on the symphysis pubis
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and/or superior pubic rami in addition to the three positive provocation tests further improves
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the predictive ability of the examination(Slavotinek, et al., 2005; Verrall, et al., 2005). This
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provides useful guidelines in the clinic if BMO is suspected and MRI is unavailable.
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management of the long-standing groin pain, these were excluded from the systematic review as
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they failed to meet the inclusion criteria for assessment against a reference standard. Clinically
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useful measures such as strength of the “squeeze test” (isometric adduction in crooked lying) are
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both clinically and statistically significantly less in athletes with long-standing groin pain
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(Malliaras, et al., 2010) but this may not be entirely related to adductor pathology (Mens,
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Inklaar, Koes, & Stam, 2006). Lovell et al (2012) evaluated six clinical tests for the adductors.
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Their findings showed that the tests cannot discriminate between the muscles that form the
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adductor group(G. A. Lovell, Blanch, & Barnes, 2012). Mens et al. (2006) applied a pelvic belt
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and increased the strength of adduction and decreased difficulty in lower limb tasks (Mens, et
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al., 2006) indicating that there is either reflex inhibition occurring and/or an inability to stabilise
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the pelvic ring when transferring loads from the lower limbs across the SIJ to the spine. This
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suggests that there may be multiple co-existing pathologies and conditions and the examiner
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should consider the entire lumbo-pelvic-hip complex prior to diagnosis. Mens et al. (2006) did
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not describe whether there was tenderness over the adductor enthesis and/or pubic symphysis, a
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common finding in athletes with adductor-related longstanding groin pain (Robinson, et al.,
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2004; Schilders et al., 2007). This may guide the clinician in deciding the value of applying the
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pelvic stabilisation test. Pain in the groin without adductor entheseal/pubic bone tenderness is
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considered a separate entity (Verrall, et al., 2001). Palpation was included in the cluster of
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fourteen clinical tests proposed by Hölmich, Hölmich and Bjerg (2004). Hölmich et al (2004)
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was excluded from this systematic review as it did not have a reference standard and therefore
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did not evaluate the diagnostic ability of the described tests. Their recommendation for
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assessing athletes with groin pain included palpation, stretching, pain provocation and strength
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tests. Good reliability and inter-observer agreement (κ>0.60) was achieved between examiners
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for 11 of 14 tests. While clinically useful in assessment and reassessment, these findings do not
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definitively diagnose the source of groin pain in the athletes. Zoga et al. (2008) utilised physical
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assessment results as a reference standard in their study. Unfortunately the details of these
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assessments were not reported.
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This systematic review highlights that MRI can be used as part of the diagnostic procedure.
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Abnormalities of the anterior pubis and adductor enthesis on MRI have been shown to
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correspond to the side of presenting symptoms (Robinson, et al., 2004). Oedema in pubic bone
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marrow, pubic symphysis and periarticular region is associated with an earlier stage of injury
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(Kunduracioglu, et al., 2007). Subchondral sclerosis and resorption, symphysis pubis margin
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irregularities and tendon injuries to the adductors, iliopsoas and gluteus maximus have a
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significant correlation (p
