Physical Therapy in Sport 16 (2015) 127e134
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Physical Therapy in Sport journal homepage: www.elsevier.com/ptsp
The inﬂuence of joint hypermobility on functional movement control in an elite netball population: A preliminary cohort study Kessie Soper a, b, *, Jane V. Simmonds a, f, Hanadi Kaz Kaz c, d, Nelly Ninis c, e a
University of Hertfordshire, Hatﬁeld, Hertfordshire, AL10 9AB, UK Bodybalance Physiotherapy and Sports Injuries Clinic, University of Hertfordshire, De Havilland Campus, Hatﬁeld, Hertfordshire, AL10 9EU, UK c Hypermobility Unit, Hospital of St John and St Elizabeth, 60 Grove End Road, London NW8 9NH, UK d University College London Hospital, 235 Euston Road, London NW1 2BU, UK e Imperial Healthcare NHS trust, St Mary's Hospital, Praed St, London W2 1NY, UK f Institute of Child Health, University College London, 30 Guilford St, London WC1N 1EH, UK b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 16 May 2014 Received in revised form 10 July 2014 Accepted 14 July 2014
Objectives: To ascertain the prevalence of General Joint Hypermobility (GJH) and Joint Hypermobility Syndrome (JHS) in elite level netballers. To investigate whether GJH inﬂuences functional movement control and explore whether symptoms of dysautonomia are reported in this population. Design: Observational within-subject cross-sectional design. Setting: Field based study. Participants: 27 elite level netballers (14e26 years). Main outcome measures: GJH and JHS were assessed using the Beighton scale, 5 point questionnaire and the Brighton Criteria. Functional movement control was measured using posturography on a force platform and the Star Excursion Balance Test (SEBT). Results: The prevalence of GJH was 63% (n ¼ 17) (Beighton score 4/9) and JHS was 15% (n ¼ 4). Symptoms of dysautonomia were minimally prevalent. A trend was observed in which participants with GJH demonstrated increased postural instability on the functional tests. Following Bonferroni adjustment, this was statistically signiﬁcant only when comparing posturographic data between the distinctly hypermobile participants and the rest of the group for path area (p ¼ 0.002) and velocity (p ¼ 0.002) on the left side. Conclusions: A high prevalence of GJH was observed. A trend towards impairment of functional movement control was observed in the netballers with GJH. This observation did not reach statistical significance except for posturographic path area and velocity. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Hypermobility Laxity Balance Sport
1. Introduction The prevalence of General Joint Hypermobility (GJH) differs between different sporting populations but appears to be higher than in the general population (Russek, 1999; Simmonds & Keer, 2007). Joint hypermobility is often considered an asset in sports for which performance requires a high degree of ﬂexibility (Gannon & Bird, 1999), with estimates as high as 90% in ballet dancers (McCormack, Briggs, Hakim, & Grahame, 2004) and 66% in dance students (Scheper et al., 2013). Research has reported estimates
* Corresponding author. Present address: Physiotherapy London, 150 Westferry Studios, Milligan Street, Canary Wharf, London E14 8AS, UK. Tel.: þ44 (0)20 7093 3499. E-mail addresses: [email protected]
(K. Soper), [email protected]
uk (J.V. Simmonds). http://dx.doi.org/10.1016/j.ptsp.2014.07.002 1466-853X/© 2014 Elsevier Ltd. All rights reserved.
between 33 and 42% in professional football (Collinge & Simmonds, 2009; Konopinski, Jones, & Johnson, 2012) and 24% in amateur rugby (Stewart & Burden, 2004). One previous study has investigated GJH in netball (Smith, Damodaran, Swaminathan, Campbell, & Barnsley, 2005). This involved 200 children (6e16 years), of which 40% were reported as distinctly hypermobile (Beighton score 5e9/9) and a further 26% as moderately hypermobile (Beighton score 3e4/9). There is a paucity of epidemiological data for Joint Hypermobility Syndrome (JHS) in sport. In a group of ballet dancers, 38% were reported to have JHS (McCormack et al., 2004). It has been suggested that a degree of autonomic neuropathy may afﬂict the cardiovascular system in people with joint hypermobility (Bird, 2011; Hakim & Grahame, 2004). Reported symptoms include dizziness, syncope, palpitations, temperature dysregulation and fatigue (Gazit, Nahir, Grahame, & Jacob, 2003;
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To critically appraise the current criteria for deﬁning GJH and JHS in a sporting population. To explore whether symptoms of dysautonomia are reported in this population.
Kanjwal, Saeed, Karabin, Kanjwal, & Grubb, 2010). Studies of patients with JHS in rheumatology clinics have reported a high occurrence of orthostatic symptoms (Gazit et al., 2003; Hakim & Grahame, 2004). Potential explanations for this include increased vascular distensibility, weakened vascular tissue elasticity, impaired central sympathetic control and deconditioning secondary to inactivity (Grubb, 2008; Hakim & Grahame, 2004; Kanjwal et al., 2010). It is currently unknown whether deconditioning is a causative or secondary factor in dysautonomia, therefore it is of interest to explore whether symptoms of dysautonomia are prevalent in a sporting population. People with hypermobility are anecdotally observed to incur recurrent injuries such as joint dislocations, tendinopathies and ligament ruptures (Keer, 2003; Russek, 1999; Simpson, 2006). Whilst this is a common clinical observation, research evidence is inconsistent. Prospective studies have found no additional risk of injury in hypermobile individuals in professional football (Collinge & Simmonds, 2009), lacrosse (Decoster, Bernier, Lindsay, & Vailas, 1999) or collegiate athletes (Krivickas & Feinberg, 1996). An increased absence from sport following injury was observed in hypermobile dancers (Briggs, McCormack, Hakim, & Grahame, 2009) and footballers (Collinge & Simmonds, 2009). Conﬂicting evidence concluded hypermobile athletes have a signiﬁcantly higher risk of injury in an ensuing study in professional football (Konopinski et al., 2012), amateur rugby (Stewart & Burden, 2004), € derman, Alfredson, Pietila €, & Werner, 2001) and female football (So netball (Smith et al., 2005). A recent well designed systematic review with stringent inclusion criteria and meta-analysis concluded that hypermobile individuals have an increased risk of injury of the knee during contact sports, but not the ankle (Pacey, Nicholson, Adams, Munn, & Munns, 2010). It has been hypothesised that impaired proprioception and neuromuscular control may contribute towards an increased risk of injury in hypermobile individuals (Ferrell et al., 2004; Rombaut, De Paepe, Malfait, Cools, & Calders, 2010). Whilst it is widely accepted that hypermobility may compromise static collagenous components of joint stability such as ligaments and joint capsule, it is now thought that dynamic components, controlled by the central and peripheral nervous system, may also be affected (Bird, 2011; Ferrell, Tennant, Baxendale, Kusel, & Sturrock, 2007). Research has demonstrated impaired proprioception at the knee joint in people with hypermobility compared to matched controls in both adults (Hall, Ferrell, Sturrock, Hamblen, & Baxendale, 1995; Rombaut et al., 2010), and children (Fatoye, Palmer, Macmillan, Rowe, & van der Linden, 2009). Previous research found that 22 participants with Ehlers Danlos Syndrome (EDS) had signiﬁcantly impaired postural control and increased dependency on visual information compared to age matched controls when investigating displacement of centre of pressure (COP) on a force platform in a variety of standing conditions (Rombaut et al., 2011). Similar results were replicated in a subsequent study (Galli et al., 2011). The applicability to an elite athletic population has limitations as these studies involved older participants with high levels of impairment. A programme of closed kinetic chain exercise has been demonstrated to improve proprioception, balance and musculoskeletal reﬂex function in hypermobile individuals (Ferrell et al., 2004, 2007; Sahin et al., 2008). It is therefore of interest whether impairments persist in well-conditioned hypermobile athletes.
The Beighton score (Beighton, Soloman, & Soskolne, 1973) is a screening tool for GJH which assesses range of motion of the elbows, knees, thumbs, 5th ﬁngers and lumbar spine (Fig. 1). Joint range of motion was measured passively with a goniometer. The Brighton criteria (Grahame, Bird, & Child, 2000) was used to assess for JHS. The Brighton criteria is yet to be validated in children under 16, but remains the best available tool (Grahame et al., 2000; McCormack et al., 2004). Previously published standardised protocols were followed (Boyle, Witt, & Riegger-Krugh, 2003; JuulKristensen, Røgind, Jensen, & Remvig, 2007).
1.1. Study objectives
2.2. Single leg stand and posturography
To ascertain the prevalence of GJH and JHS in an elite netball squad. To compare performance in a series of functional tests of movement control between participants with and without GJH.
2. Methods 27 elite level netball players (age 14e26 years, mean 19.3) were recruited from a UK superleague franchise. It was speciﬁed that the participant must be a minimum of 14 years old, national or international standard, have had a minimum of 3 years netball experience and understand English. Injured players (who were not ﬁt to participate in full training or match play) were excluded as they would be unable to safely complete the testing protocol. All testing was completed before training, ensuring that the participant had not exercised for at least 12 h prior. This was important as activity is thought to affect tissue viscoelastic properties and fatigue is known to inﬂuence functional movement control (Fox, Mihalik, Blackburn, Battaglini, & Guskiewicz, 2008; Gribble, Robinson, Hertel, & Denegar, 2009; Springer & Pincivero, 2009). The start leg was pre-randomised for all tests. Testing was completed by the lead researcher, who is well practiced in all testing methods. A self-reported questionnaire was completed to record basic demographic information such as age, netball experience, playing position, ethnicity, participation in other sports and injury history. The 5 point questionnaire was integrated into the self-reported questionnaire as an additional screen for hypermobility (Hakim & Grahame, 2003a). A series of questions exploring the athlete's experience of dysautonomic symptoms was also included. These were developed in conjunction with a paediatrician with an interest in hypermobility. To the researcher's knowledge, no standardised method for self-reporting of dysautonomia is available. The presence, location and severity of musculoskeletal pain was recorded using a body chart and the Visual Analogue Scale (VAS) (Burckhardt & Jones, 2003). Participants in pain were not excluded from the study as pain is known to be a common feature in joint hypermobility (Murray, 2006). Height was measured with the participant standing with their feet together and back against the wall. Arm span was measured between the most distal points of the third ﬁngers with the arms supinated and outstretched horizontally against the wall (standardised with a spirit level). Leg length was measured in supine from the anterior inferior iliac spine to the medial malleolus following standardisation of the pelvic position (Plisky, Rauh, Kaminski, & Underwood, 2006). 2.1. Screening for hypermobility
The participant stood on the force plate (ICS balance platform 400 mm 400 mm x 42 mm, Otometrics, Denmark) without shoes, with their feet on the marked area on the platform and their arms folded across the chest. They were asked to move onto one leg by
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Fig. 1. Measuring knee hypermobility.
lifting the contralateral foot with the knee bent without touching the weight bearing leg. The participant was then instructed to close the eyes and remain as “still as possible”, according to published protocol (Durall et al., 2011). The trial was terminated if the participant's legs touched each other, foot touched down, or arms moved from the start position. Ability to complete 30 s was noted and if this was not achieved, the time of failure was recorded (Bohannon, Larkin, Cook, Gear, & Singer, 1984). Posturographic data was collected from the force platform for the ﬁrst 10 s after closing the eyes at a sampling rate of 50 Hz. Computer automated stability analysis software (Vestlab version 7.0) was used to calculate changes in displacement of COP. The following COP measurements were recorded: path length (mm), velocity (mm/s), sway ( ), lateral variance (mm2), anterioreposterior (AP) variance (mm2), standard ellipse (mm2) and sway area (mm2). A higher value for each coefﬁcient indicates a €tterstro €m, Fride n, greater degree of postural instability (Ageberg, Za & Moritz, 2001; Hertel, Gay, & Denegar, 2002). Three practice trials were completed before 3 consecutive trials on the same leg with a 30 s rest between trials. The results were averaged across the 3 trials, which is proposed to improve reliability due to the potential for occasional irregularities due to fatigue or diminished attention (Ruhe, Fejer, & Walker, 2010; Scoppa, Capra, Gallamini, & Shiffer, 2013). The test was repeated on the opposite leg. 2.3. Star excursion balance test The grid consisted of 8 lines at 45 from each other, extending from a centre point (Fig. 2). Published protocol was followed (Robinson & Gribble, 2008). The participant placed their stance foot in the middle of the grid. They were instructed to keep their hands on their hips and to keep the stance foot in position, with the heel remaining in contact with the ﬂoor. A maximal reach was made with the other leg to lightly touch the toe on the tape according to the pre-randomised order of directions. Participants were required to successfully return to double leg stance in the centre of the grid without any additional touchdowns or disruption to the stance foot. The trial was discarded and repeated if balance was lost. The distance reached along the tape was recorded for each attempt. Four practice attempts were provided to account for a learning effect (Gribble, Hertel, & Plisky, 2012; Munro & Herrington, 2010). Three trials were completed on each leg with a 2 min rest between trials. Reach values were expressed as a percentage of leg length. 2.4. Data analysis Independent-samples t-tests were used to compare results between participants who were hypermobile and distinctly
Fig. 2. Star excursion balance test.
hypermobile to those without GJH. The alpha level for statistical signiﬁcance was p 0.003 following a Bonferroni adjustment. 3. Results Descriptive characteristics of the participants are shown in Table 1. The mean age was 19.3 years (14e26 years, Standard Deviation (SD) 3.7 years). 89% of participants were aged 16 or over. 3.1. Prevalence of general joint hypermobility 17 participants (63%) scored 4 or more on the Beighton score, indicating GJH. The participants with GJH were further subgrouped as distinctly hypermobile (7e9/9) (n ¼ 5, 18.5%) and hypermobile (4e6/9) (n ¼ 12, 44.5%). This method of classiﬁcation was previously described by Stewart and Burden (2004). Fig. 3 illustrates the percentage of hypermobility per body part. 11 participants (48.2%) scored 2 or more on the 5 part questionnaire, indicating GJH according to this criteria. 3.1.1. Ethnicity and GJH 67% of participants were white British (n ¼ 17), 22% black Caribbean (n ¼ 6) and 11% mixed race (white and black Caribbean, n ¼ 3). An independent-samples t-test was conducted to compare the Beighton scores between white and non-white (black or mixed race) participants. It was found that the scores of the non-white participants were signiﬁcantly higher (p ¼ 0.01). 3.2. Prevalence of joint hypermobility syndrome The Brighton criteria indicated that 4 participants (14.8%) had JHS. The categories of the Brighton criteria in which positive results were attained are graphically illustrated in Fig. 4. Table 1 Demographics (n ¼ 27). Variable
Age (years) Height (cm) Weight (kg) BMI (kg/m2) Experience in sport (years) Playing time per week (h)
19.3 176.7 69.7 22.2 8.5 15.4
14e26 163e193 53e93 17.8e26.5 3e18 10e24
3.7 7.8 10.7 2.3 4.1 4.3
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Fig. 3. Percentage of hypermobility per body part (n ¼ 27).
3.3. Single leg stand test The time achieved on the single leg stand test was lower in the hypermobile group than the non hypermobile group. This is illustrated in Fig. 5. This observation was not statistically signiﬁcant (right p ¼ 0.083, left p ¼ 0.043). 3.4. Posturography Mean posturographic values were higher for every parameter in the hypermobile group (4/9) when compared to the non hypermobile group, indicating a consistent trend of postural instability in hypermobile participants. This was particularly apparent when
comparing the distinctly hypermobile group (7/9) to all other participants (<7/9). Statistical signiﬁcance was found in this comparison for path area and velocity on the left side only (p ¼ 0.002, p ¼ 0.002). 3.5. Star excursion balanche test Fig. 6 illustrates the mean normalised distances reached in each direction for the hypermobile and non hypermobile groups. A trend was demonstrated in which the non hypermobile group achieved greater distances, except in the posterior and posteromedial directions, when the hypermobile group performed better. This observation was not statistically signiﬁcant (p ¼ 0.043e0.882).
Fig. 4. Percentage of positive results per category on Brighton criteria (n ¼ 27).
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3.6. Prevalence of dysautonomia Four participants reported 2 or more symptoms of dysautonomia and a further 7 participants reported just one symptom. Eight of these 11 participants scored 4 or more on the Beighton score. Dizziness and fainting was the most commonly reported complaint (22%), followed by migraines, nausea and temperature dysregulation (11% each). Constipation and palpitations were reported by just one participant. No statistical relationship was found between the presence of JHS or GJH and reporting of dysautonomic symptoms. 3.7. Missing data One participant was unable to attain 10 s single leg standing on one leg and therefore it was not possible to collect posturographic data for that leg. Missing data was excluded from analysis. 4. Discussion 4.1. Prevalence of GJH and JHS
Fig. 5. Time to failure on single leg stand test.
The prevalence of GJH within this elite netball population was 63% (n ¼ 17) using the generally accepted criteria of 4/9 on the Beighton score (mode 5, range 0e7). In order to allow comparison with previous research, the mean Beighton score was calculated. At 3.96 (SD 2.4), this is similar to published research in netball, which reported a mean score of 3.99 (SD 2.8), a prevalence of 40% distinct hypermobility (5e9/9) and a further 26% moderate hypermobility (3e4/9) (Smith et al., 2005). However, this study's use of a classiﬁcation system including a category of 3e4/9, which bridges the standard criteria of 4/9, raises the question as to how accurately this category can represent ‘moderate hypermobility’ and limits comparison to other research. In addition, this study assessed for GJH after exercise, which may have inﬂuenced their results. The prevalence of GJH is higher than in the general population, in which it is thought to be between 10 and 30% in adults and slightly higher in children (Hakim & Grahame, 2003b). The mean age in this study was 19.3 years, 3 participants were under 16. Nonetheless, the prevalence of GJH was still considerably higher than the 27.5% previously observed in 14 year old females (Clinch et al., 2011).
Fig. 6. SEBT distances by direction.
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The prevalence was lower than in professional dancers (90%) (McCormack et al., 2004) but higher than has been reported in other team sports including professional football (33e42%) and amateur rugby (24%) (Collinge & Simmonds, 2009; Konopinski et al., 2012; Stewart & Burden, 2004). It is important to note that the latter studies involved older male participants (mean age 22.5e24.4 years), which may account for the observed difference, as the prevalence of GJH is known to decrease with age and is more common in females (Beighton et al., 1973; Remvig, Jensen, & Ward, 2007a). Ethnic background may be relevant to both hypermobility prevalence and measures of functional stability. Nine participants within this group (33%) were black Caribbean or mixed white and black Caribbean. In a sport such as netball, the performance beneﬁt of GJH is less obvious than in the performing arts, for which the potential advantages of increased hypermobility are well documented (Scheper et al., 2013). However, in elite netball, excessive joint mobility may be one component which allows an athlete to obtain a large reach distance from a ﬁxed foot as well as better reach at the shoulder complex. Speciﬁc aspects of GJH may be observed within certain sports. This study found that the 5th ﬁngers were the least hypermobile joints, with hyperextensibility of the right 5th ﬁnger occurring in only 15% (n ¼ 4) of participants. This is conﬂicting to previous research which proposed that 5th ﬁnger hyperextensibility is normal in adolescent girls (Clinch et al., 2011). A potential explanation may be the large amount of ﬁnger ﬂexor conditioning which is inherent to netball as increased neuromuscular tone has been hypothesised to limit passive joint range (Bird, 2011). The prevalence of JHS in this study was 15% (n ¼ 4), which is somewhat lower than the 34% reported in professional ballet dancers (McCormack et al., 2004). It is important to note that the ballet study did not exclude injured dancers, which may partly account for this difference. However, only one netballer in the squad was excluded by injury from this study. No other research has reported the prevalence of JHS in sport. Each participant who was classiﬁed with JHS did so by meeting one major criteria (4/9 Beighton score) and two minor criteria (marfanoid habitus, history of >1 dislocation, abnormal skin) (see Fig. 4). All the participants with JHS scored highly on the Beighton test, with 3 scoring 7/9 and 1 scoring 6/9. Several participants were observed to have complete marfanoid habitus. This may be due to the performance beneﬁts for shooters and defenders of being tall with disproportionately long limbs, which may create selection bias.
hypermobility relevant for the elite sportsperson and therefore its speciﬁcity has been questioned (Bird & Foley, 2013). For example, assessment of the foot is not included, despite pes planus being highly prevalent within the hypermobile population and potentially relevant to injury risk (Adib, Davies, Grahame, Woo, & Murray, 2005; Moen, Tol, Weir, Steunebrink, & De Winter, 2009). A criteria of 4/9 has been generally accepted within the literature to deﬁne GJH, despite this not being speciﬁed by the original authors (Remvig et al., 2007b). Although JHS and EDS hypermobility type are widely considered synonymous (Tinkle et al., 2009), the Brighton criteria employs a criteria of 4/9 (Grahame et al., 2000), whereas the Villefranche recommendations for EDS use 5/9 (Beighton, De Paepe, Steinmann, Tsipouras, & Wenstrup, 1998). It has been proposed that it may be more scientiﬁcally accurate to apply different criteria according to sex, age and ethnicity (Juul-Kristensen et al., 2009). Criteria as high as 7/8 or 8/9 have been recommended for use in children aged 6e12 (Jansson, €m, 2004; Smits-Engelsman et al., Saartok, Werner, & Renstro 2011). The justiﬁcation for this may be unsubstantiated, relying on calculations which assume 5% of the population are hypermobile. It is interesting to consider whether different criteria should be applied to different sporting populations. To allow widespread comparison with other literature, the criterion of 4/9 was used in this study, resulting in GJH representing the majority. It is pertinent to consider whether this illustrates a departure from normality or rather a different range of normal. Subgroup analysis revealed that 18.5% (n ¼ 5) of the participants would be considered distinctly hypermobile (7/9) according to the criteria suggested by Stewart and Burden (2004). It remains difﬁcult to ascertain whether this is the most appropriate criteria to distinguish athletes for which GJH is clinically relevant, but it is the most reliable and validated tool currently available. The 5 part questionnaire is proposed to accurately identify GJH in 84% of cases (Hakim & Grahame, 2003a). The results of the 5 part questionnaire in this study indicate a prevalence of 48.2%, which is lower than the Beighton test. Participants accurately reported their ability to bend their thumb backwards with 100% correlation with objective testing. The ability to place the hands ﬂat on the ﬂoor was over estimated, with 63% of participants reporting the ability, versus 37% being able to demonstrate this on testing. Interestingly, only 26% of the participants considered themselves ‘double jointed’. This may represent an issue with perception of the condition or a misunderstanding of terminology. 4.4. Functional movement control
4.2. Dysautonomia The results indicate that symptoms suggestive of cardiovascular dysautonomia were not highly prevalent within this population, despite the high prevalence of GJH. There was only one case in which several symptoms were reported in combination with GJH and JHS. The preliminary interpretation of this concurs with the theory that exercise may help regulate autonomic function (Mathias et al., 2012). Hypermobile people with dysautonomia may be a separate group who do not achieve this level of ﬁtness. 4.3. Classifying hypermobility in sportspeople The Beighton et al. (1973) score was originally designed for use as a descriptive tool in an epidemiological survey. It has since seen an unprecedented proliferation in its use within research (Remvig, Jensen, & Ward, 2007b). It is assumed that the sample of joints included in the Beighton score correlate to hypermobility in other joints (Smits-Engelsman, Klerks, & Kirby, 2011). However, this simple method of classiﬁcation may fail to explore vital aspects of
The results of this study indicate that the hypermobile group (4/9) demonstrated increased postural instability, determined by increased posturographic values and decreased single leg stand time, compared to the non hypermobile group. This was a trend and not statistically signiﬁcant, but was consistently observed through all parameters of posturography. Further subgroup analysis comparing the distinctly hypermobile group (7/9) to all other participants revealed statistically signiﬁcant differences for path area and sway velocity on the left side. This concurs with previous research comparing sway velocity in patients with EDS hypermobility type to a control group (Rombaut et al., 2011). Previous research has also demonstrated statistical signiﬁcance for AP and lateral excursion and sway area (Galli et al., 2011; Rombaut et al., 2011). Whilst the trend in this study replicated this, results were not statistically signiﬁcant. The observed deﬁcit in postural control amongst hypermobile participants may be attributed to proprioceptive deﬁcits which have been well established in the literature (Fatoye et al., 2009; Rombaut et al., 2010). Previous research has indicated that
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exercise signiﬁcantly improves balance and proprioception in hypermobile individuals (Ferrell et al., 2004; Sahin et al., 2008). The smaller difference between groups in this study may be explained by the intensive training schedule which is completed by all participants, including proprioceptive training. Both Fatoye et al. (2009) and Rombaut et al. (2010) investigated bipedal standing conditions, whereas in this study, single leg standing was investigated. It was thought that bipedal standing would not suitably challenge the high level participants. However, it is possible that this was too challenging, resulting in high variability between attempts. This was also reported during the most challenging balance task in Rombaut et al.'s (2011) study. During the SEBT, a trend was observed in which participants with GJH achieved smaller normalised reach distances in all directions except posterior and posteromedial directions bilaterally, in which the hypermobile group performed better (Fig. 6). No previous research was identiﬁed which investigates performance on this test in hypermobile individuals. The SEBT demands a combination of balance, co-ordination, lower limb strength and ﬂexibility (Filipa, Byrnes, Paterno, Myer, & Hewett, 2010). Research has suggested that increased ﬂexibility improves SEBT performance (Gribble et al., 2009). It is possible that increased ﬂexibility in the hypermobility group may have confounded any deﬁcit in postural control in posterior and posteromedial reach directions. In addition, preliminary research has proposed that people with GJH may use different postural strategies to maintain stability during balance tasks, whereby they may ‘hang’ from passive joint structures rather than engaging active methods of control (Greenwood, Duffell, Alexander, & McGregor, 2011). 4.5. Limitations This pilot study recruited a small number of participants, which may have resulted in failure to reach statistical signiﬁcance in many of the tests and the possibility of type II error (Sim & Wright, 2000). It is recognised that the addition of a control group and researcher blinding would improve validity. 5. Conclusion A high prevalence of GJH was observed in this elite netball population. It is proposed that some of the characteristics of GJH may be advantageous to elite level netball performance. This preliminary study demonstrated that GJH appears to impair functional movement control in this group of elite level netballers, but to a lesser extent than previously demonstrated in sedentary individuals. It is thought that exercise may help normalise neuromuscular deﬁcits. Symptoms of dysautonomia were minimally prevalent in this population. It is recommended that subsequent, larger scale research is completed to further investigate the inﬂuence of hypermobility in elite athletes in terms of both functional movement control and injury risk. Conﬂict of Interest None declared. Ethical Approval Ethical approval for this study was granted by the University of Hertfordshire Health and Emergency Professions Ethics Committee (HEPEC reference 10/12/08). Written consent was obtained from all participants.
Funding None declared.
Acknowledgements The authors also would like to thank TASS and Bodybalance physiotherapy and sports injuries clinic who supported this study, the netball franchise and all participants who volunteered to take part and Dr Alan Hakim for his kind advice.
References Adib, N., Davies, K., Grahame, R., Woo, P., & Murray, K. J. (2005). Joint hypermobility syndrome in childhood. A not so benign multisystem disorder? Rheumatology (Oxford), 44(6), 744e750. €tterstro €m, R., Fride n, T., & Moritz, U. (2001). Individual factors Ageberg, E., Za affecting stabilometry and one-leg hop test in 75 healthy subjects, aged 15e44 years. Scandinavian Journal of Medicine & Science in Sports, 11(1), 47e53. Beighton, P., De Paepe, A., Steinmann, B., Tsipouras, P., & Wenstrup, R. J. (1998). Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK). American Journal of Medical Genetics, 77(1), 31e37. Beighton, P., Solomon, L., & Soskolne, C. L. (1973). Articular mobility in an African population. Annals of the Rheumatic Diseases, 32(5), 413e418. Bird, H. (2011). Hypermobility e does it cause joint symptoms? European Musculoskeletal Review, 6(1), 34e37. Bird, H., & Foley, E. C. (2013). Hypermobility in dancers. Rheumatology (Oxford), 52(4), 585e586. Bohannon, R. W., Larkin, P. A., Cook, A. C., Gear, J., & Singer, J. (1984). Decrease in timed balance test scores with aging. Physical Therapy, 64(7), 1067e1070. Boyle, K. L., Witt, P., & Riegger-Krugh, C. (2003). Intrarater and interrater reliability of the Beighton and Horan joint mobility Index. Journal of Athletic Training, 38(4), 281e285. Briggs, J., McCormack, M., Hakim, A. J., & Grahame, R. (2009). Injury and joint hypermobility syndrome in ballet dancersea 5-year follow-up. Rheumatology (Oxford), 48(12), 1613e1614. Burckhardt, C. S., & Jones, K. D. (2003). Adult measures of pain: the McGill Pain Questionnaire (MPQ), Rheumatoid Arthritis Pain Scale (RAPS), Short-Form McGill Pain Questionnaire (SF-MPQ), Verbal Descriptive Scale (VDS), Visual Analog Scale (VAS), and West Haven-Yale Multidisciplinary Pain Inventory (WHYMPI). Arthritis Care & Research, 49(S5), S96eS104. Clinch, J., Deere, K., Sayers, A., Palmer, S., Riddoch, C., Tobias, J. H., et al. (2011). Epidemiology of generalized joint laxity (hypermobility) in fourteen-year-old children from the UK: a population-based evaluation. Arthritis & Rheumatism, 63(9), 2819e2827. Collinge, R., & Simmonds, J. V. (2009). Hypermobility, injury rate and rehabilitation in a professional football squad e a preliminary study. Physical Therapy in Sport, 10(3), 91e96. Decoster, L. C., Bernier, J. N., Lindsay, R. H., & Vailas, J. C. (1999). Generalized joint hypermobility and its relationship to injury patterns among NCAA Lacrosse players. Journal of Athletic Training, 34(2), 99e105. Durall, C. J., Kernozek, T. W., Kersten, M., Nitz, M., Setz, J., & Beck, S. (2011). Associations between single-leg postural control and drop-landing mechanics in healthy women. Journal of Sport Rehabilitation, 20(4), 406e418. Fatoye, F., Palmer, S., Macmillan, F., Rowe, P., & van der Linden, M. (2009). Proprioception and muscle torque deﬁcits in children with hypermobility syndrome. Rheumatology (Oxford), 48(2), 152e157. Ferrell, W. R., Tennant, N., Baxendale, R. H., Kusel, M., & Sturrock, R. D. (2007). Musculoskeletal reﬂex function in the joint hypermobility syndrome. Arthritis & Rheumatism, 57(7), 1329e1333. Ferrell, W. R., Tennant, N., Sturrock, R. D., Ashton, L., Creed, G., Brydson, G., et al. (2004). Amelioration of symptoms by enhancement of proprioception in patients with joint hypermobility syndrome. Arthritis & Rheumatism, 50(10), 3323e3328. Filipa, A., Byrnes, R., Paterno, M. V., Myer, G. D., & Hewett, T. E. (2010). Neuromuscular training improves performance on the star excursion balance test in young female athletes. Journal of Orthopaedic & Sports Physical Therapy, 40(9), 551e558. Fox, Z. G., Mihalik, J. P., Blackburn, J. T., Battaglini, C. L., & Guskiewicz, K. M. (2008). Return of postural control to baseline after anaerobic and aerobic exercise protocols. Journal of Athletic Training, 43(5), 456e463. Galli, M., Rigoldi, C., Celletti, C., Mainardi, L., Tenore, N., Albertini, G., et al. (2011). Postural analysis in time and frequency domains in patients with Ehlers-Danlos syndrome. Research in Developmental Disabilities, 32(1), 322e325. Gannon, L. M., & Bird, H. A. (1999). The quantiﬁcation of joint laxity in dancers and gymnasts. Journal of Sports Sciences, 17(9), 743e750. Gazit, Y., Nahir, A. M., Grahame, R., & Jacob, G. (2003). Dysautonomia in the joint hypermobility syndrome. American Journal of Medicine, 115(1), 33e40.
K. Soper et al. / Physical Therapy in Sport 16 (2015) 127e134
Grahame, R., Bird, H. A., & Child, A. (2000). The revised (Brighton 1998) criteria for the diagnosis of benign joint hypermobility syndrome (BJHS). Journal of Rheumatology, 27(7), 1777e1779. Greenwood, N. L., Duffell, L. D., Alexander, C. M., & McGregor, A. H. (2011). Electromyographic activity of pelvic and lower limb muscles during postural tasks in people with benign joint hypermobility syndrome and non hypermobile people: a pilot study. Manual Therapy, 16(6), 623e628. Gribble, P. A., Hertel, J., & Plisky, P. (2012). Using the star excursion balance test to assess dynamic postural-control deﬁcits and outcomes in lower extremity injury: a literature and systematic review. Journal of Athletic Training, 47(3), 339e357. Gribble, P. A., Robinson, R. H., Hertel, J., & Denegar, C. R. (2009). The effects of gender and fatigue on dynamic postural control. Journal of Sport Rehabilitation, 18(2), 240e257. Grubb, B. P. (2008). Postural tachycardia syndrome. Circulation, 117(21), 2814e2817. Hakim, A. J., & Grahame, R. (2003a). A simple questionnaire to detect hypermobility: an adjunct to the assessment of patients with diffuse musculoskeletal pain. International Journal of Clinical Practice, 57(3), 163e166. Hakim, A., & Grahame, R. (2003b). Joint hypermobility. Best Practice & Research Clinical Rheumatology, 17(6), 989e1004. Hakim, A. J., & Grahame, R. (2004). Non-musculoskeletal symptoms in joint hypermobility syndrome. Indirect evidence for autonomic dysfunction? Rheumatology (Oxford), 43(9), 1194e1195. Hall, M. G., Ferrell, W. R., Sturrock, R. D., Hamblen, D. L., & Baxendale, R. H. (1995). The effect of the hypermobility syndrome on knee joint proprioception. British Journal of Rheumatology, 34(2), 121e125. Hertel, J., Gay, M. R., & Denegar, C. R. (2002). Differences in postural control during single-leg stance among healthy individuals with different foot types. Journal of Athletic Training, 37(2), 129e132. € m, P. (2004). General joint laxity in Jansson, A., Saartok, T., Werner, S., & Renstro 1845 Swedish school children of different ages: age- and gender-speciﬁc distributions. Acta Paediatrica, 93(9), 1202e1206. Juul-Kristensen, B., Kristensen, J. H., Frausing, B., Jensen, D. V., Røgind, H., & Remvig, L. (2009). Motor competence and physical activity in 8-year-old school children with generalized joint hypermobility. Pediatrics, 124(5), 1380e1387. Juul-Kristensen, B., Røgind, H., Jensen, D. V., & Remvig, L. (2007). Inter-examiner reproducibility of tests and criteria for generalized joint hypermobility and benign joint hypermobility syndrome. Rheumatology (Oxford), 46(12), 1835e1841. Kanjwal, K., Saeed, B., Karabin, B., Kanjwal, Y., & Grubb, B. P. (2010). Comparative clinical proﬁle of postural orthostatic tachycardia patients with and without joint hypermobility syndrome. Indian Pacing & Electrophysiology Journal, 10(4), 173e178. Keer, R. (2003). Physiotherapy assessment of the hypermobile adult. In R. Keer, & R. Grahame (Eds.), Hypermobility syndrome, recognition and management for physiotherapists (pp. 67e86). Edinburgh: Butterworth Heinemann. Konopinski, M. D., Jones, G. J., & Johnson, M. I. (2012). The effect of hypermobility on the incidence of injuries in elite-level professional soccer players: a cohort study. American Journal of Sports Medicine, 40(4), 763e769. Krivickas, L. S., & Feinberg, J. H. (1996). Lower extremity injuries in college athletes: relation between ligamentous laxity and lower extremity muscle tightness. Archives of Physical Medicine and Rehabilitation, 77(11), 1139e1143. McCormack, M., Briggs, J., Hakim, A., & Grahame, R. (2004). Joint laxity and the benign joint hypermobility syndrome in student and professional ballet dancers. Journal of Rheumatology, 31(1), 173e178. Mathias, C. J., Low, D. A., Iodice, V., Owens, A. P., Kirbis, M., & Grahame, R. (2012). Postural tachycardia syndromeecurrent experience and concepts. Nature Reviews Neurology, 8(1), 22e34. Moen, M. H., Tol, J. L., Weir, A., Steunebrink, M., & De Winter, T. C. (2009). Medial tibial stress syndrome: a critical review. Sports Medicine, 39(7), 523e546. Munro, A. G., & Herrington, L. C. (2010). Between-session reliability of the star excursion balance test. Physical Therapy in Sport, 11(4), 128e132. Murray, K. J. (2006). Hypermobility disorders in children and adolescents. Best Practice & Research Clinical Rheumatology, 20(2), 329e351.
Pacey, V., Nicholson, L. L., Adams, R. D., Munn, J., & Munns, C. F. (2010). Generalized joint hypermobility and risk of lower limb joint injury during sport: a systematic review with meta-analysis. American Journal of Sports Medicine, 38(7), 1487e1497. Plisky, P. J., Rauh, M. J., Kaminski, T. W., & Underwood, F. B. (2006). Star Excursion Balance Test as a predictor of lower extremity injury in high school basketball players. Journal of Orthopaedic & Sports Physical Therapy, 36(12), 911e919. Remvig, L., Jensen, D. V., & Ward, R. C. (2007a). Epidemiology of general joint hypermobility and basis for the proposed criteria for benign joint hypermobility syndrome: review of the literature. Journal of Rheumatology, 34(4), 804e809. Remvig, L., Jensen, D. V., & Ward, R. C. (2007b). Are diagnostic criteria for general joint hypermobility and benign joint hypermobility syndrome based on reproducible and valid tests? A review of the literature. Journal of Rheumatology, 34(4), 798e803. Robinson, R., & Gribble, P. (2008). Kinematic predictors of performance on the Star Excursion Balance Test. Journal of Sport Rehabilitation, 17(4), 347e357. Rombaut, L., De Paepe, A., Malfait, F., Cools, A., & Calders, P. (2010). Joint position sense and vibratory perception sense in patients with Ehlers-Danlos syndrome type III (hypermobility type). Clinical Rheumatology, 29(3), 289e295. Rombaut, L., Malfait, F., De Wandele, I., Thijs, Y., Palmans, T., De Paepe, A., et al. (2011). Balance, gait, falls, and fear of falling in women with the hypermobility type of Ehlers-Danlos syndrome. Arthritis Care & Research, 63(10), 1432e1439. Ruhe, A., Fejer, R., & Walker, B. (2010). The test-retest reliability of centre of pressure measures in bipedal static task conditionsea systematic review of the literature. Gait & Posture, 32(4), 436e445. Russek, L. N. (1999). Hypermobility syndrome. Physical Therapy, 79(6), 591e599. Sahin, N., Baskent, A., Cakmak, A., Salli, A., Ugurlu, H., & Berker, E. (2008). Evaluation of knee proprioception and effects of proprioception exercise in patients with benign joint hypermobility syndrome. Rheumatology International, 28(10), 995e1000. Scheper, M. C., de Vries, J. E., de Vos, R., Verbunt, J., Nollet, F., et al. (2013). Generalized joint hypermobility in professional dancers: a sign of talent or vulnerability? Rheumatology (Oxford), 52(4), 651e658. Scoppa, F., Capra, R., Gallamini, M., & Shiffer, R. (2013). Clinical stabilometry standardization: basic deﬁnitions e acquisition interval e sampling frequency. Gait & Posture, 37(2), 290e292. Simmonds, J. V., & Keer, R. J. (2007). Hypermobility and the hypermobility syndrome. Manual Therapy, 12(4), 298e309. Simpson, M. R. (2006). Benign joint hypermobility syndrome: evaluation, diagnosis, and management. Journal of the American Osteopathic Association, 106(9), 531e536. Sim, J., & Wright, C. (2000). Research in healthcare: Concepts, designs and methods. Cheltenham: Nelson Thornes Ltd. Smith, R., Damodaran, A. K., Swaminathan, S., Campbell, R., & Barnsley, L. (2005). Hypermobility and sports injuries in junior netball players. British Journal of Sports Medicine, 39(9), 628e631. Smits-Engelsman, B., Klerks, M., & Kirby, A. (2011). Beighton score: a valid measure for generalized hypermobility in children. Journal of Paediatrics, 158(1), 119e123. €derman, K., Alfredson, H., Pietil€ So a, T., & Werner, S. (2001). Risk factors for leg injuries in female soccer players: a prospective investigation during one out-door season. Knee Surgery, Sports Traumatology, Arthroscopy, 9(5), 313e321. Springer, B. K., & Pincivero, D. M. (2009). The effects of localized muscle and wholebody fatigue on single-leg balance between healthy men and women. Gait & Posture, 30(1), 50e54. Stewart, D. R., & Burden, S. B. (2004). Does generalised ligamentous laxity increase seasonal incidence of injuries in male ﬁrst division club rugby players? British Journal of Sports Medicine, 38(4), 457e460. Tinkle, B. T., Bird, H. A., Grahame, R., Lavallee, M., Levy, H. P., & Sillence, D. (2009). The lack of clinical distinction between the hypermobility type of EhlersDanlos syndrome and the joint hypermobility syndrome (a.k.a. hypermobility syndrome). American Journal of Medical Genetics Part A, 149A(11), 2368e2370.