Abstract
Purpose of Review
The objectives of this review are to explore the recent literature evaluating sports-related shoulder injuries among female athletes.
Recent Findings
Recent literature has highlighted sex-related differences in injury trends and patterns among athletes. Increased participation of women in both recreational and professional sports has resulted in increased exposure to injury. While men experience greater rates of shoulder injury overall, women tend to experience more overuse-related injuries. Evidence also suggests women are more susceptible to shoulder laxity and rotator cuff tears. In comparison to their male counterparts, women note poorer function, increased pain, and decreased activity level following shoulder injuries. Women may also be more likely to experience worse outcomes following surgical intervention. Sex-related differences in injury patterns and outcomes results from a combination of molecular and environmental influences, including hormone pathways, shoulder morphology, and differing rates of participation in, and athletic regulations among, certain sports.
Summary
Sex-related differences occur in how athletes sustain, experience, and recover from sports-related injuries. A comprehensive understanding of sex-related injuries enhances clinical decision making, treatment, and recovery. Further research is needed to clarify sex as an independent variable when evaluating sports-related shoulder injuries.
Keywords: Sex-related differences, Shoulder injuries, Female athletes, Sport-related injuries, Overuse injuries, shoulder instability
Introduction
In 2001, an Institute of Medicine report advocated for the evaluation of sex-related differences in all aspects of health research [1]. Since that time, the number of studies considering sex-related differences in orthopaedic surgery has significantly increased [2]. However, continued progress is necessary in the proportion of studies in which sex is considered an independent variable. While slightly over half of participants included in studies in high-impact orthopaedic journals are women, a minority (34%) of studies include gender in multifactorial statistical models [3••]. Of those, 39% demonstrate differences in outcomes between men and women.
Evaluating sex-based differences among athletes is vital as evidence suggests sex-based differences exist in how athletes incur, experience, and recover from sports-related injuries, as well as in injury trends over time [4–7]. Title IX, enacted in 1972, increased women’s access to organized athletics resulting in a subsequent increase in participation across all age groups. In tennis, female participation at the college level increased by nearly 2000 athletes between 1981–1982 and 2018–2019, representing a 30% increase [8]. Men’s tennis, on the other hand, increased by only 445 athletes over the same time period, a 6% increase. Accompanying increased participation in athletics is increased exposure to injury. USA Hockey, for example, reported a 34% increase in female adult ice hockey participation between 2007 and 2016 [9]. During this same time period, a study evaluating a sampling of emergency departments within the USA noted a concomitant increase (2.5-fold) in female adult hockey injuries presenting to medical attention, although this value did not reach statistical significance (P = 0.085) [7].
Despite increasing participation in athletics over recent decades, there continues to be a general paucity of literature examining how female athletes are differently affected by injuries, particularly as it relates to the shoulder. Orthopaedic studies evaluating sex-related differences among athletes have largely focused on lower extremity injuries such as ACL tears [10]. Upper extremity injuries, however, are common and occur in approximately 20% of NCAA Division I athletes [11]. While evidence suggests men sustain shoulder injuries at a higher rate, women participate in three of four NCAA sports with the highest upper extremity injury rates (softball, tennis, and volleyball), likely having a large impact on female athletes [12]. Failure to recognize and appropriately address the ways in which female athletes experience shoulder injuries may result in reduced performance or future inability to participate in athletics.
Sex-based differences in injury incidence occur not only at the collegiate level, but at all levels of play. A study of the Association of Tennis Professionals and Women’s Tennis Association demonstrates this disparity, with high-ranking female players sustaining injuries and leaving the sport at a higher rate than men [13]. At the Australian Open between 2011 and 2016, women sustained shoulder injuries at twice the rate of their male counterparts [14]. While the rate of shoulder injuries climbed among women during the time period studied (rate ratio 3.6 ± 5.8), it decreased among men (rate ratio 0.8 ± 0.8). Even after accounting for varying set regulations among men’s and women’s tennis, the increased rate of injuries among women persisted.
While studies suggest men sustain severe or operative shoulder injuries at a higher rate, much of the difference can largely be attributed to increased male participation in high-risk contact sports [15]. When excluding non-sex-comparable sports (e.g., those with varying regulations among genders), data demonstrate similar incidences and likelihoods of operative shoulder injuries. A 2018 evaluation of severe shoulder injuries among 25 NCAA sports, for example, found women’s gymnastics had the fourth highest incidence of operative shoulder injuries (0.44 per 10,000 athlete-exposures) [15]. When assessing the proportion of operative shoulder injuries, women’s lacrosse had the highest proportion of operative injuries (15.4%), followed by men’s football (9.9%). These data highlight the risk of severe shoulder injuries among female athletes, despite differences in regulations. Additionally, although women tend to participate in sports with less contact, several female-predominant sports such as volleyball, softball, and gymnastic place women at a high risk of shoulder injury via noncontact mechanisms. Each of these sports places high stress on the glenohumeral joint, either via overhand mechanisms or via uneven bars in gymnastics [16].
Understanding the overall impact and trends of shoulder injuries among female athletes is important for healthcare professionals, coaches, parents, and athletes in optimizing injury avoidance, treatment, and recovery. Here, we review recent literature on sex-based differences for specific shoulder injuries.
Atraumatic Shoulder Pain
While men experience greater rates of shoulder injury overall, women tend to experience more overuse-related injuries [17–19]. Among injuries reported in the National High School Sports-Related Injury Surveillance System between 2006–2007 and 2011–2012, female athletes experience overuse injuries at a rate of 1.88 per 10,000 athlete-exposures (AE), compared to 1.25 per 10,000 AE among male athletes (rate ratio 1.50, 95% CI 1.39–1.61) [18]. Overuse injury rates are prominent among female-predominant sports at the college level, as well. Data from 16 sports in the National Collegiate Athletic Association’s Injury Surveillance System between 2004–2005 and 2008–2009 demonstrate overuse injury rates of 8.85 (7.97–9.80) among women’s softball and 7.37 (6.56–8.25) among women’s volleyball [20]. Men’s baseball, on the other hand, shows an overuse injury rate of 6.13 (5.52–6.77). Comparative data on men’s volleyball was not included.
Increased rates of overuse injuries may be associated with increased sport-specific specialization. In their recent study of youth athletes, Post and colleagues found female athletes tend to be more often classified as “highly specialized” (53.8% of female athletes vs. 46.2% of male counterparts, P = 0.011), with greatest levels of specialization occurring prior to age 15 [21••]. Specialization was characterized by a perceived dedication to a particular sport. Declining participation in another sport to focus on one’s primary sport, the importance assigned to the particular sport by athletes, and the number of months per year athletes participated in their chosen sport all contributed to specialization determinations. Specialization was noted to be associated with an increase in both traumatic and overuse injuries. As specialization rates continue to increase in adolescence, overuse injury rates can be expected to follow. Increased overuse injuries, coupled with improper rehabilitation, may have long-lasting effects on an athlete’s performance and overall health.
Athletes participating in overhead sports are particularly susceptible to overuse injuries, with increased specialization effecting a large impact on injury risk [21••, 22]. Significant research efforts have been invested in evaluating overuse injuries among baseball players at all levels of play [23]. However, all overhead sports, including volleyball, handball, tennis, and softball, have high rates of overuse-related injuries [19, 20, 24]. In their 2017 study of 175 high school female volleyball athletes, Frisch and colleagues noted 40% of athletes reported experiencing atraumatic shoulder pain [22]. Two-thirds of those studied reported the pain recurred frequently. Increased specialization, as characterized by number of years played, weightlifting out of season, and number of contacts per week, was associated with increased atraumatic shoulder pain. Apart from specialization, players in the position of “hitters” also reported high levels of pain. While it may be hard to quantify the impact of atraumatic shoulder pain, 13% of the athletes missed practice or games to recover.
Despite high overuse injury rates, regulations governing athlete exposures among female athletes are notably absent. Among high school and college female softball athletes, for example, shoulder injuries comprise 81% of all time-loss injuries [25]. Although data suggests this is at least equivalent to that found among their male counterparts in baseball, in-depth explorations of softball pitch workload and injury association pale in comparison to studies among baseball players [20, 26]. The paucity of gender-specific exposure analyses may contribute to the absence of regulations governing pitch counts, innings pitched, or pitch exposures similar to those which exist at varying levels of baseball [27]. Similar counts should exist in volleyball and tennis for overhead hitting and serving.
Shoulder Instability
Shoulder stability is a complex process influenced by both static and dynamic stabilizers of the shoulder. Static stabilizers include the glenoid, labrum, and capsuloligamentous complex. Dynamic stabilizers, on the other hand, include the rotator cuff, deltoid and biceps tendon, which create concavity-compression of the humeral head into the glenoid. Injury to or laxity of any of these structures may contribute to the pathologic process of instability, which can occur in the anterior, inferior, or posterior directions. In 1980, Neer first described multidirectional instability as a distinct entity in which instability occurs in greater than one direction [28].
Multidirectional instability is thought to be more common among women, likely due to increased generalized joint laxity [29]. Higher Beighton scores, which have been noted to be greater among female adolescents [30], are associated with instability [31]. One large prospective study on shoulder instability by the Multicenter Orthopaedic Outcomes Network consortium (MOON) found average Beighton scores among women to be 2.76, compared to 0.65 among men (P < 0.001) [32••]. Women also demonstrated a greater percentage of scores greater than 5 (26.2% vs. 3.8% among men), indicating a greater degree of ligamentous laxity (Table 1).
Table 1.
The Beighton Score assesses generalized joint hypermobility. It is a 9 point scale evaluating upper limb movement, lower limb movement, and combined limb/spinal movement. A higher Beighton Score represents increased hypermobility [33]
| Maneuver | Positive finding | Scoring |
|---|---|---|
| Passive hyperextension of small finger MCP joint | > 90° | + 1 point per side, maximum score + 2 |
| Passive apposition of the thumb to the flexor aspect of the forearm | Thumb touches forearm | + 1 point per side, maximum score + 2 |
| Passive hyperextension of the elbow | > 10° | + 1 point per side, maximum score + 2 |
| Passive hyperextension of the knee | > 10° | + 1 point per side, maximum score + 2 |
| Active forward flexion of the trunk with knees fully extended | Palms rest flat on ground | + 1 |
The molecular basis of sex-based differences in shoulder instability is an area of ongoing research. Relaxin, a female hormone responsible for loosening pelvic ligaments to support childbirth, has been implicated in acute ACL pathology among female athletes [34, 35]. With receptors located on ligaments and cartilage, relaxin upregulates matrix metalloproteinases resulting in collagen breakdown within the extracellular matrix and altered mechanical properties [36]. Only recently, however, has relaxin been linked to shoulder instability [37]. In their prospective cohort study involving 1050 individuals, Owens and colleagues demonstrated for every 1-pg/mL increase in serum relaxin concentration, individuals were 2.18 times more likely to have shoulder instability (95% confidence interval, 1.01–4.76) [37]. Glenoid morphology may also contribute to greater glenohumeral instability among women. Studies have found women to have a more oval-shaped and thinner glenoid with greater inclination, which may predispose to greater instability [38, 39]. In fact, Owens and colleagues found coracohumeral interval to be a risk factor for anterior glenohumeral instability (HR, 1.20; 95% CI, 1.08–1.34; P = .001), with each 1 mm increase in coracohumeral distance associated with a 20% increased risk of shoulder instability [40]. While the biologic factors contributing to generalized joint laxity and glenohumeral instability are still being elucidated [41–43], studies demonstrate that sex-related differences become more pronounced following puberty [44, 45].
The mechanisms by and severity with which male and female athletes incur instability events also differ. Men, who comprise the majority of the literature on shoulder instability, are 2.7 times more likely to sustain an instability event, as defined by a subluxation or dislocation requiring medical attention and absence from participation of at least 1 day [6]. Men’s injuries are more likely due to contact with another athlete [6, 46], and have a higher rate (6.3 times higher) of season-ending shoulder instability [47]. Women, on the other hand, are more likely to experience traumatic shoulder instability after contact with the ground or an object [6]. Differences in the rate and mechanism by which female athletes sustain shoulder instability events is partially attributable to differences in participation in contact sports. Men’s ice hockey and lacrosse, whose female correlates have no-contact rules, account for a 2.17-fold difference in gender-related differences for shoulder instability [46]. Sex-comparable sports with similar contact rules on the other hand, such as rugby, have been shown to result in similar rates of glenohumeral instability among men and women [48].
The MOON study on shoulder instability offers further insight into sex-related differences in how men and women differently experience instability events [32••]. Results of the study demonstrate that while men and women experience an equivalent proportion of dislocations (compared to subluxations), men experience more traumatic instability. Women more frequently demonstrate capsular pathology, while men have increased rates of labral pathology and glenoid bone loss [32••, 49] (Fig. 1). Recognizing sex-related differences in injury is important due to its implications for treatment. In the previously mentioned MOON study, for example, men were more likely to undergo Latarjet procedures to address glenoid bone loss than women, who more frequently required soft tissue procedures to address greater capsular laxity [32••].
Fig. 1.
MRI and arthoscopic images of a posterior labral tear in a female athlete
In addition to distinct etiologies and treatment options, outcomes following shoulder instability events and shoulder stabilization procedures are not independent of the influence of sex. At the time of surgery, women have been noted to have worse baseline function (RAND-36, P < 0.001), greater pain (VAS, P < 0.001), and a decreased activity level [32••]. Even after shoulder stabilization procedures women may have lower Constant scores, greater levels of residual apprehension, and greater functional deficits [4, 50]. Female sex remains a risk factor for requiring revision stabilization procedures, independent of glenoid size [51, 52••]. Among throwing athletes who underwent arthroscopic posterior capsulolabral repair, female athletes comprised 55.5% of the revision and 23.4% of the no-revision group (P = 0.03) [51]. While no significant difference in outcomes was noted among individuals who required revision surgery, return to sport was significantly lower among the revision group (83.6% vs. 14.3%, P < 0.001). Even when athletes return to play, it is difficult to do so at a comparable level. When studying female professional tennis players, for example, Young and colleagues noted that while 88% returned to play following arthroscopic shoulder stabilization, they experienced a significant delay in or incomplete return to their prior singles ranking [53].
Rotator Cuff Injuries
Recent research into rotator cuff pathology suggests sex-related differences affect how women develop, experience, and recover from such injuries. Several studies have found female sex to be an independent risk factor for rotator cuff disease [54, 55]. In a cross-sectional study of 410 patients, female sex had an odds ratio of 2.07 for the development of rotator cuff pathology [55].
The development of rotator cuff disease is attributable to both genetic and environmental factors. Figueiredo and colleagues evaluated how genes affecting the tendon extracellular matrix differentially affect susceptibility to rotator cuff disease among men and women [56••]. Their study demonstrated certain single-nucleotide polymorphisms (SNPs) of MMP2, MMP3, and TIMP2 proteins were more strongly correlated with rotator cuff disease in females compared to males, in whom SNPs among collagen haplotypes such as COL5A1 and TGFBR1 altered susceptibility. Such research suggests tendinopathies may result from the distinct interactions of proteins within hormone-dependent pathways.
Increased shoulder laxity is also a risk factor for rotator cuff tendinopathy [57, 58]. Among the 2008 US Olympic Swimming Team, a positive sulcus sign was found to have an OR of 33.2 (95% CI, 3.09–355; P = .004) for rotator cuff tendinosis [58]. Such changes to the shoulder joint predispose to pain, with increased odds for impingement in the presence of a positive sulcus sign (OR 5.4, 95% CI, 0.80–36.3; P = .083). Swimmers, in particular, who benefit from shoulder laxity, have a high prevalence of rotator cuff disease. In the previously mentioned study of the 2008 US Olympic Swimming Team, 96% of those studied had evidence of tendinosis on ultrasound [58]. When evaluating female collegiate swimmers, Dischler and colleagues noted increased supraspinatus tendon thickness was positively associated with both years of participation in the sport (P = 0.01) and tendinosis (P = 0.02) [59].
In addition to increased susceptibility to rotator cuff tears, women report greater symptomatology. When evaluating the Western Ontario Rotator Cuff (WORC) index among men and women with rotator cuff tears, Razmjou and colleagues discovered women report greater levels of disability and interference with social functioning [60]. Similar to the results following shoulder stabilization surgery, women undergoing rotator cuff repair also have been found to experience greater pain and decreased function within the first three months, although these differences subside by one year [61••].
Understanding sex- and gender-related differences of rotator cuff tears should play an important role in treatment decisions to optimize outcomes for this population. Among an adolescent cohort, although girls comprised only 4.3% of non-operative injuries, they comprised 46.7% of operative rotator cuff injuries. [62]. The authors hypothesized that increased laxity among women may not only predispose them to rotator cuff disease, but also contribute to worse outcomes following physical therapy and continued symptoms of impingement. Consequently, women may be more likely to require operative treatment for partial tears.
Acromioclavicular Sprains
Much of the literature on acromioclavicular (AC) sprains among female athletes has focused on ice hockey. When evaluating female world cup hockey players, Tuominen and colleagues found shoulder injuries occurred at a rate of 0.5/1000 player-games, of which 50% were AC joint sprains [63]. Although studies demonstrate men experience AC joint sprains at a higher rate than women, women still sustain AC sprains at a rate of 2.12 (1.38–2.87) per 10,000 AE [64]. Notably, women are significantly more likely to experience AC sprains during competition than during practice [65, 66]. Hibberd and colleagues, who evaluated the epidemiology of AC sprains among NCAA athletes, found the largest difference between competition and practice injury rates existed in women’s ice hockey, with a rate ratio of 18.60 (95% CI 6.51–53.16). Injuries among female hockey players are most commonly due to contact with an apparatus or surface, which contrasts with the high rate of injuries sustained among male ice hockey players following contact with another player [64–66]. The difference in injury mechanism is largely attributable to differences in regulations, with body checking being allowed in men’s but not women’s hockey. Despite this, Lynall and colleagues found 38% of all injuries sustained in women’s ice hockey competitions are sustained due to contact with another player [66]. This data highlights that, despite altered regulations, women’s ice hockey remains a high-intensity contact sport, especially during competition. Consequently, women experience a similar proportion of AC sprains classified as “severe” and a similar percentage of shoulder injuries resulting in time loss as men [64, 65].
Clavicle Fractures
Similar to AC sprains, players in contact sports are at increased risk for fractures, including clavicle fractures. Approximately 7.8% of injuries among soccer field players are clavicle fractures [47]. Clavicle fractures are much more common in males than females, which likely reflects the difference in participation in high-risk contact sports [67]. Among sex-comparable high school sports, McCarthy and colleagues found boys sustained clavicle fractures at an injury rate of 1.03 per 100,000 AE compared to 0.35 for girls. Much of this difference is likely attributable to lacrosse in which, despite being considered a “sex-comparable” sport in the study, contact rules drastically differ. The clavicle fracture rate among boys lacrosse was 5.26 per 100,000 AEs compared to only 0.26 among girls lacrosse. Despite the lower incidence of clavicle fractures among female athletes, female sex has been identified as an independent risk factor for nonunion which has important implications for treatment and outcomes [68].
Conclusions
As demonstrated in our review, recent publications have improved our understanding of shoulder injuries among female athletes. While men experience higher rates of shoulder injury, women experience more overuse injury and are more susceptible to ligamentous laxity. Women have also been noted to experience greater disability from common shoulder injuries and may have poorer outcomes following operative intervention. Continued efforts to analyze sex as an independent variable remain critical to understanding how sex impacts the different ways in which female athletes sustain, experience, and recover from sports-related injuries. Delineating the ways in which biologic mediators and environmental variables converge to impact disease pathology and recovery remains essential to this process. Through deliberate efforts to generate sex-driven hypotheses, we may advance our knowledge of injuries in female athletes to lessen disease burden and optimize clinical outcomes. Focused studies on female athletes may contribute to the development of informed regulations regarding athlete exposures, aiding in injury prevention.
Funding
No funding was received.
Declarations
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
Conflict of Interest
Casey L. Wright, Jhillika Patel, and Carolyn Hettrich declare that they have no conflict of interest.
Footnotes
This article is part of the Topical Collection on Gender and Racial Disparities
Publisher’s note
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Contributor Information
Casey L. Wright, Email: clwright@bwh.harvard.edu
Jhillika Patel, Email: jpatel41@bwh.harvard.edu.
Carolyn M. Hettrich, Email: carolyn.hettrich@gmail.com
References
Papers of particular interest, published recently, have been highlighted as: •• Of major importance
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