Risk Factors, Diagnosis and Management of Bone Stress Injuries in Adolescent Athletes: A Narrative Review

hysical activity is known to be bene cial for bone; however, some athletes who train intensely are at risk of bone stress injury (BSI). Incidence in adolescent athlete populations is between 3.9 and 19% with recurrence rates as high as 21%. Participation in physical training can be highly skeletally demanding, particularly during periods of rapid growth in adolescence, and when compe- tition and training demands are heaviest. Sports involving running and jumping are associated with a higher incidence of BSI and some athletes appear to be more susceptible than others. Maintaining a very lean physique in aesthetic sports (gymnastics, gure skating and ballet) or a prolonged negative energy balance in extreme endurance events (long distance running and triathlon) may compound the risk of BSI with repetitive mechanical loading of bone, due to the additional negative effects of hormonal disturbances. The following review presents a summary of the epidemiology of BSI in the adolescent athlete, risk factors for BSI (physical and behavioural characteristics, energy balance and hormone disruption, growth velocity, sport-speci c risk, training load, etc.), prevention and management strategies. Keywords:bone stress injury; adolescent; athletes; stress fracture; injury management; risk factors 1. Introduction Bone stress injuries (BSI) are typically associated with

following review presents a summary of the epidemiology of BSI in the adolescent athlete, risk factors for BSI (physical and behavioural characteristics, energy balance and hormone disruption, growth velocity, sport-speci c risk, training load, etc.), prevention and management strategies. Keywords:bone stress injury; adolescent; athletes; stress fracture; injury management; risk factors 1. Introduction Bone stress injuries (BSI) are typically associated with athletic or occupational overuse loading of the skeleton. The primary negative consequence of bone stress injuries (BSI) is time loss from training and competition which, at the elite junior level (speci cally, under age 20), may have profound implications for professional opportunities. More broadly, BSIs represent a public health concern from the perspective that they may hinder ongoing participation in physical activity. While numerous factors have been associated with the incidence of BSI, the extent to which each factor contributes to the development of stress fractures in the young athlete is yet to be fully understood. The following is a consolidation of the literature around stress fractures and BSI in adolescent athletes, including epidemiology, risk factors, diagnosis, management and prevention, with a focus on the highest quality evidence. 2. De ning Stress Fracture and Bone Stress Injury (BSI) Stress fractures are focal structural weaknesses in bone occurring in response to the repeated application of stresses below the fracture threshold. The term bone stress injury (BSI) encompasses a range of bone tissue disturbances resulting from prolonged repetitive loading ranging from periostitis (in ammation of the periosteum), to periosteal, endosteal and bone tissue oedema (in ammation of the bony linings, or within the cortical bone tissue itself), to partial or complete stress fracture. All may be referred to as bone stress reactions or bone stress injuries; however, stress reaction typically denotes a less severe stage than stress fracture [1,2]. Sports2021,9, 52.

Sports2021,9, 52 2 of 24 As bone is well supplied with nociceptors, BSIs tend to be painful and disruptive to athletic pursuits, although bone stress apparent on nuclear medicine bone scan and MRI is not consistently symptomatic [3,4]. Furthermore, pain severity is not well correlated with radiological severity [5]. Bones remodel in response to changes in type or intensity of chronic mechanical loading in order to adapt their density and morphology to best withstand future loads of the same nature (a phenomenon re ecting Wolff's Law) [6]. It is this precise reason that exercise is bene cial for bone. In some cases, the adaptive process is insuf ciently rapid to replace localised microdamage which, with further loading, can coalesce into one or more stress fractures. Furthermore, the process of remodelling and repair of microdamage involves an initial stage of resorption before new bone is formed [7]. It has been hypothesised that this transient period of increased porosity temporarily places bone at greater risk of further tissue damage under ongoing loading, thus creating a positive feedback cycle culminating in even greater risk of stress fracture [8]. The in uence of adolescent growth on this cycle is not fully understood, but there is no evidence to suggest a different process occurs in the growing athlete. Microdamage and repair may manifest with degrees of upregulated metabolism (such as periostitis) and/or in ammation in or around the bone tissue (oedema) which may or may not be symptomatic or radiologically evident [3]. Attempts to categorise BSI severity clinically and radiologically have been only moderately successful [5]. This complexity, coupled with marked individual differences in pain perception and tolerance [9,10], accounts for the spectrum of bone tissue disturbances referred to as BSIs, the disparity in abilities to tolerate similar forms and intensities of training, and marked variation in times to recovery. Athletes training in a sport involving dominant limb use such as tennis, high jump and long jump have long exhibited greater BMD (bone mineral density) or cross-sectional area in the dominant limb [11]. For exercise to stimulate bone adaptation, loading must be high-magnitude and/or applied

to tolerate similar forms and intensities of training, and marked variation in times to recovery. Athletes training in a sport involving dominant limb use such as tennis, high jump and long jump have long exhibited greater BMD (bone mineral density) or cross-sectional area in the dominant limb [11]. For exercise to stimulate bone adaptation, loading must be high-magnitude and/or applied rapidly. Examples include jumping, hopping and bounding as well as progressive resistance and power training, whereas swimming and cycling are relatively ineffective [12]. Bone also responds positively to unusual or novel forms of loading [13]. 3. Epidemiology of Bone Stress Injuries in Adolescent Athletes Lifetime prevalence of athletic stress fracture is reportedly 10% [14] but reports of incidence in adolescence range between 0.8 and 19% [15–18]. Teenagers may be more at risk of bone stress injury than young adults, with those aged 15–19 representing the largest proportion af icted in an athletic population (42.6%) [19,20]. Additionally, recurrence rates may be up to 21% in collegiate sport, thus attention to management of risk factors in this age group is indicated [15]. 3.1. Commonly Affected Sites In athletes under the age of 20, 77% of stress fractures reportedly occur in the lower limb [21]. A description of 389 BSI occurring in high school athletes across a variety of sports, reported stress fractures occurring most commonly in the leg (40.3%), foot (34.9%), and lumbar spine or pelvis (15.2%), with upper limb and thoracic BSI being relatively uncommon (2.8%) [16]. It is possible this pattern of prevalence is a function of relative exposure and the sports represented, rather than a greater predisposition of the lower limb bones to BSI. Tibial BSI predominantly occur in sports that include repetitive jumping/landing (basketball and gymnastics) and running. Incidence of tibial BSIs in adolescent runners has been reported as 0.29/1000 AE (athletic exposures) for stress reactions and 0.06/1000 AE for stress fractures [22]. The most common location is the distal two thirds of the tibia, more speci cally, at the junction of the mid to distal thirds [23], which corresponds to the narrowest cross section of the tibia

Incidence of tibial BSIs in adolescent runners has been reported as 0.29/1000 AE (athletic exposures) for stress reactions and 0.06/1000 AE for stress fractures [22]. The most common location is the distal two thirds of the tibia, more speci cally, at the junction of the mid to distal thirds [23], which corresponds to the narrowest cross section of the tibia and the likely site of greatest strain during loading [24]. In pre-professional dancers, BSI can represent up to 19% of injuries over an academic year, with tibial stress fractures taking the longest time to return

Sports2021,9, 52 3 of 24 to full dance [17]. When managed conservatively, tibial BSI may require 6–27 weeks to return to sport depending on severity [2,25,26]. 3.2. Sports-Speci c Bone Stress Injury An overview of bones affected by BSI in childhood and adolescence is summarised in Table, along with the sports or activities commonly associated with them. Several studies have compared risk of BSI across different sports. While trends are evident, it is dif cult to fully ascertain risk by sport as the gamut of sports compared, age of participants, and levels of training have been inconsistent between studies. Table 1.Stress fracture locations in adolescent athletes, related sports, and associated activities.Location Examples of Sports Additional Considerations Tibia Running (endurance and track) [18,22] Basketball, netball, volleyball [16,19] Gymnastics [27] Ballet [17] Figure Skating [28] Track and Field [16,19] 19.4% recurrence in collegiate athletes [15]. Include medial malleolus stress fracture or reaction in running or jumping athletes [29] Metatarsal (Figure) Running (athletics) [20] Gymnastics [27] Basketball [21,30] Volleyball [15] Ballet [17,31,32] Most common bone affected in runners and highest rate of recurrence in collegiate athletes (29.2%) [15,18] Fifth metatarsal stress fractures have a high risk of delayed healing or non-union (Jones' Fracture) [33] Pre-professional and young professional dancers experience more metatarsal stress fractures than senior professional dancers [31,32]. May re ect self-selection bias, i.e., injured dancers not progressing to professional level. Tarsals (cuneiform, navicular, talus, calcaneus, cuboid) Athletics [20] Basketball [16,21] Soccer (football) [16] Lacrosse [16] Figure skating [28] Ballet [17,29] Consider tarsal coalition and bipartite navicular for differential diagnosis [34] Cuboid stress fractures are uncommon and may present similarly to an ankle sprain. CT diagnosis may be required [35] Comprise 13–19% of injuries in junior gure skaters [36] Fibula Running (track) [15] Soccer [15] Basketball [15] Figure skating [28] 9.7% prevalence in collegiate athletes [15] Lumbar spine Cricket [4,37,38] Tennis/Racquet sports [39] Gymnastics [15] Ballet [32] Recurrence in 22.2% of collegiate athletes [15] Common presentation on opposite side to the dominant throwing arm or kicking leg and commonly, L5 vertebral level is affected [39] May span several vertebral levels in cricketers

[15] Soccer [15] Basketball [15] Figure skating [28] 9.7% prevalence in collegiate athletes [15] Lumbar spine Cricket [4,37,38] Tennis/Racquet sports [39] Gymnastics [15] Ballet [32] Recurrence in 22.2% of collegiate athletes [15] Common presentation on opposite side to the dominant throwing arm or kicking leg and commonly, L5 vertebral level is affected [39] May span several vertebral levels in cricketers [38] Associated with repetitive lumbar extension with or without rotation for example, arabesques, gymnastic walk-overs, ips or pitching/bowling [4,32] Pars stress reactions and fractures are known to be among the top ve most frequent paediatric sports injuries for both sexes [40] Sesamoid Running (endurance) [41] Soccer (football) Basketball and volleyball [19] Ballet [41] Common in sports requiring weightbearing on an extended rst toe. Possible association with pronation of the foot or hallux valgus [29,42]

Sports2021,9, 52 4 of 24 Table 1.Cont. Location Examples of Sports Additional Considerations Ribs Rowing [43] Baseball/Pitching sports [19,44] Tennis [19] Swimming [45] Reported 8–16% incidence during rowing career and associated with sudden increase in training load, poor rowing biomechanics or a change in rowing blade [19,43,46] First rib BSI may present as pain in the dominant posterior shoulder or upper thorax [44] Olecranon and medial epicondyle Baseball [19,47] May occur following repetitive valgus stress forces and olecranon traction via the triceps tendon in pitching or throwing sports [19,47] Pelvis/Sacrum Running (endurance and athletics) [18] Football (Soccer) (kicking, sprinting or cutting) [19] Both have a high proportion of trabecular bone, thus may be related to energy availability and menstrual regularity [48–51] Osteitis pubis (stress reactions at the pubic symphysis) often occur in adolescent and adult footballers [52] Femur Running (endurance and athletics) [15,53] Coxa varum of the femur may be a contributing factor [53] Wrist (Distal radius and carpal) Diving [54] Tennis [55,56] Gymnastics [27] Distal radial epiphyseal bone stress injuries may occur in children and adolescents yet to experience growth plate closure [57,58] Patella Gymnastics [59] Jumping sports (e.g., volleyball) [60] Very rare [19] Consider bipartite patella as differential diagnosis [59] Running as a mechanism of injury may account for up to 50.5% of BSI in athletes under 20 years of age [21]. Runners who have had prior involvement in ballet or gym- nastics (aesthetic sports) have a higher risk of developing stress fractures than ball sports competitors, the reasons for which are not fully understood [18]. Aside from running (50.5%), in 222 cases, other stress fracture provoking activities include throwing (7.7%), jumping (6.7%), kicking (3.8%) and hitting a ball (3.4%) [21]. Many sports involve a combi- nation of running and kicking, or running and jumping, thus differentiating one speci c precipitating factor is challenging. Ball sport athletes generally have higher than average bone mass, and individuals with a history of participation in ball sports as adolescents appear to be protected from stress fractures in future athletic activity [18,61]. However, playing ball sports involves considerable running and can therefore

running and kicking, or running and jumping, thus differentiating one speci c precipitating factor is challenging. Ball sport athletes generally have higher than average bone mass, and individuals with a history of participation in ball sports as adolescents appear to be protected from stress fractures in future athletic activity [18,61]. However, playing ball sports involves considerable running and can therefore be associated with incidence of BSIs in adolescent athletes at the time of involvement [16]. Female high school athletes participating in ball sports such as soccer, volleyball and basketball appear to experience a higher incidence of BSI than their male counterparts, particularly in the lumbar spine and lower limb [16,21,62]. Incidence of BSI in aesthetic sports (10%) may be even higher than endurance sports (such as running; 8%), with prevalence in technical or ball sports being negligible by comparison [20]. The progression of gymnasts and gure skaters (aesthetic athletes) into elite level competition (Olympic level) during adolescence likely results in higher training loads at younger ages than other sports [63], which may partly account for the higher prevalence of BSI in these young athletes.

Sports2021,9, 52 5 of 24Sports 2021, 9, x 5 of 25 Figure 1. Coronal plane MRI of T2 weighted image of 2nd metatarsal stress fracture (as indicated by the green arrow) in 14-year-old ballet student training 25–30 h per week. The risk of stress fracture in swimmers is not lower than those participating in impact sports [12] and may include upper extremity and rib BSIs. Although swimmers are un- likely to sustain lower extremity impact-related BSI while swimming [16], low BMD due to the weight-supported nature of the sport may render swimmers susceptible to BSI dur- ing lower limb-loading cross training activities [51]. Stress fractures at highest risk of poor or delayed healing include the anterior tibia, superior femoral neck, medial malleolus, talus, navicular, proximal fifth metatarsal, pel- vis, hallux sesamoids and patella; likely as a result of high tensile loading and/or poor blood supply [29]. 4. Risk Factors for Bone Stress Injuries in Adolescent Athletes Sudden changes in training, low energy availability, race, previous stress fracture, bone mineral density (BMD), genetics, sex, biomechanics, hormone disruption, medica- tions, and exercise history are broadly considered to be risk factors for BSI at any age [42,64,65]. The extent to which each factor contributes to the development of stress frac- tures in the young athlete is yet to be fully understood and likely differs from individual to individual [66]. 4.1. Training Load and Early Specialisation A change (type, intensity, surface, apparel) in training is the most common precursor to BSI, theoretically a function of the adaptive response to altered mechanical loading. A particularly intense period of increased or altered loading or inadequate rest predisposes to injury during the aforementioned window between the bone resorption and bone for- mation phases of bone remodelling [23,29]. A high number of weekly training hours may also place an athlete at increased risk of BSI by virtue of the accumulation of load related microdamage [20,67]. Training load describes the relationship between training volume (time) and training intensity (physiological demand) [68]. An increase in either volume or intensity will therefore affect risk of BSI [67]. As all athletes and

A high number of weekly training hours may also place an athlete at increased risk of BSI by virtue of the accumulation of load related microdamage [20,67]. Training load describes the relationship between training volume (time) and training intensity (physiological demand) [68]. An increase in either volume or intensity will therefore affect risk of BSI [67]. As all athletes and sports are different, there is no known training threshold at which BSI are likely to occur. Of the female teenage athletes from The Japan Institute of Sport, those completing a higher number of training hours per week were most likely to sustain a stress fracture [20]. Others have shown that female adolescents exercising 12–16 h or more per week have an increased risk of BSI [30,67,69]. In one prospective study, 90% of Figure 1. Coronal plane MRI of T2 weighted image of 2nd metatarsal stress fracture (as indicated by the green arrow) in 14-year-old ballet student training 25–30 h per week. The risk of stress fracture in swimmers is not lower than those participating in impact sports [12] and may include upper extremity and rib BSIs. Although swimmers are unlikely to sustain lower extremity impact-related BSI while swimming [16], low BMD due to the weight-supported nature of the sport may render swimmers susceptible to BSI during lower limb-loading cross training activities [51]. Stress fractures at highest risk of poor or delayed healing include the anterior tibia, superior femoral neck, medial malleolus, talus, navicular, proximal fth metatarsal, pelvis, hallux sesamoids and patella; likely as a result of high tensile loading and/or poor blood supply [29]. 4. Risk Factors for Bone Stress Injuries in Adolescent Athletes Sudden changes in training, low energy availability, race, previous stress fracture, bone mineral density (BMD), genetics, sex, biomechanics, hormone disruption, medications, and exercise history are broadly considered to be risk factors for BSI at any age [42,64,65]. The extent to which each factor contributes to the development of stress fractures in the young athlete is yet to be fully understood and likely differs from individual to individual [66]. 4.1. Training Load and Early Specialisation A change

sex, biomechanics, hormone disruption, medications, and exercise history are broadly considered to be risk factors for BSI at any age [42,64,65]. The extent to which each factor contributes to the development of stress fractures in the young athlete is yet to be fully understood and likely differs from individual to individual [66]. 4.1. Training Load and Early Specialisation A change (type, intensity, surface, apparel) in training is the most common precursor to BSI, theoretically a function of the adaptive response to altered mechanical loading. A particularly intense period of increased or altered loading or inadequate rest predisposes to injury during the aforementioned window between the bone resorption and bone formation phases of bone remodelling [23,29]. A high number of weekly training hours may also place an athlete at increased risk of BSI by virtue of the accumulation of load related microdamage [20,67]. Training load describes the relationship between training volume (time) and training intensity (physiological demand) [68]. An increase in either volume or intensity will therefore affect risk of BSI [67]. As all athletes and sports are different, there is no known training threshold at which BSI are likely to occur. Of the female teenage athletes from The Japan Institute of Sport, those completing a higher number of training hours per week were most likely to sustain a stress fracture [20]. Others have shown that female adolescents exercising 12–16 h or more per week have an increased risk of BSI [30,67,69]. In one prospective study, 90% of stress fractures recorded occurred in adolescent females training for 1 h per day [70],

This review summarizes the epidemiology, risk factors, and management strategies for BSI in adolescent athletes.