Purpose: Adolescent females and males participating in running represent a population at high risk of stress fracture. Few investigators have evaluated risk factors for prospective stress fracture in this population.
Methods: To better characterize risk factors for and incidence of stress fractures in this population, we collected baseline risk factor data on 748 competitive high school runners (442 girls and 306 boys) using an online survey. We then followed them prospectively for the development of stress fractures for a mean ± SD of 2.3 ± 1.2 total seasons of cross-country and track and field; follow-up data were available for 428 girls and 273 boys.
Results: We identified prospective stress fractures in 5.4% of girls (n = 23) and 4.0% of boys (n = 11). Tibial stress fractures were most common in girls, and the metatarsus was most frequently fractured in boys. Multivariate regression identified four independent risk factors for stress fractures in girls: prior fracture, body mass index < 19, late menarche (age menarche ≥15 yr), and previous participation in gymnastics or dance. For boys, prior fracture and increased number of seasons were associated with an increased rate of stress fractures, whereas prior participation in basketball was associated with a decreased risk of stress fractures.
Conclusions: Prior fracture represents the most robust predictor of stress fractures in both sexes. Low body mass index, late menarche, and prior participation in gymnastics and dance are identifiable risk factors for stress fractures in girls. Participation in basketball appears protective in boys and may represent a modifiable risk factor for stress fractures. These findings may help guide future translational research and clinical care in the management and prevention of stress fractures in young runners.
1Division of Physical Medicine and Rehabilitation, Department of Orthopedic Surgery, Stanford University, Stanford, CA; 2Stanford Undergraduate Programs, Stanford University, Stanford, CA; and 3Division of Epidemiology, Department of Health Research and Policy, Stanford University, Stanford, CA
Address for correspondence: Michael Fredericson, M.D., 450 Broadway Street, Pavilion A, 2nd Floor MC 6120, Redwood City, CA; E-mail: firstname.lastname@example.org.
Submitted for publication September 2012.
Accepted for publication April 2013.
Stress fractures are a form of overuse injury that commonly occurs in athletes who participate in sports predisposing the bone to repetitive loading and mechanical stressors that exceed bone remodeling and adaptation. Stress fractures account for 0.7%–20% of all injuries sustained by athletes, and track-and-field athletes have the highest incidence of stress fractures (7). There is a recognized need for more prospective studies to identify risk factors for stress fractures in adolescent athletes (11), as prospective evaluation of risk factors for stress fractures or overuse musculoskeletal injuries in this population is limited (5,25–29). In the Growing Up Today Study, Field et al. (5). reported that 3.9% of female adolescent athletes developed a stress fracture over 7 yr and identified running, basketball, and cheerleading/gymnastics as sports particularly at high risk for stress fracture. Rauh et al. (25–27) have reported on the incidence of injuries in high school athletes, particularly cross-country runners, and noted that girls are at higher risk for both injury and reinjury than boys. Most other studies have been in runners older than 18 yr, and previous study investigators have identified prior stress fracture as a strong risk factor for future stress fracture for both sexes (14,18,34).
In girls, participation in lean sports such as distance running can negatively influence bone density through the female athlete triad. The female athlete triad is defined as the interrelationships between energy availability (with or without eating disorders), menstrual function, and bone mineral density (20). Athletes who participate in sports emphasizing leanness such as distance running may adopt restrictive eating behaviors that result in low energy availability. Low energy availability (≤30 kcal·kg−1 of lean body mass per day) has been shown to disrupt reproductive and metabolic hormones, which may lead to menstrual irregularities and altered bone microarchitecture (12,16). The end results are impaired bone health and increased stress fracture risk (20) and musculoskeletal injuries (28). Few prior prospective studies have been conducted to evaluate these relationships in high school–age female runners. Specific nutrients may also play a role in stress fracture risk in both male and female runners. Results from some prospective studies support the concept that calcium intake or calcium supplementation protects against stress fractures in older female runners (22) and military recruits (15), whereas other investigators have found no effect of increased calcium intake for stress fracture prevention in female adolescents participating in sports (29). Few prior published prospective studies performed report on the relationship between particular nutrients and stress fracture risk in male runners of any age or in high school–age female runners.
Participation in high-impact and odd-impact loading sports during adolescence may enhance bone density and geometry, whereas running involves repetitive lower-impact loads and has not been shown to clearly improve bone health (31). Participation in ball sports (basketball and soccer) during adolescence has been detected as protective against the development of stress fractures in adult female and male distance runners (8) and in the military (17). A similar evaluation of the crossover effects of prior sports participation in relationship to stress fracture risk in adolescent runners has not been previously reported.
The aim of our study was to identify sex-specific modifiable risk factors for stress fracture in runners. Understanding sex-specific risk factors and anatomical injury patterns may lead to better screening and management of stress fractures in the adolescent running population. We hypothesized that components of the female athlete triad (including menstrual irregularities, eating disorders, and behaviors), history of fracture, lower body mass index (BMI), and training factors (duration, intensity, and length of participation in running) would each be independent risk factors for stress fracture in female runners. In male runners, we hypothesized that prior fracture, lower BMI, training variables, and eating behaviors would be risk factors for stress fracture. In both sexes, we anticipated that prior participation in sports that emphasized leanness would contribute to stress fractures, whereas playing ball sports that involve high impact loading (basketball and soccer) would be protective against stress fractures.
Study design and recruitment
Details of study design and methods have been published previously (32,33). Subjects were recruited from September 2008 to December 2009 from 28 public and private high schools in the San Francisco Bay Area, Northern California. We invited teams to participate by contacting coaches through e-mail and at local high school cross-country and track-and-field events. Written permission was obtained from a high school administrator before visiting each school. At each school, the study investigators introduced the study and provided information regarding participation to the team.
To be eligible, athletes were in high school and participating in cross-country or track and field at time of enrollment. Those who were interested in participating in the study provided their names and were contacted by personalized e-mail. Reminder e-mails were periodically sent to subjects who did not complete the survey initially to increase enrollment. The e-mails contained information about the study, a unique study identifier, and the Web address to complete the online survey. Unique study identification codes were generated using random letters and numbers and assigned to each subject to allow for tracking the development of a stress fracture on subsequent surveys. Subjects were instructed to review information about the study with their parent or legal guardian before choosing to participate in the online survey. On the basis of the study design, the waiver for written informed consent was granted by our institutional review board, and we obtained online assent before subject participation. Each subject completed a self-administered online baseline questionnaire that took approximately 15 min to complete. Each subject was contacted after each competitive season with a link to a follow-up survey that confirmed participation in the prior season of cross-country and track and field and in the development of a stress fracture after each season for a goal of four consecutive seasons of prospective follow-up. Subjects were each compensated for their participation with a 15-dollar coupon to a local running store for their participation after completion of the initial and final surveys, and a 5-dollar gift card was provided for completing an interval survey after the second season of follow-up. The research protocol was approved by the institutional review board of Stanford University.
A series of online questionnaires was prepared using the program Surveyor, which allowed us to generate surveys hosted on a secure server. Collected data were encrypted and password protected (32). The baseline survey contained a series of questions designed to identify risk factors for the development of a stress fracture. Anthropometric variables, including age, height, weight, and ethnicity, were reported by each subject.
Training history and performance
Assessed training variables included the age of onset in competing in running races, the average weekly miles of running for the past year, the percentage of running occurring on either pavement or hills, and the training intensity (number of workouts and average speed during workouts). Each athlete was asked to report current or best estimated mile time and performance in the 5000-m cross-country events.
Prior injury and fracture
Athletes were instructed to report prior injuries from a list of common overuse injuries in long-distance runners, including the following: shin splints, sprained ankle, patellofemoral pain, iliotibial band syndrome, Achilles tendonitis, and plantar fasciitis. We asked subjects to include details for prior injuries sustained (including the type of injury, details on physician diagnosis, and imaging studies) in a text box provided for free response. Each subject was queried whether he or she had sustained a prior fracture. Subsequent questions requested subjects who sustained a fracture to provide more information to confirm the diagnosis, including anatomical location, physician diagnosis, and radiographic confirmation. When study investigators discovered incomplete responses from the initial questionnaire, subjects were contacted individually to obtain this information. For our baseline assessment of prior history of fracture, we included both traumatic fractures and stress fractures if they met the criteria of occurrence before study enrollment, physician diagnosis, and radiographic confirmation (radiograph, magnetic resonance imaging, or bone scan) in the spine or lower extremities. One spine fracture occurred in a female participant was coded as a prior fracture. Two additional fractures were included in athletes who did not report physician diagnosis or imaging but indicated casting was used for management of their fracture. Both fractures were coded as prior fractures.
Dietary intake and eating behaviors
We asked each subject to complete a series of questions regarding diet and eating behaviors on the baseline questionnaire, using questions similar to a prior published report (14). Assessed dietary variables included dairy intake (cups of milk and servings of dairy), intake of calcium-fortified foods, and consumption of beverages, including coffee, carbonated beverages (soda and energy drinks), and other caffeine-containing drinks. Subjects were provided answer choices for the frequency of consuming each item, in units per month, per week, or per day. These were converted and analyzed into daily intake (U·d−1). Subjects were asked to report the use of calcium supplements and multivitamins containing calcium and calcium dose in each. Assessed dietary behaviors included following a vegetarian diet, dieting or skipping meals to lose weight, and use of diet pills. All subjects were asked to report prior diagnosis of anorexia nervosa or bulimia nervosa. Female subjects completed an Eating Disorder Inventory (EDI) designed to identify subclinical eating disorders (10), whereby the total EDI score is composed of the sum of three subscales (drive for thinness, bulimic tendencies, and body dissatisfaction). Boys completed a series of questions about healthy and unhealthy eating behaviors adapted from Project EAT (21).
A full menstrual history was obtained from each female participant, including the age of menarche, the number of menstrual periods in the past year, the history of missing three or more menstrual periods for 1 yr, and the history of missing three or more menstrual periods for the past year. We defined current amenorrhea as having three or fewer periods in the past year or having primary amenorrhea (not reaching menarche by age 15 yr) (24). Late menarche was defined as age of menarche at 15 yr or older. Each female subject was asked whether a physician had previously diagnosed her with amenorrhea or oligomenorrhea. Girls were asked to report use of oral contraceptive pills.
Sports participation and cross-training
We requested each subject to report participation in sports outside of running. Because there is no other tool in the literature that investigates ball sport participation in high school athletes, we developed a questionnaire about this participation and participation in cross-training. This is a more extensive version of the Ball Sport Questionnaire that was published previously (8). The survey tool categorized loading activities: weight lifting, plyometrics, basketball, and soccer. This entailed the ages of participation in these sports, the number of hours per week, and whether participation was through a recreational, interscholastic, or club team. Similar questions were obtained on frequency and period for any upper or lower body weight lifting, plyometrics, or core-strengthening exercises. We also inquired about prior participation in the following sports: gymnastics, dance, volleyball, baseball, football, water polo, hockey, tennis, water polo, and swimming.
Measurement of the dependent variable: stress fracture
Participants were followed for the occurrence of stress fractures for a goal of four consecutive competitive seasons including interval training between seasons (cross-country, winter training, spring track, and summer training). All subjects and their coaches were instructed to notify the study investigators on the development of a suspected stress fracture. Subjects were contacted after each season using personalized e-mails and asked to complete an online survey that queried the development of a stress fracture. These surveys included whether an athlete sustained a stress fracture, date of injury, anatomical location, physician diagnosis, and imaging confirmation. Coaches were reminded each year to communicate the development of a stress fracture. Prospective stress fractures were counted if they occurred after enrollment in the study while the athlete was still participating in cross-country or track and field or while training for a running event (between running seasons or in preparation for a race). Prospective stress fractures that occurred during participation in nonrunning activities or stress fractures that occurred outside sports participation, including trauma, were excluded from analysis. Any missing or incomplete responses regarding a possible stress fracture were further clarified by contacting the subject directly. We excluded subjects with stress fractures that were not diagnosed by a physician (girls n = 11, boys n = 6), did not have radiographic confirmation (girls n = 1), or were associated with trauma (girls n = 2, boys n = 2). These subjects were included in the analysis in the nonfractured cohort.
Survey data results were stored on a secure server that is data encrypted and password protected. These data were merged with information on the prospective development of stress fractures, and two individuals independently reviewed the coded data. Analyses were performed with the SAS statistical package, version 9.1 (SAS Institute, Cary, NC) and via IBM SPSS (Armonk, NY) statistical software, version 20. Female and male athletes were analyzed separately. Characteristics of the population who sustained a stress fracture and the nonstress fracture cohort were compared using t-tests, Wilcoxon rank sum tests, χ2 tests, or Fisher’s exact tests, as appropriate. Univariate relationships between each independent variable and the rate of stress fractures were also assessed in univariate Cox proportional hazards models. We evaluated independent variables that have been previously assessed as potential risk factors for stress fractures by other investigators, including menstrual history (age of menarche, number of periods in past year, prior history of amenorrhea) (3,5,14), BMI (6), eating disorders (20), dietary intake of dairy and calcium (14,22,29), history of fracture (14,18,34), training variables (14), and prior sports participation (5,8,17). Variables that appeared significant or marginally significant in univariate analyses (P < 0.10 for girls, P < 0.15 for boys) were further evaluated in multivariate analyses. We used an iterative model building process to identify the most robust predictors of stress fracture. All variables retained in the multivariate model were significant at P < 0.05. The proportional hazards assumption was evaluated by examining log–log survival plots.
Our initial population enrolled was 748 subjects (girls n = 442, boys n = 306, equaling a completion rate of 62%) (33). Prospective follow-up data were collected for 97% of girls (n = 428) and 89% boys (n = 273), spanning a total of 11.4 ± 7.5 months and 2.3 ± 1.2 total seasons of cross-country and track and field.
A total of 44 incident stress fractures (girls n = 32, boys n = 12) occurred in 5.4% of female runners (n = 23) and 4.0% of male runners (n = 11). Nine girls and one boy sustained two stress fractures. Most common locations for developing a stress fracture in girls included the tibia (n = 14), femur (n = 8), fibula (n = 4), metatarsus (n = 4), and calcaneus (n = 2). For boys, the stress fractures were localized to the metatarsus (n = 7), tibia (n = 2), fibula (n = 2), and femur (n = 1). There were no differences in risk of stress fracture based on the high school an athlete attended.
Anthropometric characteristics and training variables: female runners
Table 1 shows descriptive characteristics of the study participants according to whether they sustained a prospective stress fracture. Table 2 shows the corresponding univariate hazard ratios for select variables for girls. In comparing individuals without a given risk factor, girls who were leaner at baseline (lower weight or BMI) were at three times greater risk to sustained a prospective stress fracture, as were those who ran more (twofold higher risk for athletes running >32 km·wk−1) or were more competitive (every 10-s improvement in the mile was associated with 9% increased risk of stress fracture).
Prior injury and fracture: female runners
Girls with a history of fracture before baseline had a sixfold greater risk of the development of a stress fracture. No other type of injury was associated with increased risk for sustaining a stress fracture.
Dietary intake and eating behaviors: female runners
Female runners with a history of eating disorders (anorexia nervosa or bulimia nervosa) were at five times greater risk for developing a stress fracture compared with those without a diagnosed eating disorder at baseline assessment. In contrast, higher EDI scores were not significantly associated with stress fracture risk. However, higher EDI scores correlated with increasing (rather than decreasing) weight and BMI in this population (data not shown). Girls who used a calcium supplement were three times more likely to sustain a prospective stress fracture. However, calcium supplementation was also strongly correlated with a history of fracture before baseline (data not shown). None of the other dietary variables were significantly associated with prospectively developing a stress fracture.
Multiple menstrual variables were significantly associated with prospective stress fractures, including late menarche (four times increased risk with age of menarche ≥15 yr), current amenorrhea (twofold greater risk), and fewer periods in the past year (each menstrual period was associated with 11% decreased risk of sustaining a stress fracture).
Sports participation and cross-training: female runners
Prior participation in dance or gymnastics was associated with four times greater risk to prospectively sustain a stress fracture, as was prior participation in tennis (threefold increased risk), although tennis participation was strongly associated with participation in dance or gymnastics.
Combined risk factors: female runners
In multivariate analyses (Table 2), significant independent risk factors for prospective stress fractures in girls were as follows: prior fracture, prior participation in dance or gymnastics, BMI < 19.0 kg·m−2, and late menarche. After accounting for these four variables, the remaining variables encompassing menstrual irregularity, mileage and running times, participation in tennis, eating disorders, and calcium supplementation were no longer significant (P > 0.10). After adjusting for other variables, the effect of calcium supplementation was 1.35 (P = 0.54); thus, the effect of this variable was almost completely attenuated after accounting for confounders.
In 23 girls who developed a stress fracture, we identified 21 who had one or more of the four identified risk factors (prior fracture, previous participation in gymnastics or dance, BMI < 19 kg·m−2, or late menarche), and 18 had two or more risk factors (Table 3). Among the girls with one or fewer risk factors (n = 319), the risk of prospective stress fracture was 1.6%; in contrast, among the girls with two or more risk factors (n = 109), risk was 16.5%. Among girls with three or more risk factors (n = 15), risk increased to 40%.
Anthropometric characteristics and training variables: male runners
Univariate analyses for boys is presented in Tables 4. None of the body composition variables were significantly related to prospective stress fracture; however, boys who developed a prospective stress fracture were slightly taller than those who did not. Boys who ran more mileage and were more competitive (faster mile and 5000-m times) were somewhat more likely to develop a prospective stress fracture, although these associations did not reach statistical significance (P < 0.15).
Prior injury and fracture: male runners
We observed a sevenfold greater risk for prospective stress fracture in boys with a history of fracture before baseline. However, there were no clear associations between a history of nonbone injuries and prospective stress fractures.
Sports participation and cross-training: male runners
Prior participation in basketball was associated with 81% decreased risk for prospective stress fracture, and each competitive season of participation in running during follow-up was associated with two times greater risk for developing a stress fracture. Boys who participated in plyometrics exercises were nearly three times more likely to sustain a prospective stress fracture (P = 0.07) in univariate analysis. Boys who did plyometrics ran more miles, had faster running times, and were more likely to have fractured before baseline (data not shown).
Combined risk factors: male runners
In boys, multivariate analysis identified prior fracture and a greater number of competitive seasons during follow-up as the most robust risk factors for prospective stress fracture and prior participation in basketball as a protective factor (Table 4). Boys who participated in a greater number of competitive seasons had a greater opportunity to develop a stress fracture while running, so this variable reflects different at-risk windows and is not helpful as a clinical predictor of stress fracture. Of the 11 boys that developed stress fracture, nine had one or both of the two clinically relevant risk factors (prior fracture and lack of previous participation in basketball; Table 5). Among the boys with neither risk factor (n = 167), the risk of prospective stress fracture was 1.2%; among the boys with exactly one risk factor (n = 100), risk was 7.0%. Among boys with both risk factors (n = 6), risk increased to 33.0%, although the denominator is small.
In our prospective study of competitive high school runners, we were able to identify risk factors common and unique to each sex. The strongest risk factor for developing a stress fracture in both sexes was a history of prior fracture. Unique risk factors in girls included delayed menarche, low BMI and prior participation in gymnastics or dance. In boys, stress fractures were more common with increased exposure to running quantified by number of seasons of participation. Overall, 5.4% of girls and 4.0% of boys sustained one or more stress fractures for 11.4±7.5 months. Our findings add to the limited number of prospective studies performed to identify risk factors for stress fractures in adolescent females (5,29) and musculoskeletal injuries (25–28) in adolescent runners. Unlike previous investigators, we did not find a significantly elevated rate of stress fractures in female runners compared with male runners (13,19). This may be due to insufficient statistical power. However, our findings do agree with results from a prior study in track-and-field athletes ages 17–26 yr, where study investigators did not detect differences in stress fracture incidence by sex (4). We also note that most stress fractures for female runners occurred in the tibia and for male runners, the metatarsus. Our findings are in partial agreement with reports of the tibia being the most common site of stress fractures in 18- to 26-yr-old cohort of female runners (14) and 17- to 26-yr-old female and male track-and-field athletes (4).
The observation of prior fractures being common in boys who subsequently sustain stress fractures (34) and the absence of other identifiable risk factors for stress fracture are consistent with prior findings in older male track-and-field athletes ages 17–26 yr (3). In boys, we were able to identify a possible activity that may reduce stress fractures in runners. Male runners who participated in basketball were at lower risk of developing stress fractures, consistent with prior reports (8,17). Milgrom et al. (17) observed that premilitary induction participation in ball sports, primarily basketball for at least 2 yr, was associated with a lower rate of stress fractures during infantry basic training. Milgrom et al. (17) demonstrated greater in vivo tibial strain measurements measured in rebounding over running activities that may stiffen bones and result in lower rate of stress fractures (17). Fredericson et al. (8) observed the association of prior ball sports participation in stress fracture prevention for older elite track-and-field runners. We did not detect a difference in ball sports participation and stress fracture rate in female athletes in our study. Our findings may be explained by the high number of risk factors, including late menarche, that may attenuate benefits of ball sports in preventing stress fractures (8). Frost and Schönau (9) have suggested bone strength is influenced by muscle forces and strain acting on bone during childhood and adolescence. The influence of ball sports on increased muscle strength and the association of muscle strength to stress fractures cannot be determined based on our study design. Our observational findings in our younger population of male runners strengthen the relationship of prior participation in basketball as being protective against stress fractures.
We detected prior participation in gymnastics and dance as predictive of increased stress fracture risk in girls. Like running, gymnastics and dance are sports that emphasize leanness; and we hypothesize that cumulative exposure to sports that emphasize leanness may result in negative health behaviors that aversely affect bone density and strength. Our finding is somewhat surprising because prior investigators studying elite and highly competitive gymnasts demonstrated that high-impact loading encountered in gymnastics greatly improves bone density (23,30). Athletes in our population may have had more modest participation than athletes in these prior studies; thus, the negative aspects of the sport’s emphasis on leanness may have outweighed any bone benefits conferred by the high-impact loading.
In addition to gymnastics or dance participation, identified risk factors for stress fracture in girls from our univariate analysis included prior fracture, lower BMI, prior participation in tennis, menstrual irregularities, running greater than 32 km·wk−1, faster running performances, calcium supplementation, and a history of anorexia or bulimia. However, our multivariate modeling identified prior fracture, prior participation in dance or gymnastics, BMI <19 kg·m−2, and late menarche as the strongest independent predictors for developing a stress fracture. In the multivariate model, prior fracture was associated with a sixfold increase in the rate of stress fracture, and low BMI, late menarche, and prior participation in dance or gymnastics were associated with two- to threefold increases in the rate of stress fracture. Prior stress fracture as a risk factor for future stress fracture has been reported in older runners (14,18,34). Long-term participation in endurance running has been negatively associated with low bone mineral density and may influence bone health through interactions of low energy availability and menstrual irregularities (2). Lower BMI has been associated with reduced bone mineral density in adolescent female runners (1) and increased rate of stress fractures female infantry recruits (6). Our findings of association between late menarche and increased stress fracture risk have been previously described in adolescent female athletes (5) and track-and-field athletes ages 17–26 yr (3).
The risk factors identified in multivariable analysis (fracture, BMI <19 kg·m−2, late menarche, and prior gymnastics or dance participation) appear to have a cumulative effect on increasing risk of stress fractures in girls. Most stress fractures (18 of 23) occurred in the 109 girls who had at least two of the risk factors. Of the 15 girls, 6 had at least three of the four risk factors fractured (40%). These risk factors are relatively easy to measure and thus may represent a set of screening questions to determine female runners at higher risk for the development of stress fractures.
We were unable to detect increased intake of calcium or dairy as protective against stress fracture, consistent with a prior report in adolescent females (29). However, we may have lacked sufficient power to detect these effects. For girls, drinking more cups of milk tended to decrease stress fracture risk, although this was not statistically significant (hazard ratio = 0.77 per additional cup of milk, P = 0.16). In prospective study in female runners 18 to 26 yr old, Nieves et al. (22) suggested a protective effect for milk drinking and intake of calcium from foods against stress fractures. Lappe et al. (15) reported on a randomized trial of calcium and vitamin D supplementation in female military recruits that demonstrated a protective effect for supplements against stress fracture. In our cohort, calcium supplementation was associated with an increased risk of stress fracture in female runners. We observed that girls who took calcium supplements were more likely to have a fractured before baseline and were also more likely to show signs of the female athlete triad (menstrual irregularities and low BMI). As a result, a greater number of girls who prospectively developed a stress fracture may have been taking calcium supplements because they were aware that they were at heightened risk. After adjustment for these confounding factors, the hazard ratio for calcium supplementation was close to null. Both calcium and vitamin D have been shown to contribute to overall bone health and remain important for adolescent athletes who have yet to reach peak bone density.
Limitations of our study include the small number of stress fractures detected and the possible introduction of recall bias, given that athletes were asked to self-report injuries and risk factors. Our research design addressed this by assigning subject ID codes and ensuring confidentiality to all subjects. We cannot exclude that some stress fractures may not have been detected on follow-up, although we asked both athletes and coaches to report stress fractures to study investigators. We found excellent agreement in independent report of stress fractures by athletes and coaches, and we were able to obtain additional information to confirm suspected stress fractures through e-mail. To minimize recall bias, we contacted subjects after each season to remind them to report new or suspected stress fractures. We accounted for the different length of participation and time to prospective stress fracture in our analysis by using a Cox time-dependent regression model. Some stress fractures occurred after the athlete began to run in college, and many baseline variables are likely to change with time. We assessed dietary behaviors using an EDI and requested information on quantities of types of food rich in calcium consumed at baseline assessment, but we did not collect food diaries or prospective dietary behaviors. We are unable to detect these changes based on study design. Despite these limitations, our study has significant strengths, including reporting on a large cohort of both female and male athletes participating in a sport that is at high risk for stress fractures. Although recruitment and surveillance in a young population may be difficult, we were able to enroll most potential subjects and to obtain follow-up data from most subjects. Our population contains a large proportion of self-identified Caucasians and Asian/Pacific Islander, two ethnicities at increased risk for low bone density. We demonstrate a novel approach in using electronic online surveys to conduct research in an adolescent population (32).
In summary, we identified that both young female and male runners are at risk for stress fractures, and prior fracture is a common risk factor. In addition, stress fractures in female runners may be more likely in athletes with BMI <19 kg·m−2, late menarche, and history of participation in gymnastics or dance. Screening for these risk factors may help identify young athletes at higher risk for stress fractures. Prior participation in basketball appears protective against stress fracture in male runners and may represent a form of loading activity that promotes bone health. Translational research on optimal timing, duration, and frequency of ball sport or similar loading activities may provide advances for strategies to optimize bone health and to prevent stress fractures. Future studies should examine how these risk factors can be used to guide prevention and management of stress fractures in adolescent runners.
The authors are grateful for funding support from the 2010 Richard S. Materson Education Research Fund New Investigator Research Grant, the 2008 Medical Student Research Grant awarded by the Education Research Fund for Physical Medicine and Rehabilitation, and the Medical Scholars Research Program awarded to Adam Tenforde. Michael Fredericson has ongoing consultancy with Cool Systems, Inc., and receives payment for lectures and royalties from OPTP. For the remaining authors, no conflicts of interest were declared. Dr. Hervé Collado, Dr. Shelley MacDonald, and John McGuire helped with data collection and recruitment.
The authors thank Dr. Dianne Neumark-Sztainer for the permission to use Project EAT questions. They also thank the athletes for their participation and the coaches and school administrators for their assistance.
The published findings and conclusions do not constitute endorsement by the American College of Sports Medicine.
1. Barrack MT, Rauh MJ, Nichols JF. Prevalence of and traits associated with low BMD among female adolescent runners. Med Sci Sports Exerc
. 2008; 40 (12): 2015–21.
2. Barrack MT, Rauh MJ, Nichols JF. Cross-sectional evidence of suppressed bone mineral accrual among female adolescent runners. J Bone Miner Res
. 2010; 25 (8): 1850–7.
3. Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in track and field athletes. A twelve-month prospective study. Am J Sports Med
. 1996; 24 (6): 810–8.
4. Bennell KL, Malcolm SA, Thomas SA, Wark JD, Brukner PD. The incidence and distribution of stress fractures in competitive track and field athletes. A twelve-month prospective study. Am J Sports Med
. 1996; 24 (2): 211–7.
5. Field AE, Gordon CM, Pierce LM, Ramappa A, Kocher MS. Prospective study of physical activity and risk of developing a stress fracture among preadolescent and adolescent girls. Arch Pediatr Adolesc Med
. 2011; 165 (8): 723–8.
6. Finestone A, Milgrom C, Evans R, Yanovich R, Constantini N, Moran DS. Overuse injuries in female infantry recruits during low-intensity basic training. Med Sci Sports Exerc
. 2008; 40 (11 Suppl): S630–5.
7. Fredericson M, Jennings F, Beaulieu C, Matheson GO. Stress fractures in athletes. Top Magn Reson Imaging
. 2006; 17 (5): 309–25.
8. Fredericson M, Ngo J, Cobb K. Effects of ball sports on future risk of stress fracture in runners. Clin J Sport Med
. 2005; 15 (3): 136–41.
9. Frost HM, Schönau E. The “muscle–bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab
. 2000; 13 (6): 571–90.
10. Garner DM, Olmsted MP, Polivy J. Development and validation of a multidimensional Eating Disorder Inventory for anorexia nervosa and bulimia. Intl J Eat Disord
. 1983; 2: 15–34.
11. Heyworth BE, Green DW. Lower extremity stress fractures in pediatric and adolescent athletes. Curr Opin Pediatr
. 2008; 20 (1): 58–61.
12. Ihle R, Loucks AB. Dose–response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res
. 2004; 19 (8): 1231–40.
13. Iwamoto J, Takeda T, Sato Y, Matsumoto H. Retrospective case evaluation of gender differences in sports injuries in a Japanese sports medicine clinic. Gend Med
. 2008; 5 (4): 405–14.
14. Kelsey JL, Bachrach LK, Procter-Gray E, et al. Risk factors for stress fracture among young female cross-country runners. Med Sci Sports Exerc
. 2007; 39 (9): 1457–63.
15. Lappe J, Cullen D, Haynatzki G, Recker R, Ahlf R, Thompson K. Calcium and vitamin d supplementation decreases incidence of stress fractures in female navy recruits. J Bone Miner Res
. 2008; 23 (5): 741–9.
16. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab
. 2003; 88 (1): 297–311.
17. Milgrom C, Simkin A, Eldad A, Nyska M, Finestone A. Using bone’s adaptation ability to lower the incidence of stress fractures. Am J Sports Med
. 2000; 28 (2): 245–51.
18. Nattiv A. Stress fractures and bone health in track and field athletes. J Sci Med Sport
. 2000; 3 (3): 268–79.
19. Nattiv A, Casper J, Abdelkerim A, Dorey F, Hecht S, Puffer JC. Female track and field athletes are at increased risk for stress fractures. Med Sci Sports Exerc
. 2002; 34 (5 suppl): S157.
20. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine Position Stand. The female athlete triad. Med Sci Sports Exerc
. 2007; 39 (10): 1867–82.
21. Neumark-Sztainer D, Story M, Hannan PJ, Perry CL, Irving LM. Weight-related concerns and behaviors among overweight and nonoverweight adolescents: implications for preventing weight-related disorders. Arch Pediatr Adolesc Med
. 2002; 156 (2): 171–8.
22. Nieves JW, Melsop K, Curtis M, et al. Nutritional factors that influence change in bone density and stress fracture risk among young female cross-country runners. PM R
. 2010; 2 (8): 740–50; quiz 94.
23. Pikkarainen E, Lehtonen-Veromaa M, Kautiainen H, Heinonen OJ, Viikari J, Mottonen T. Exercise-induced training effects on bone mineral content: a 7-year follow-up study with adolescent female gymnasts and runners. Scand J Med Sci Sports
. 2009; 19 (2): 166–73.
24. Practice Committee of American Society for Reproductive Medicine. Current evaluation of amenorrhea. Fert Steril
. 2008; 90 (11 Suppl): S219–25.
25. Rauh MJ, Koepsell TD, Rivara FP, Margherita AJ, Rice SG. Epidemiology of musculoskeletal injuries among high school cross-country runners. Am J Epidemiol
. 2006; 163 (2): 151–9.
26. Rauh MJ, Koepsell TD, Rivara FP, Rice SG, Margherita AJ. Quadriceps angle and risk of injury among high school cross-country runners. J Ortho Sports Phys Ther
. 2007; 37 (12): 725–33.
27. Rauh MJ, Margherita AJ, Rice SG, Koepsell TD, Rivara FP. High school cross country running injuries: a longitudinal study. Clin J Sport Med
. 2000; 10 (2): 110–6.
28. Rauh MJ, Nichols JF, Barrack MT. Relationships among injury and disordered eating, menstrual dysfunction, and low bone mineral density in high school athletes: a prospective study. J Athl Train
. 2010; 45 (3): 243–52.
29. Sonneville KR, Gordon CM, Kocher MS, Pierce LM, Ramappa A, Field AE. Vitamin D, calcium, and dairy intakes and stress fractures among female adolescents. Arch Pediatr Adolesc Med
. 2012; 166 (7): 595–600.
30. Taaffe DR, Robinson TL, Snow CM, Marcus R. High-impact exercise promotes bone gain in well-trained female athletes. J Bone Miner Res
. 1997; 12 (2): 255–60.
31. Tenforde AS, Fredericson M. Influence of sports participation on bone health in the young athlete: a review of the literature. PM R
. 2011; 3 (9): 861–7.
32. Tenforde AS, Sainani KL, Fredericson M. Electronic Web-based surveys: an effective and emerging tool in research. PM R
. 2010; 2 (4): 307–9.
33. Tenforde AS, Sayres LC, McCurdy ML, Collado H, Sainani KL, Fredericson M. Overuse injuries in high school runners: lifetime prevalence and prevention strategies. PM R
. 2011; 3 (2): 125–31; quiz 31.
34. Touhy J, Nattiv A, Streja L. A prospective analysis of tibial stress fracture incidence, distribution and risk factors in collegiate track athletes. Clin J Sport Med
. 2008; 18 (2): 186.
Keywords:© 2013 American College of Sports Medicine
BONE HEALTH; EPIDEMIOLOGY; FEMALE ATHLETES; MALE ATHLETES; LONG-DISTANCE RUNNERS