POPP, KRISTIN L.1; HUGHES, JULIE M.1; SMOCK, AMANDA J.1; NOVOTNY, SUSAN A.1; STOVITZ, STEVEN D.2; KOEHLER, SCOTT M.3; PETIT, MOIRA A.1
Stress fractures are among the most prevalent sports injuries, particularly in sports involving running, jumping, and repetitive cyclic loading (6,17). Stress fractures differ from traumatic or osteoporotic fractures in that they occur in the absence of an acute traumatic event. Stress fractures have been diagnosed in as many as 20% of athletes, up to 50% of which occur in the distal two-thirds of the tibia, at the point of maximum tensile stress due to bending (22). The highest prevalence of stress fractures among athletes is reported in members of track and field teams with rates from 10% to 31% (17). Stress fractures are also a common occurrence in military basic training. US military reports from the recruit populations indicate an incidence rate of 0.9%-5.2% for men and 3.4%-21.0% for women (25). Other countries report stress fractures in as many as 49% of their military recruits (12).
Ultimately, a stress fracture represents the inadequate adaptation of bone in response to the mechanical loads imposed upon it, resulting in damage to the bone accruing faster than it can be repaired (7). Microscopic cracks in the bone form, which, without a break in loading, can coalesce into macrocracks. If the damage continues to occur without adequate time to be repaired, a stress fracture will result (7).
Owing to the prevalence of stress fractures in the military and athletic population, as well as the costly nature of the injury in terms of recovery time, it is important to understand the causative factors. These factors fall into two categories: factors that affect bone strength (bone mineral density, bone geometry, age, genetics, nutrition, endocrine and hormonal status, exercise or loading history, and bone disease) and factors that affect the mechanical load on bone (changes in loading intensity and frequency, training surface, footwear, body size and composition, and biomechanical factors) (7). Although there are numerous risk factors within these two areas thought to contribute to the occurrence of stress fracture, the exact etiology remains unknown.
From a bone perspective, numerous studies have focused on assessing surrogates of bone strength-particularly bone mineral density. Although several previous studies have explored the relationship of areal bone mineral density (aBMD, g·cm−2) assessed by dual-energy x-ray absorptiometry (DXA) to stress fractures, the findings remain controversial (1,4-6,8,10,23). Studies that found differences imply that bone "density" is lower in those with a history of stress fracture. However, there are several limitations to using a two-dimensional DXA assessment of aBMD for estimating bone strength. Bone geometry and mechanically meaningful assessments of bone strength can change with or without a change in aBMD (15,16). A few studies suggest that geometric parameters may be helpful for predicting stress fracture risk (3,4,13,21). One particularly strong study in a military population showed that female military recruits who subsequently fractured had smaller cortical bone area than controls at the 33% site of the tibia (4). However, most of these studies used DXA-derived bone geometric parameters, which, because they are done in two dimensions, involve estimations that may fail to depict true bone geometry. Further, few studies have accounted for muscle size, which could be an important predictor of bone strength and stress fracture risk (4,6). Therefore, studies using measurement techniques such as peripheral quantitative computed tomography (pQCT), which is capable of assessing bone structure and volumetric bone mineral density (vBMD), are needed. Thus, the primary purpose of this study was to explore differences in tibial bone strength in competitive female distance runners with and without a history of stress fractures. Our secondary aim was to explore differences in bone geometry, bone volumetric density, and muscle size that may underpin bone strength differences. We hypothesized that female distance runners with a history of stress fracture will have lower bone strength because of smaller total tibial cross-sectional area (CSA) than runners with no history of stress fracture. Although previous research supports this hypothesis, there have been no studies assessing these measurements using pQCT technology in an athletic population.
Competitive female distance runners (aged 18-35 yr) were recruited from the Twin Cities metropolitan area. "Competitive" was defined as having a competitive season(s) each year in which three or more distance races are completed. Participants competed in multiple distance events ranging from 5 km to the marathon during their competitive seasons. To be eligible for the study, athletes must have run an average of ≥25 miles·wk−1 during their competitive season. Runners were recruited by; emails to coaches of collegiate teams within the metropolitan area, a flyer in the twin cities marathon newsletter, flyers posted in the recreation center at the University of Minnesota campus, and through word of mouth. A total of 43 runners agreed to participate in the study and completed the screening questionnaire. In a screening questionnaire, participants were asked a series of screening questions related to stress fracture history, competition and training status, and basic health. Participants were excluded if they had a stress fracture at the time of study (n = 3), had a history of an eating disorder (n = 1), medication use (other than oral contraceptives) known to influence bone metabolism (n = 0), or were pregnant at the time of the study (n = 0). A pregnancy test was administered to all participants before any pQCT scans. After exclusion, the remaining 39 participants were classifed into a stress fracture group (SFX, n = 19) and a nonstress fracture group (NSFX, n = 20) depending on whether they have had a stress fracture in the femur (n = 4), shank bones (n = 12) or any bone in the foot (n = 6) in the past 5 yr. Three participants in the SFX group have had a stress fracture in more than one location. On average, the participants' most recent stress fracture occurred 3 yr (±1.5 yr) before study participation. This study was approved by the internal review board (IRB) of the University of Minnesota. All participants signed an informed consent form in accordance with IRB guidelines before participation in the study.
Participants were required to visit the Laboratory for Musculoskeletal Health for approximately 1.5 h on one occasion. After consent, anthropometry, questionnaires, bone health, and aerobic fitness were assessed.
Each participant's height was measured to the nearest millimeter, using a wall-mounted stadiometer (Seca Model 242, Hanover, MD). Weight was measured on a calibrated electronic scale (Seca Model 840) to the nearest 0.1 kg. Tibial length was measured to the nearest millimeter by standard method using an anthropometric tape. All measurements were taken twice, and the mean of two measurements was used.
Questionnaires assessing training history, health history, sport-related injury, and stress fracture history as well as past/current oral contraceptive use were administered. The eating attitudes test (EAT-26) was used to assess eating attitudes and had been used in numerous studies including several assessing runners (14,24). General history of health, physical activity, menstrual status, running training, and stress fracture was assessed by brief questionnaires developed in our laboratory.
Bone volumetric density, geometry, and strength were assessed with peripheral quantitative computed tomography (pQCT; XCT 3000; Orthometrix, White Plains, NY). Participants were required to sit with one leg extended for ∼30 min for each limb. Scans were taken at the distal region (4% of the length) and along the midshaft (15%, 25%, 33%, 45%, 50%, and 66%) of each tibia. Each participant's leg was positioned using a customized leg hold (Bone Diagnostic, Inc., Fort Atkinson, WI). A Velcro strap was used to ensure each participant's leg remained stationary during scan acquisition. A scan speed of 25 mm·s−1 and a sampling resolution (voxel size) of 0.4 mm were used according to the manufacturer's recommendation. The anatomic reference line was determined by acquisition of a 30-mm planar scout view of the joint line. The distal (4%) trabecular site of the tibia was assessed for total bone CSA (ToA, mm2) and total volumetric density (ToD, mg·mm−3). At the distal site, bone strength was estimated using the bone strength index (BSI, mg·mm−4) calculated as ToA × ToD2/100,000. The low- and midshaft cortical regions (15%-66%) of the tibia were assessed for geometric parameters ToA, cortical area (CoA, mm2), and cortical volumetric density (CoD, mg·mm−3). Bone strength at these sites was estimated using the polar strength-strain index (SSIp, mm3). Muscle CSA (MCSA, mm2) was assessed at the 66% site.
One trained operator (K.P.) performed all measurements as well as the scan analysis. Repositioning precision in our laboratory was determined in adults (women n = 11, men n = 4, age = 25.8 ± 6.5 yr) as a coefficient of variation (CV, %) and varied from 0.28% to 1.2% for all measurements. Quality assurance was performed daily using the cone phantom provided by the manufacturer. Because there are currently no standardized analysis protocols for pQCT studies analyzing the present target population, the modes and thresholds used in this study are similar to those based on the manufacturer's recommendations.
Maximal aerobic capacity.
V˙O2max testing was performed to assess fitness levels in runners. Participants were asked to complete the Physical Activity Readiness Questionnaire (2) before V˙O2max testing. A Medgraphics metabolic cart (CPX Ultima; Medical Graphics Corporation, St. Paul, MN) was used for gas analysis. HR was monitored using Polar brand HR monitors and watches. Before the max test, each participant completed a 5-min walking warm-up at 3.1 mph. The test protocol was adjusted for individual fitness level in that participants started at a pace corresponding to 2 mph slower than their self-reported easy-run pace. The speed was then increased by 0.4 mph·min−1 for the first 6 min followed by a 1°·min−1 increase in incline until self-reported fatigue. This protocol was a modification of a V˙O2max protocol developed for runners (28).
Data were analyzed using SPSS (v15.0) statistical software. Means and 95% confidence intervals are reported for each group. Descriptive characteristics were compared between groups using unpaired t-tests. Differences in bone outcomes were assessed using ANCOVA. To control for body size, we adjusted for tibial length. Although not statistically significant, mean age was slightly different between groups so we also adjusted for age in all analyses. In a second model, we added MCSA as a covariate to determine whether differences in bone geometry and strength remained after MCSA was controlled for. Differences were considered significant if P ≤ 0.05.
To establish if fracture region influenced the results, we compared bone strength and geometry outcomes between runners with tibial stress fractures compared with other fractures and found no differences between these groups (data not shown). Results were also similar if those with nonshank fractures were excluded from the analyses. We therefore included individuals with any fracture in the analyses.
Values for descriptive variables for the females in both the SFX and NSFX group are displayed in Table 1. Overall, participants ranged in age from 18 to 35 yr were 47-66 kg and had normal body mass index (BMI, 17-23 kg·m−2). Participants had been running for 2-20 yr averaging 20-55 miles·wk−1 and maximal aerobic capacity ranged from 42.6 to 63.8 mL·kg−1·min−1, indicating that runners were well trained. Runners in both groups reported completing 60-75 min of strength training each week on average. Mean values for body size and training variables were not different between groups (P > 0.05 for all). There was no significant difference in EAT-26 scores between groups, and no scores were indicative of eating disorders. Birth control use as well as age of menarche and menstrual status was similar between groups with most participants in each group averaging more than 10 cycles per yr.
Bone density, geometry, and strength.
Comparisons of pQCT values for bone and muscle parameters between the SFX group and NSFX group adjusting for age and tibial length are presented in Table 2. Before adjusting for MCSA, nearly all bone geometric and strength variables at the cortical sites (15%-66%) tended be lower in the SFX group for both the right and left legs. SFX participants had significantly smaller CoA at the 45%, 50%, and 66% sites (Fig. 1A). Differences became more pronounced moving proximally along the tibia and were similar on the left and right limbs (regardless of fracture location). At the 45% site, participants in the SFX group had 7.0% and 6.8% smaller CoA than the NSFX group for the right and left legs, respectively. At the 50% site, there was a 7.7% difference in both legs, and at the 66% site, results were similar, yielding a 7.9% and 7.8% difference for the right and left legs, respectively. Estimates of bone strength (SSIp) at the 50% and 66% sites were also significantly different (Fig. 1B). Participants in the SFX group had a significantly lower (9.2% and 9.0%) SSIp at the 50% site as well as the 66% site (9.0% and 9.5%) than the NSFX group in the right and left legs. Mean MCSA was also significantly lower (8%) in the SFX group after adjusting for tibial length and age. Interestingly, after adjusting for MCSA, differences were no longer significant at any site.
We assessed tibial vBMD, bone strength, bone geometry, and MCSA by pQCT in female distance runners and showed significantly higher estimates of bone strength, at the 45%, 50%, and 66% sites, in runners with a history of stress fracture compared with those without. Differences in bone geometry underpinned strength differences. However, because MCSA was also significantly lower in runners with a history of stress fracture, differences in skeletal parameters were no longer significant after adjusting for MCSA. These data highlight the importance of assessing bone structure and strength when investigating skeletal pathologies and indicate an important role of muscle size in stress fracture etiology. Each of these points will be discussed in detail below.
Bone strength differences.
The first important finding of this study is lower bone strength in runners with a history of lower limb stress fractures compared with runners without a history of stress fracture. SSIp was ∼9%-10% lower in the SFX group at the 50% and 66% sites on both the left and the right tibias (P ≤ 0.05 for all). Our findings are consistent with previous studies that used two-dimensional technology such as radiographs and DXA to estimate bone geometry. Milgrom et al. (21) were among the first to estimate bone strength in individuals with stress fracture by deriving cortical dimensions from tibial radiographs to estimate area moments of inertia (I), an indicator of bone bending strength. Results showed smaller values of I in fracture cases in accordance with higher bending stresses. Beck et al. (3,4) found similar results in two separate prospective studies using DXA to estimate bone strength in military recruits. Results of these studies showed smaller cross-sectional moments of inertia and section moduli among those who experienced a stress fracture as well as thinner cortices in female fracture cases. In contrast, Bennell et al. (5) used computerized tomography to estimate strength differences in participants with and without a stress fracture and found no significant differences between groups. However, measurements were taken only at the 33% site of the tibia. Our results suggest that significant differences in bone strength did not occur at sites distal to the 50% site.
Structural underpinnings of strength differences.
The structural basis for the lower bone strength in the SFX group was a significantly lower CoA (−3.2% to −4.0%, P < 0.05) within a similar diameter bone and similar total CSA-indicating thinner cortices. However, there was no significant difference in vBMD between groups. Again, our findings are consistent with those of Beck et al. (4) who showed that female fracture cases had similar tibial diameters but thinner cortices using the DXA hip structure analysis program. A smaller cortical area with similar bone diameter in SFX could be due to either greater endocortical resorption or reduced apposition. Beck et al. (3) suggested that differences in bone strength and geometry in military personnel may be attributed to lower baseline physical fitness levels among stress fracture participants (4). However, results in our study suggest that SFX participants have thinner cortices but similar bone diameter despite equivalent aerobic fitness levels. Because there were no significant differences between groups in descriptive variables, miles run per week, or aerobic fitness, the differences in bone strength are likely due to other factors. It is possible that there is a relationship between muscle size and bone strength that contributes to the thicker cortices in NSFX participants. This theory is discussed in greater detail in the following sections. The difference in bone structure between groups may be due to various genetic factors. Further research is needed to further explore these findings.
MCSA is an important determinant of bone morphology.
When bone measurements were adjusted for MCSA, differences in bone parameters were no longer significant between groups, suggesting that participants in both groups had bones that were adequately adapted to their MCSA regardless of fitness, training, or nutritional factors. Although the cross-sectional nature of the study precludes the ability to make causal inferences, these findings are consistent with the mechanostat and related theories (11,26), which suggest that bone adapts its strength to the highest peak voluntary loads. Because muscles produce the highest loads on bone (19), bone strength should be adapted to muscle force. We did not measure muscle force directly, rather we used muscle size (MCSA) as a surrogate measure. Future studies should include a more direct assessment of muscle force such as the peak force during a countermovement jump (9).
Muscle and stress fracture etiology
MCSA at the 66% site of the tibia was significantly smaller in stress fracture subjects compared with controls, both before and after adjusting for age, tibial length, and weight. A common belief in much of the stress fracture literature is that muscle can play both a causative and a protective role in the occurrence of stress fractures (7). The damaging role muscles play in stress fracture etiology is evident in the case of rowers, in whom stress fractures of the ribs, exposed to muscle torque rather than external reaction forces, are common (18,20). At the same time, muscle has the ability to absorb 100 more times the shock than a bone of the same length (12), suggesting that muscle can play a large role in protecting bones from absorbing excessive shock, stress, or strain. Because stress fractures are most common in the tibia, research on the etiology of stress fractures at other sites is limited. In an effort to understand loading characteristics of the tibia during running, Sasimontonkul et al. (27) found that both the peak compressive and shear forces acting on the tibia occurred during the midstance of running gait rather than at impact. This suggests that muscle pull produces more force on bone than ground reaction forces (GRF). This study computed that tibial loading during gait would compress and bend the distal portion of the tibia backward throughout most of the stance leading to the greatest stresses in the posterior face of the tibia, which is the most common site of fracture. The combination of GRF and muscle (plantarflexors) force acted to compress the tibia during stance and reinforced each other to increase compressive forces on the distal tibia. However, the GRF and muscle forces contributing to shear forces act in opposite directions to reduce the net shear on, and bending of, the tibia. So, although larger muscle forces could potentially cause larger compressive forces, they may reduce the shear force, in turn, reducing stress to the posterior tibia (27). As noted above, MCSA is only a surrogate measure of muscle force, and future studies should include direct measures of muscle force to confirm these findings. Our data suggest that runners in the SFX group had smaller MCSA, which implies that a smaller amount of force would be generated during midstance. If confirmed in other studies, this suggests that stress fractures may be due to shear forces on the posterior tibia.
Limitations and strengths.
The cross-sectional design of this study was a limitation because it only allows the collection of data at one point in time. Although cross-sectional designs can reveal associations among variables, they cannot reveal causality. A longitudinal design would be necessary to determine causality among variables that potentially contribute to stress fractures. As noted, we used muscle size as a surrogate measure of force. Although MCSA is correlated with muscle force, future studies should include direct measurement of force to confirm our findings. Finally, our study was focused on exploring differences in bone strength but did not directly assess hormonal, nutritional, genetic, or other factors that may have influenced bone geometry. Future studies that explore the factors that contribute to differences in bone strength and geometry in those with a history of stress fracture are needed.
In conclusion, our data suggest that female runners with a history of stress fracture have significantly lower CoA, lower bone strength, and smaller MCSA in the middle third of the tibia. Lower bone strength is due to smaller CoA with no significant differences in vBMD. After controlling for MCSA, there are no longer differences in any measured bone parameter between groups, suggesting that tibial strength in this group of female runners is adequately adapted to muscle size. This study suggests that suboptimal bone geometry and smaller absolute MCSA may lead to decreased bone strength and, in turn, predispose an individual to stress fracture. Because the muscle-bone relationship remained intact in those with stress fracture history, our data suggest that interventions aimed at improving muscle size and strength may help prevent stress fractures, although longitudinal studies are needed to confirm these findings.
Disclosure of funding: This work was supported in part by a grant from the National Institutes of Health (NIAMS-K23 AR49040-01A1 (M.P.)).
The results of the present study do not constitute endorsement by ACSM.
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