
==== Front
Int J Sports Phys Ther
Int J Sports Phys Ther
2159
International Journal of Sports Physical Therapy
2159-2896
NASMI Website: International Journal of Sports Physical Therapy

35136691
31653
10.26603/001c.31653
Original Research
Analysis of Calcaneal Bone Mineral Density (cBMD) in Healthy College Students
Bennett Jason E. PT, PhD, SCS, ATC 1
Austin Tricia M. PT, PhD, ATC 2
Hayes Ann M. PT, DPT, MHS, OCS 2
Reinking Mark F. PT, PhD, SCS, ATC, FAPTA 3
1 Department of Physical Therapy Carroll University (WI)
2 Department of Physical Therapy and Athletic Training Saint Louis University https://ror.org/04k7nem08
3 School of Physical Therapy Regis University https://ror.org/043ae9h44
Corresponding Author: Jason E. Bennett, PT, PhD, SCS, ATC Department of Physical Therapy Carroll University, Waukesha, WI, 53186, USA (262) 951-3034 jbennett@carrollu.edu
2 2 2022
2022
17 2 218227
9 2 2021
9 12 2021
© The Author(s)
https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (4.0) which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Background

There is limited evidence describing the relationship between calcaneal bone mineral density (cBMD) and activity level, menstrual history, or the development of bone stress injury (BSI).

Hypothesis/Purpose

The purposes of this study were to: 1) examine the influence of physical activity on cBMD in healthy college students (HCS), 2) determine if there is an association between cBMD, body mass index (BMI), sex, menstrual history, and history of BSI in HCS, and 3) compare the cBMD of HCS to cBMD data collected on intercollegiate athletes (ICA) from a previous study.

Study Design

Cross-sectional design

Methods

This cross-sectional study recruited a convenience sample of HCS at one institution. Subjects provided self-reported injury and menstrual history, completed a physical activity questionnaire, and cBMD and BMI measures were obtained. Descriptive statistics, statistical analyses of relationships (Chi-square and relative risk), logistic regression, and differences (t-tests) were used in the statistical analyses.

Results

One hundred three HCS (82 female, 21 male; age 21.9 ± 1.13) consented to participate. The composite score for work, leisure, and sport activity ranged from 5.6 to 11.1 (7.9 ± 1.1) for HCS subjects. There was no significant correlation between cBMD and physical activity in HCS, however, a significant correlation was found between reported age of onset of menstruation and left and right cBMD (r = -0.22 and r = -0.23; p < 0.05) and history of secondary amenorrhea and history of BSI (r = 0.32; p < 0.05). There was no difference in cBMD between the male ICA and male HCS, but highly significant differences in cBMD between the female ICA and female HCS groups (p < 0.000).

Conclusions

Age of menarche and secondary amenorrhea are significantly associated with cBMD and history of BSI in HCS subjects, respectively. Differences in cBMD among the HCS subjects were not related to activity level. cBMD was significantly lower in female HCS as compared to female ICA. This difference in cBMD between ICA and HCS may be activity related.

Level of Evidence

Level 3

amenorrhea
menarche
physical activity
bone stress injury
bone density
==== Body
pmcINTRODUCTION

Bone health is a significant global health issue facing our 21st century world. In 2000, there was estimated to be nine million osteoporotic fractures across the world, with hip, forearm, and vertebral fractures among the most common.1 Such fractures lead to decreased functional ability, inability to fulfill social roles, loss of independence, and higher mortality.2 The personal, social, and economic burden of poor bone health requires attention to this issue and close examination of the factors leading to poor bone health with aging.

Multiple factors have an influence on bone health including genetics, nutrition, physical activity, sex, age, and ethnicity. Some of those factors are non-modifiable (age, sex, genetics) while others including nutrition and physical activity are modifiable. The majority of bone mass is achieved by late adolescence, and, as such, maximizing bone accrual during adolescence is crucial in the prevention of early bone demineralization.3 Given that premenopausal bone fractures have been shown to increase the risk for future fractures in a woman’s life,4,5 attention to bone health in young women is critical. Bone mineral density (BMD) is one important indicator of bone health, and several studies have demonstrated a positive relationship between increased physical activity and higher BMD.6–12 A common theme to these studies is the importance of ground based, moderate intensity exercise as a stimulus for higher BMD. Studies by Reinking et al13 and Risser et al14 of BMD in collegiate athletes have shown lower BMD in swimmers as compared to ground-based athletes.

Given this evidence, it would be anticipated that participation in weight bearing sports would result in increased BMD. However, some evidence has shown lower BMD in endurance athletes as compared to a group of active, non-athletic subjects.15–19 Bone stress injury, including stress fracture and medial tibial stress syndrome, are commonly experienced in running and jumping athletes.16–24 Consequently, the dose-response relationship between weight-bearing physical activity and BMD is not fully understood. To encourage optimal bone health in a young adult population and minimize risk of bone demineralization and fracture in older adults, a deeper understanding of this relationship is critical.

The calcaneus is the only site recognized by the International Society of Clinical Densitometry (ISCD) for the assessment of bone density using quantitative ultrasound (QUS) bone densitometry.25 Consisting of 75-95% trabecular bone, the calcaneus demonstrates greater degradation in response to age and disease compared to cortical bone due to its high rate of turnover, and structurally is well-suited for the horizontal transmission of sound energy due to its two relatively opposed lateral surfaces and minimal amount of soft tissue. The speed of sound (SOS) is determined by measuring the time it takes for sound energy to travel across the width of the calcaneus, and as such, is measured in units of meters per second (m/s). Broadband ultrasound attenuation (BUA) is the slope of the line formed by plotting sound intensity (dB) across a range of sound frequencies (MHz) and is reported in units of dB/MHz. BUA has been reported to provide a general indicator of bone quality, or architecture, rather than the quantity of mineral in bone.26

These measures collectively provide qualitative and quantitative information regarding the density, microarchitecture, and mechanical properties of the calcaneus. Faster SOS and greater BUA reflect more dense and homogenous bone structure, respectively, and when combined linearly provide a measure of relative bone “stiffness” referred to as the quantitative ultrasound index (QUI). The QUI value is rescaled to provide an estimate of BMD (g/cm2) allowing for determination of a t-score and comparison to previously established normative data. In vivo and in vitro QUS measures have been shown to be highly correlated (r = 0.82 - 0.85) with other measures of calcaneal bone quality such as dual-energy x-ray absorptiometry (DXA), and with measures of bone density obtained at other anatomical locations such as the femur and lumbar spine.27–32

At present, inconsistent evidence is available pertaining to BMD values in athletic and non-athletic collegiate-aged persons, and the influence of physical activity on those values. Based on the literature review and the authors’ previous work with cBMD in intercollegiate athletes, we established three purposes of this study: 1) compare cBMD of intercollegiate athlete (ICA) and healthy college students (HCS), 2) examine the influence of physical activity on cBMD in HCS, 3) investigate the effects of multiple variables on cBMD including body mass index (BMI), sex, menstrual history in females, and history of bone stress injury (BSI). Previously published data on ICAs were used to compare cBMD values obtained in HCS subjects.13

METHODS

Study Design

Following approval by the Saint Louis University Institutional Review Board, a cross-sectional sample of HCS was recruited to participate in this study. Subjects who elected to participate in the research study provided consent and were scheduled for data collection. Data collection consisted of subjects completing a health and activity questionnaire and members of the research team collecting calcaneal bone mineral density, height, and weight measures.

Subjects

Full-time college students (82 female, 21 male) at one academic institution between 18-24 years of age (21.9 ± 1.13) who were not currently or previously rostered as a member of an intercollegiate athletic team were recruited to participate. Students not meeting the inclusion criteria or who described an existing lower-extremity injury were excluded from the study.

Procedures

Health & Activity Questionnaire

Participants completed a web-based questionnaire including date of birth, sex, age, race/ethnicity, use of foot orthotics, lifetime history of diagnosed lower extremity or pelvic stress fracture or medial tibial stress syndrome (MTSS), and menstrual history. The Habitual Physical Activity Questionnaire was included in the web-based questionnaire as a measure of self-reported activity level.33 The Habitual Physical Activity Questionnaire assesses activity across work, sport, and leisure not involving sport, and has been found to be a valid measure of activity level. The questionnaire consists of 16 items scored on a five-point scale which are used to calculate composite and categorical measures of self-reported physical activity.

Height and Weight

Height (inches) and weight (pounds) were recorded using conventional methods employing a standard scale and tape measure. Height and weight measures were converted to the metric scale to allow for calculation of body mass index (kg/m2).

Calcaneal Densitometry

Quantitative ultrasound (QUS) involves the measurement of speed of sound (SOS) and attenuation of sound energy, or broadband ultrasound attenuation (BUA), as the sound wave passes through soft tissue and bone. Based on SOS and BUA measures, the quantitative ultrasound index (QUI) is obtained through simple linear combination of both values and then rescaled to give an estimate of bone mineral density. For the current study, calcaneal bone mineral density (cBMD) was determined via QUS using the Sahara clinical bone sonometer (Hologic, Inc, Waltham, MA). The Sahara clinical bone sonometer uses a specific technique involving the transmission of sound energy from one transducer through the calcaneus to a second receiver.31,34,35

Calibration of the densitometer was performed as described by manufacturer guidelines each day prior to data collection. Participants were seated in a straight-back chair approximately 12-18 inches from the scanner and both heels were inspected for abrasions or open sores. The tester cleaned the sides of the heels with a towelette and dried the heel prior to testing. The tester then applied an oil-based coupling gel (Hologic, Inc.) to both elastomer transducer pads. The subject’s foot was then placed into the foot well and the leg secured using the positioning aid (Figure 1). The subject was instructed to remain still during the test and heel placement was checked to ensure proper placement prior to initiating the measurement. Once initiated, the elastomer pads moved to the measurement position contacting the sides of the calcaneus and measurement was performed. Upon completion of the measurement, SOS (m/s), BUA (dB/MHz), estimated cBMD (g/cm2), and BMD t-scores were recorded, and the steps repeated for the subject’s contralateral calcaneus.

79435 Figure 1. Measurement of Calcaneal Bone Mineral Density (cBMD)

Data Analysis

Descriptive statistics (means, percentages) for height, weight, and BMI were calculated using the demographic data of HCS subjects. The independent group t-test was used to compare self-reported physical activity scores to QUS measures in the group of HCS subjects. Self-reported physical activity, BMI, sex, and menstrual function were compared between HCS subjects with a history of BSI to the HCS subjects who denied a history of BSI using analyses of relationships (chi-square and relative risk). Comparison was made between QUS data collected on the group of 84 ICAs13 (64 female, 20 male) to the QUS data from the 103 HCS in this study using the independent group t-test. R statistical computing environment (R Core Team, 2013) was used for data management and analysis.

Reliability

Reliability of the calcaneal bone densitometer (cBMD, SOS) was determined through random selection of subjects to have repeated density measures of both calcanei at the time of initial data collection. Intrarater reliability, calculated using intraclass correlation coefficients (ICC 3.1) for cBMD, were previously reported as demonstrating a high level of measurement consistency (> 0.95).13

RESULTS

Participant demographics for the HCS subjects are summarized in Table 1 and self-reported history of stress fracture or leg pain (defined as pain occurring on the inside of the lower leg between the knee and ankle) is reported in Table 2.

79436 Table 1. Healthy College Student Demographics

	Healthy College Students (n=103)*	
	Female (n=82)	Male (n=21)	
Height (m)	1.64 (0.06)	1.78 (0.07)	
Weight (kg)	63.26 (8.65)a	85.57 (15.95)a	
BMI (kg/m2)	23.46 (2.95)b	26.93 (3.92)b	
BMI = body mass index

*Values are mean ± SD

a,bSignificantly different at p < 0.001

79437 Table 2. Healthy College Student Bone Stress Injury History

	Healthy College Students (%)	
	Total (n=103)	Female (n=82)	
Stress Fracture Hx	8 (7.8)	8 (9.8)	
Leg Pain Hx	29 (28.2)	25 (30.5)	
Hx = history

Twenty HCS (19.4%) reported participating in organized sports and 48 HCS (46.6%) reported “more” or “much more” physical activity compared to their peers on the Habitual Physical Activity Questionnaire. Habitual Physical Activity Scores were not associated with self-reported history of BSI (stress fracture or MTSS) or with cBMD or SOS measures. However, a small but significant negative association between BMI and the Habitual Physical Activity work subscale was identified across all HCS subjects (r = -0.29, p < 0.05) and in the female HCS group (r = -0.23, p < 0.05). Small but significant negative associations were also found in the female HCS group between age of menarche and cBMD in both the left (r = -0.22, p < 0.05) and right (r = -0.23, p < 0.05) calcanei, and between a history of stress fracture in the pelvis or lower extremity and a history of secondary amenorrhea (r = 0.32, p < 0.05, Table 3).

Calcaneal QUS measures (cBMD, SOS) for all HCS subjects were significantly lower (p < 0.000) than preseason measures obtained in ICAs (Table 4). Calcaneal BMD and SOS measures were significantly lower in HCS females compared to ICA females; however, male ICA and HCS had cBMD and SOS measures that were not significantly different (Table 4). From the cBMD reliability study the intraclass correlation coefficient values (ICC 3,1) were all greater than 0.95, indicating a high level of measurement consistency.

DISCUSSION

Physical Activity and cBMD in HCS

Although numerous studies have reported the benefits of exercise and sport on bone accrual and bone strength, few studies have examined the relationship between physical activity level and optimal bone health.36–38 While athletes have been shown to have greater BMD and bone health when compared to a referent group of non-athletes, the level of physical activity necessary to stimulate an osteogenic response has not been identified. Researchers have provided conflicting evidence to support the benefits of physical activity on bone health in the general population.6,36,38–40 Thus, the second purpose of the study was to examine the relationship between self-reported physical activity and cBMD in a group of HCS. The results did not identify a significant relationship between self-reported physical activity as measured by the Habitual Physical Activity Questionnaire and cBMD or SOS in this group of HCS. Comparing the results to previous studies is difficult due to differences in the methods used to assess physical activity level. It is also important to note the limitations of available methods used to measure physical activity. For example, the Habitual Physical Activity Questionnaire addresses frequency of exercise but may not account for osteogenic differences between various exercise modes. Therefore, subjects reporting higher levels of physical activity who are performing activities that are generally considered low-load, endurance activities are less likely to demonstrate significant differences in bone development and structure when compared to less physically active subjects. Wallace et al38 assessed both historical and current physical activity level in their study and reported that lifetime physical activity and lifetime weight-bearing activity accounted for 3-15% of the variance in BMD in a group of 19-25 year old regularly menstruating females. Sawyer et al39 used calcaneal QUS in a group of healthy subjects aged 6.6-20 years of age (n=311) and found a significant relationship between BUA and SOS and physical activity. However, when accounting for age and weight, physical activity accounted for only 1.0-1.4% of the variance in SOS and bone stiffness. In a study of 60 healthy, eumenorrheic women aged 25-34 years of age, physical activity was found to be significantly associated with vertebral bone density (r = 0.41, p < 0.005).36 A study of adolescent females with a history of an eating disorder were compared to matched females with no history of eating disorder who were also grouped based on performing more or less than seven hours of physical activity per week. No differences in total body or site-specific BMD were found between the eating disorder group or two activity groups.40

Association between Bone Stress Injury and cBMD, BMI, Sex, and Menstrual Function

Bone stress injuries have been identified as a common injury among endurance athletes. The long-term consequences of maladaptive changes in bone microarchitecture and bone geometry to repetitive loading have not been studied. Methods to assess bone health during periods of development, changes in activity, and with ageing will allow medical professionals to identify risk factors for bone stress injury and evaluate interventions designed to influence bone health. Quantitative ultrasound has also been shown to have similar prediction capability for fracture risk as compared to DXA and has been shown to correlate with DXA measures in young children and adolescents.31,34,35 Van Mechelen41 has described a “sequence” for the prevention of sports injury which includes identifying factors which play a role in the occurrence of sports injury followed by the introduction of measures to address the aforementioned factors.

A number of authors have shown significantly altered bone microarchitecture and lower bone density and bone strength in athletes with stress fracture or bone stress injury when compared to healthy athletes.21,42–44 The authors of this study have shown that QUS measures in female athletes involved in ground based sports who develop a bone stress injury during the competitive season are significantly lower relative to their peers.13 It is worth noting that studies that did not find a significant difference in BMD between subjects with bone stress injury and controls reported important methodological differences. For example, Bennell et al45 reported no significant difference in BMD when comparing female runners with a history of healed tibial stress fracture to female runners without a history of stress fracture, suggesting that timing of the densitometry measurement relative to the diagnosis of bone stress injury may influence BMD measures. In a study comparing military recruits who developed a bone stress injury to healthy, matched controls, there were no differences in BMD measures at the tibia and femoral neck.46 However, military recruits present with diverse levels of physical activity history, meaning the change in volume of physical activity likely varied across subjects with basic training and therefore exposed the subjects to varied levels of risk.

A number of authors have examined the influence of menstruation, BMI, and sex on risk of developing bone stress injury in athletes and the military population. When comparing cBMD between groups and blocking for sex, ICA male and HCS male subjects were found to have similar cBMD and SOS while female subjects had significantly different cBMD and SOS measures across ICA and HCS groups. This finding suggests the influence of sex linked factors in bone accrual and structure and supports previous studies demonstrating differences between male and female bone geometry and strength.35,47 For example, Beck et al47 found significantly smaller subperiosteal diameters and thinner cortices in female military recruits compared to male recruits. Several authors reporting on the incidence of stress fracture in military and athletic populations have identified female sex as a risk factor for bone stress injury.47–49

The influence of menstruation on bone health and in the development of bone stress injury has been described extensively as part of the female athlete triad, and the results of this study support the relationship between menstrual abnormality and low bone density.50–55 More specifically, amenorrhea has been shown to be a significant risk factor for bone stress injury in female athletes. The current study demonstrated a small but significant negative correlation (r = -0.22 and r = -0.23) between age of menarche and cBMD, suggesting an important relationship between earlier onset of menstruation and greater bone accrual during adolescence. A history of amenorrhea was also found to be associated with a history of stress fracture in the pelvis or lower extremity, supporting previous studies that have shown a relationship between menstruation and risk of bone stress injury. While differences in BMI across sports are common, the authors did not identify a relationship between BMI and cBMD in either the ICA or HCS groups.

cBMD in ICA vs HCS

This is the first known study to compare measures of bone health (SOS & BUA) in ICA and HCS using calcaneal QUS bone densitometry. The authors found significant differences in QUS measures for cBMD (p < 0.000) and SOS (p < 0.000) between the female ICA and female HCS groups, with female ICA having significantly greater cBMD. Previous studies have described the anabolic effects of physical activity on bone structure, especially in athletes involved in high-impact sports and weight training.7,11,12 Tenforde et al12 in their review of the literature found an association between impact sports (gymnastics, soccer, etc.) and greater bone mineral density, bone composition and bone geometry, while non-impact sports such as cycling and water polo were not associated with increased bone quality or quantity, and in the case of swimming were negatively associated. The authors of this manuscript reported similar findings in a sample of ICA, with significantly lower cBMD and SOS in swimmers & divers when compared to soccer and cross-country/track athletes.13 Considering ICA are typically engaged in high load activities associated with their sport and participate in regular strengthening and conditioning programs, it is not surprising that we found significantly higher measures of bone quality and quantity when compared to HCS subjects. However, when the QUS measures in ICA who developed BSI during their competitive season were compared to the QUS measures in HCS, there was no significant difference in cBMD or SOS between groups. This study consisted of a sample of convenience of healthy college students at one Midwest institution with a greater number of female than male subjects and therefore generalizability is limited. History of BSI relied on self-reporting and therefore is dependent on subject recall and susceptible to bias.

79438 Table 3. Association Between Variables in Female Healthy College Students

	RcBMD	RSOS	LcBMD	LSOS	BMI	FXDX	MENA	AMEN2 HX	OLIGO HX	AMEN2 YR	OLIGO YR	
RcBMD	1.00											
RSOS	.96a	1.00										
LcBMD	.88b	.89b	1.00									
LSOS	.89c	.93c	.97c	1.00								
BMI	-.04	-.09	-.05	-.13	1.00							
FXDX	-.03	-.05	-.11	-.12	.27d	1.00						
MENA	-.23e	-.18	-.22e	-.17	-.19	.08	1.00					
AMEN2 HX	-.07	-.07	-.02	-.07	.12	.32f	.18	1.00				
OLIGO HX	.01	.01	.00	.01	-.01	.10	.19	.32g	1.00			
AMEN2 YR	-.12	-.11	.02	-.03	-.04	-.09	-.03	.42h	.17	1.00		
OLIGO YR	.18	.18	.15	.15	-.02	-.10	-.13	.15	.54i	.08	1.00	
RcBMD = right calcaneal bone mineral density; RSOS = right speed of sound; LcBMD = left calcaneal bone mineral density; LSOS = left speed of sound; BMI = body mass index; FXDX= stress fracture diagnosis; MENA = age of menarche; AMEN2 HX = secondary amenorrhea history not including the last 12 months; OLIGO HX = oligomenorrhea history not including the last 12 months; AMEN2 YR = secondary amenorrhea in the last 12 months; OLIGO YR = oligomenorreha in the last 12 months

a,b,c,h,iAssociation between variables significant at p < 0.001

d,e,f,gAssociation between variables significant at p < 0.05

79439 Table 4. Speed of Sound and Calcaneal Bone Mineral Density Quantitative Ultrasound Measures Between Intercollegiate Athlete and Healthy College Students

	Quantitative Ultrasound Measures*	
	RSOS (m/s)	LSOS (m/s)	RcBMD (g/cm2)	LcBMD (g/cm2)	
ICA (n=84)	1605.2 ± 36.1a	1604.3 ± 33.4b	.710 ± .15c	.698 ± .14d	
HCS (n=103)	1582.0 ± 32.3a	1582.0 ± 34.1b	.615 ± .13c	.617 ± .14d	
Male ICA (n=20)	1597.1 ± 33.5	1595.9 ± 33.4	.687 ± .13	.681 ± .13	
Male HCS (n=21)	1601.7 ± 33.1	1597.0 ± 34.8	.693 ± .13	.688 ± .15	
Female ICA (n=64)	1607.8 ± 36.8e	1606.9 ± 34.2f	.717 ± .16g	.703 ± .14h	
Female HCS (n=82)	1577.0 ± 30.3e	1578.1 ± 33.0f	.596 ± .12g	.599 ± .13h	
RSOS = right speed of sound; LSOS = left speed of sound; RcBMD = right calcaneal bone mineral density; LcBMD = left calcaneal bone mineral density; ICA = intercollegiate athlete; HCS = healthy college students

*Values are mean ± SD

a-hp < 0.000

CONCLUSION

Methods to assess bone health are valuable to medical professionals involved in the prevention and treatment of bone stress injuries. A thorough understanding of the influence of physical activity, menstrual history, sex, BMI, BMD, and history of BSI on bone health will aide in the management of subjects at risk of or diagnosed with a bone stress injury. Age of menarche and history of amenorrhea were found to be significantly associated with cBMD and self-reported stress fracture history, respectively, and should be considered when assessing the risk of bone stress injury in females. Female HCS with no history of intercollegiate athletic participation were found to have significantly lower cBMD than a group of female ICA. The results of this study suggest that QUS is a valuable instrument for identifying subjects with low calcaneal bone mineral density who may be at risk of developing a BSI. As a non-ionizing, efficient, portable, and low-cost modality, QUS should be considered a viable instrument in monitoring the response of bone to repetitive stress, identifying athletes with low BMD at increased risk of bone stress injury, and prescribing optimal osteogenic interventions in the management of bone stress injury. Future studies should include a larger sample of collegiate and non-collegiate athletes and non-athletes and include additional risk factors that will further help identify level of risk of bone stress injury.

CONFLICTS OF INTEREST

The authors have no conflicts to disclose
==== Refs
Musculoskeletal health conditions represent a global threat to healthy aging: a report for the 2015 world health organization world report on ageing and health Gerontologist Briggs A. M. Cross M. J. Hoy D. G. Sanchez-Riera L. Blyth F. M. Woolf A. D. March L. 2016
56 Suppl 2 S243 S255 10.1093/geront/gnw002
Effects of exercise on bone status in female subjects, from young girls to postmenopausal women: an overview of systematic reviews and meta-analyses Sports Med Xu J. Lombardi G. Jiao W. Banfi G. 2016
46 8 1165 82 1179-2035 (Electronic) 0112-1642 (Linking) 10.1007/s40279-016-0494-0 26856338
An update on childhood bone health: mineral accrual, assessment and treatment Curr Opin Endocrinol Diabetes Obes Sopher A. B. Fennoy I. Oberfield S. E. 2015
22 1 35 40 1752-2978 (Electronic) 1752-296X (Linking) 10.1097/MED.0000000000000124 25517023
Fractures before menopause: a red flag for physicians Osteoporos Int Hosmer W. D. Genant H. K. Browner W. S. 2002
13 4 337 41 0937-941X (Print) 0937-941X (Linking) 10.1007/s001980200035 12030549
Fractures between the ages of 20 and 50 years increase women's risk of subsequent fractures Arch Intern Med Wu F. Mason B. Horne A. Ames R. Clearwater J. Liu M. Evans M. C. Gamble G. D. Reid I. R. 2002
162 1 33 6 0003-9926 (Print) 0003-9926 (Linking) 10.1001/archinte.162.1.33 11784217
Exercise and bone mineral density Sports Med Chilibeck P. D. Sale D. G. Webber C. E. 1995
19 2 103 22 0112-1642 (Print) 0112-1642 (Linking) 10.2165/00007256-199519020-00003 7747001
Bone mineral density of female athletes in different sports Bone Miner Heinonen A. Oja P. Kannus P. Sievanen H. Manttari A. Vuori I. 1993
23 1 1 14 0169-6009 (Print) 0169-6009 (Linking) 10.1016/s0169-6009(08)80086-4 8274875
Assessment of the bone quality of black male athletes using calcaneal ultrasound: a cross-sectional study Nutr Metab (Lond) Laabes E. P. Vanderjagt D. J. Obadofin M. O. Sendeht A. J. Glew R. H. 2008
5 13 1743-7075 (Electronic) 1743-7075 (Linking) 10.1186/1743-7075-5-13 18492264
Assessment of the bone quality of black female athletes using quantitative ultrasound J Sports Med Phys Fitness Laabes E. P. Vanderjagt D. J. Obadofin M. O. Sendeht A. J. Glew R. H. 2008
48 4 502 8 0022-4707 (Print) 0022-4707 (Linking) 18997655
Bone health in endurance athletes: runners, cyclists, and swimmers Curr Sports Med Rep Scofield K. L. Hecht S. 2012
11 6 328 34 1537-8918 (Electronic) 1537-890X (Linking) 10.1249/JSR.0b013e3182779193 23147022
Bone mineral density and long term exercise. An overview of cross-sectional athlete studies Sports Med Suominen H. 1993
16 5 316 30 0112-1642 (Print) 0112-1642 (Linking) 10.2165/00007256-199316050-00003 8272687
Influence of sports participation on bone health in the young athlete: a review of the literature PM R Tenforde A. S. Fredericson M. 2011
3 9 861 7 1934-1563 (Electronic) 1934-1482 (Linking) 10.1016/j.pmrj.2011.05.019 21944303
Lower extremity overuse bone injury risk factors in collegiate athletes: a pilot study Int J Sports Phys Ther Reinking M. F. Austin T. M. Bennett J. Hayes A. M. Mitchell W. A. 2015
10 2 155 67 2159-2896 (Print) 2159-2896 (Linking) 25883864
Bone density in eumenorrheic female college athletes Med Sci Sports Exerc Risser W. L. Lee E. J. LeBlanc A. Poindexter H. B. Risser J. M. Schneider V. 1990
22 5 570 4 0195-9131 (Print) 0195-9131 (Linking) 10.1249/00005768-199010000-00005 2233193
Musculoskeletal injuries in track and field: incidence, distribution and risk factors Aust J Sci Med Sport Bennell K. L. Crossley K. 1996
28 3 69 75 0813-6289 (Print) 0813-6289 (Linking) 8937661
Stress Fractures Phys Sportsmed Goldberg B. Pecora C. 1994
22 3 68 78 0091-3847 (Print) 0091-3847 (Linking) 10.1080/00913847.1994.11710482 27425235
Stress fractures in the female athlete Sports Med Arthrosc Rev Nelson B. J. Arciero R. A. 2002
10 83 90
Medial tibial stress syndrome in high school cross-country runners: incidence and risk factors J Orthop Sports Phys Ther Plisky M. S. Rauh M. J. Heiderscheit B. Underwood F. B. Tank R. T. 2007
37 2 40 7 0190-6011 (Print) 0190-6011 (Linking) 10.2519/jospt.2007.2343 17366958
High school cross country running injuries: a longitudinal study Clin J Sport Med Rauh M. J. Margherita A. J. Rice S. G. Koepsell T. D. Rivara F. P. 2000
10 2 110 6 1050-642X (Print) 1050-642X (Linking) 10.1097/00042752-200004000-00005 10798792
The incidence and distribution of stress fractures in competitive track and field athletes. A twelve-month prospective study Am J Sports Med Bennell K. L. Malcolm S. A. Thomas S. A. Wark J. D. Brukner P. D. 1996
24 2 211 7 0363-5465 (Print) 0363-5465 (Linking) 10.1177/036354659602400217 8775123
Risk factors for stress fractures in track and field athletes. A twelve-month prospective study Am J Sports Med Bennell K. L. Malcolm S. A. Thomas S. A. Reid S. J. Brukner P. D. Ebeling P. R. Wark J. D. 1996
24 6 810 8 0363-5465 (Print) 0363-5465 (Linking) 10.1177/036354659602400617 8947404
Stress fracture sites related to underlying bone health in athletic females Clin J Sport Med Marx R. G. Saint-Phard D. Callahan L. R. Chu J. Hannafin J. A. 2001
11 2 73 6 1050-642X (Print) 1050-642X (Linking) 10.1097/00042752-200104000-00002 11403117
Stress fractures and bone health in track and field athletes J Sci Med Sport Nattiv A. 2000
3 3 268 79 1440-2440 (Print) 1878-1861 (Linking) 10.1016/s1440-2440(00)80036-5 11101266
Bone health concerns in active and athletic women and girls Orthopedics Pepper M. Saint-Phard D. 2007
30 4 281 7; quiz 288 0147-7447 (Print) 0147-7447 (Linking) 10.3928/01477447-20070401-03 17424691
2019 ISCD Official Positions: Adult 2019
https://iscd.org/learn/official-positions/adult-positions/
Assessment of bone quantity and 'quality' by ultrasound attenuation and velocity in the heel Clin Biomech (Bristol, Avon) Grimm M. J. Williams J. L. 1997
12 5 281 285 1879-1271 (Electronic) 0268-0033 (Linking) 10.1016/s0268-0033(97)00014-4 11415735
Use of quantitative ultrasound for identifying low bone density in older people J Ultrasound Med Lee H. D. Hwang H. F. Lin M. R. 2010
29 7 1083 92 1550-9613 (Electronic) 0278-4297 (Linking) 10.7863/jum.2010.29.7.1083 20587432
Correlation between parameters of calcaneal quantitative ultrasound and hip structural analysis in osteoporotic fracture patients PLoS One Zhang L. Lv H. Zheng H. Li M. Yin P. Peng Y. Gao Y. Zhang L. Tang P. 2015
10 12 e0145879 1932-6203 (Electronic) 1932-6203 (Linking) 10.1371/journal.pone.0145879 26710123
A study on the validity of quantitative ultrasonic measurement used the bone mineral density values on dual-energy X-ray absorptiometry in young and in middle-aged or older women Radiol Phys Technol Iida T. Chikamura C. Aoi S. Ikeda H. Matsuda Y. Oguri Y. Ono Y. Katada K. Ishizaki F. 2010
3 2 113 9 1865-0341 (Electronic) 1865-0333 (Linking) 10.1007/s12194-010-0086-x 20821084
A comparison of fracture discrimination using calcaneal quantitative ultrasound and dual X-ray absorptiometry in women with a history of fracture at sites other than the spine and hip Calcif Tissue Int Frost M. L. Blake G. M. Fogelman I. 2002
71 3 207 11 0171-967X (Print) 0171-967X (Linking) 10.1007/s00223-001-2074-y 12154392
Quantitative ultrasound and bone mineral density are equally strongly associated with risk factors for osteoporosis J Bone Miner Res Frost M. L. Blake G. M. Fogelman I. 2001
16 2 406 16 0884-0431 (Print) 0884-0431 (Linking) 10.1359/jbmr.2001.16.2.406 11204441
Is calcaneal quantitative ultrasound a valid surrogate measure for hip dual-energy x-ray absorptiometry in young adults? J Ortho Sport Phys Ther Gutekunst D J Bennett J E 2018
48 1 A120
A short questionnaire for the measurement of habitual physical activity in epidemiological studies Am J Clin Nutr Baecke J. A. Burema J. Frijters J. E. 1982
36 5 936 42 0002-9165 (Print) 0002-9165 (Linking) 10.1093/ajcn/36.5.936 7137077
An update on the assessment of osteoporosis using radiologic techniques Eur Radiol Damilakis J. Maris T. G. Karantanas A. H. 2007
17 6 1591 602 0938-7994 (Print) 0938-7994 (Linking) 10.1007/s00330-006-0511-z 17131124
Evaluation of bone mineral density by quantitative ultrasound of bone in 16,862 subjects during routine health examination Br J Radiol Lin J. D. Chen J. F. Chang H. Y. Ho C. 2001
74 883 602 6 0007-1285 (Print) 0007-1285 (Linking) 10.1259/bjr.74.883.740602 11509395
Interaction of calcium nutrition and physical activity on bone mass in young women J Bone Miner Res Kanders B. Dempster D. W. Lindsay R. 1988
3 2 145 9 0884-0431 (Print) 0884-0431 (Linking) 10.1002/jbmr.5650030204 3213609
Using bone's adaptation ability to lower the incidence of stress fractures Am J Sports Med Milgrom C. Simkin A. Eldad A. Nyska M. Finestone A. 2000
28 2 245 51 0363-5465 (Print) 0363-5465 (Linking) 10.1177/03635465000280021701 10751003
Lifetime physical activity and calcium intake related to bone density in young women J Womens Health Gend Based Med Wallace L. S. Ballard J. E. 2002
11 4 389 98 1524-6094 (Print) 1524-6094 (Linking) 10.1089/152460902317586029 12150501
Calcaneus ultrasound measurements in a convenience sample of healthy youth J Clin Densitom Sawyer A. Moore S. Fielding K. T. Nix D. A. Kiratli J. Bachrach L. K. 2001
4 2 111 20 1094-6950 (Print) 1094-6950 (Linking) 10.1385/jcd:4:2:111 11477304
Bone mineral status in adolescent girls: effects of eating disorders and exercise J Adolesc Health Carruth B. R. Skinner J. D. 2000
26 5 322 9 1054-139X (Print) 1054-139X (Linking) 10.1016/s1054-139x(99)00089-0 10775824
Incidence, severity, aetiology and prevention of sports injuries. A review of concepts Sports Med van Mechelen W. Hlobil H. Kemper H. C. 1992
14 2 82 99 0112-1642 (Print) 0112-1642 (Linking) 10.2165/00007256-199214020-00002 1509229
Bone quality and muscle strength in female athletes with lower limb stress fractures Med Sci Sports Exerc Schnackenburg K. E. Macdonald H. M. Ferber R. Wiley J. P. Boyd S. K. 2011
43 11 2110 9 1530-0315 (Electronic) 0195-9131 (Linking) 10.1249/MSS.0b013e31821f8634 21552163
Fractal analysis of bone texture: a screening tool for stress fracture risk? Eur J Clin Invest Prouteau S. Ducher G. Nanyan P. Lemineur G. Benhamou L. Courteix D. 2004
34 2 137 42 0014-2972 (Print) 0014-2972 (Linking) 10.1111/j.1365-2362.2004.01300.x 14764077
Low bone density is an etiologic factor for stress fractures in athletes Ann Intern Med Myburgh K. H. Hutchins J. Fataar A. B. Hough S. F. Noakes T. D. 1990
113 10 754 9 0003-4819 (Print) 0003-4819 (Linking) 10.7326/0003-4819-113-10-754 1978620
Ground reaction forces and bone parameters in females with tibial stress fracture Med Sci Sports Exerc Bennell K. Crossley K. Jayarajan J. Walton E. Warden S. Kiss Z. S. Wrigley T. 2004
36 3 397 404 0195-9131 (Print) 0195-9131 (Linking) 10.1249/01.mss.0000117116.90297.e1 15076780
Stress fracture injury in young military men and women Bone Armstrong D. W., III Rue J. P. Wilckens J. H. Frassica F. J. 2004
35 3 806 16 10.1016/j.bone.2004.05.014 15336620
Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors Bone Beck T. J. Ruff C. B. Shaffer R. A. Betsinger K. Trone D. W. Brodine S. K. 2000
27 3 437 44 8756-3282 (Print) 1873-2763 (Linking) 10.1016/s8756-3282(00)00342-2 10962357
Epidemiology and site specificity of stress fractures Clin Sports Med Bennell K. L. Brukner P. D. 1997
16 2 179 96 0278-5919 (Print) 0278-5919 (Linking) 10.1016/s0278-5919(05)70016-8 9238304
Stress fractures and the female athlete Clin Orthop Relat Res Arendt E. A. 2000
372 372 131 8 0009-921X (Print) 0009-921X (Linking) 10.1097/00003086-200003000-00015
Low energy availability, menstrual dysfunction, and impaired bone health: A survey of elite para athletes Scand J Med Sci Sports Brook E. M. Tenforde A. S. Broad E. M. Matzkin E. G. Yang H. Y. Collins J. E. Blauwet C. A. 2019
29 5 678 685 1600-0838 (Electronic) 0905-7188 (Linking) 10.1111/sms.13385 30644600
Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women Am J Sports Med Barrack M. T. Gibbs J. C. De Souza M. J. Williams N. I. Nichols J. F. Rauh M. J. Nattiv A. 2014
42 4 949 58 1552-3365 (Electronic) 0363-5465 (Linking) 10.1177/0363546513520295 24567250
Sport and triad risk factors influence bone mineral density in collegiate athletes Med Sci Sports Exerc Tenforde A. S. Carlson J. L. Sainani K. L. Chang A. O. Kim J. H. Golden N. H. Fredericson M. 2018
50 12 2536 2543 1530-0315 (Electronic) 0195-9131 (Linking) 10.1249/MSS.0000000000001711 29975299
Bone mineral density and menstrual irregularities. A comparative study on cortical and trabecular bone structures in runners with alleged normal eating behavior Int J Sports Med Tomten S. E. Falch J. A. Birkeland K. I. Hemmersbach P. Hostmark A. T. 1998
19 2 92 7 0172-4622 (Print) 0172-4622 (Linking) 10.1055/s-2007-971888 9562216
The female athlete triad: an emerging role for physical therapy J Orthop Sports Phys Ther Papanek P. E. 2003
33 10 594 614 0190-6011 (Print) 0190-6011 (Linking) 10.2519/jospt.2003.33.10.594 14620789
Female athlete triad and stress fractures Orthop Clin North Am Feingold D. Hame S. L. 2006
37 4 575 83 0030-5898 (Print) 0030-5898 (Linking) 10.1016/j.ocl.2006.09.005 17141015
