RESEARCH ARTICLE

Relationship between Bone-Specific Physical

Activity Scores and Measures for Body
Composition and Bone Mineral Density in
Healthy Young College Women
SoJung Kim1, Wi-Young So2, Jooyoung Kim3, Dong Jun Sung4*
1 Department of Physical Therapy, College of Health Sciences, University of Massachusetts, Lowell,
Massachusetts, 01854, United States of America, 2 Sports and Health Care Major, College of Humanities
and Arts, Korea National University of Transportation, Chungju-si, 27469, Korea, 3 Health and Rehabilitation
Major, Kookmin University, Seoul, 02707, Korea, 4 Division of Sport Science, College of Science and
Technology, Konkuk University, Chungju-si, 27478, Korea

a11111 * sls98@kku.ac.kr

Abstract

Objective
OPEN ACCESS
The purpose of this cross-sectional study was to investigate the relationship between bone-
Citation: Kim S, So W-Y, Kim J, Sung DJ (2016) specific physical activity (BPAQ) scores, body composition, and bone mineral density
Relationship between Bone-Specific Physical Activity
Scores and Measures for Body Composition and
(BMD) in healthy young college women.
Bone Mineral Density in Healthy Young College
Women. PLoS ONE 11(9): e0162127. doi:10.1371/ Methods
journal.pone.0162127
Seventy-three college women (21.7 ± 1.8 years; 162.1 ± 4.6 cm; 53.9 ± 5.8 kg) between the
Editor: Karen Hind, Leeds Beckett University, ages of 19 and 26 years were recruited from the universities in Seoul and Gyeonggi prov-
UNITED KINGDOM
ince, South Korea. We used dual energy X-ray absorptiometry to measure the lumbar spine
Received: May 18, 2016 (L2-L4) and proximal femur BMD (left side; total hip, femoral neck). The BPAQ scores (past,
Accepted: August 17, 2016 pBPAQ; current, cBPAQ; total, tBPAQ) were used to obtain a comprehensive account of
Published: September 2, 2016 lifetime physical activity related to bone health. We used X-scan plus II instrumentation to
measure height (cm), weight (kg), fat free mass (FFM, kg), percent body fat (%), and body
Copyright: © 2016 Kim et al. This is an open access
article distributed under the terms of the Creative mass index (BMI). Participants were asked to record their 24-hour food intake in a
Commons Attribution License, which permits questionnaire.
unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are
Results
credited.
There were positive correlations between BPAQ scores and total hip (pBPAQ r = 0.308, p =
Data Availability Statement: All relevant data are
within the paper and its Supporting Information files. 0.008; tBPAQ, r = 0.286, p = 0.014) and FN BMD (pBPAQ r = 0.309, p = 0.008; tBPAQ, r =
0.311, p = 0.007), while no significant relationships were found in cBPAQ (p > 0.05). When
Funding: This work was supported by the National
Research Foundation of Korea Grant funded by the FFM, Vitamin D intake, cBPAQ, pBPAQ, and tBPAQ were included in a stepwise multiple
Korean Government (NRF-2013S1A5B5A07046267). linear regression analysis, FFM and pBPAQ were predictors of total hip, accounting for 16%
Competing Interests: The authors have declared (p = 0.024), while FFM and tBPAQ predicted 14% of the variance in FN (p = 0.015). Only
that no competing interests exist. FFM predicted 15% of the variance in L2-L4 (p = 0.004). There was a positive correlation

PLOS ONE | DOI:10.1371/journal.pone.0162127 September 2, 2016 1 / 10

 Bone-Specific Physical Activity Score and Bone Mineral Density

between Vitamin D intake and L2-L4 (p = 0.025), but other dietary intakes variables were
not significant (p > 0.05).

Conclusions
BPAQ-derived physical activity scores and FFM were positively associated with total hip
and FN BMD in healthy young college women. Our study suggests that osteoporosis aware-
ness and effective bone healthy behaviors for college women are required to prevent seri-
ous bone diseases later in life.

Introduction
Osteoporosis is the most common type of bone disease characterized by low bone mineral den-
sity (BMD), high bone turnover, and microarchitecture deterioration [1]. It is well known that
peak bone mass is reached by the end of the third decade [2] and increasing BMD levels is cru-
cial for preventing osteoporosis during the early adulthood. High-impact exercises, including
jumping, dynamic movements, and resistance training are recommended to increase BMD in
premenopausal women [3, 4]. In addition, maintaining optimal muscle mass is an important
factor determining bone health in young adults [5, 6]. Other factors influencing BMD in col-
lege women have been unhealthy weight control behaviors [7, 8], low body mass index [9, 10]
and low Vitamin D intake [10], low calcium intake [11], and lifestyle effects [11–13]. Due to
the lack of awareness or education for serious bone diseases such as osteoporosis among female
college students [14, 15], the last opportunity to build strong bones for life may not be impor-
tantly recognized by this population. As it turns out, mechanical loading of the skeleton during
high impact weight-bearing activities (e.g., running, jumping) has been shown to improve
bone mass in humans [16, 17].
A variety of physical activity assessment tools (e.g., questionnaires, pedometers, and acceler-
ometers) have been used to predict bone strength in diverse population groups [18–22].
Among these methods, the bone-specific physical activity questionnaire (BPAQ) is a relatively
simple method to account for the relationship between physical activity associated with bone
loading and BMD as measured by dual energy X-ray absorptiometry (DXA) and calcaneal
broadband ultrasound attenuation (BUA) [18]. The BPAQ algorithms are becoming more
widely used in children [20, 23, 24], adolescents [25, 26], young adults [18, 24], and clinical
populations [27, 28] to determine their relation to areal BMD (aBMD), geometry, and bone
architecture. The results of previous studies have shown BPAQ able to predict femoral neck
(FN), lumbar spine, and whole body aBMD (g/cm2) in young men (24.5±2.9 years) [18] and in
healthy middle-aged and older men (60.6±6.0 years) [28], while the past BPAQ score predicted
an index of bone strength at the heel for healthy young women (25.1±2.8years) [18]. However,
a study by Farr et al. [20] found that BPAQ score was not significantly associated with bone
strength index (BSI) and strength strain index (SSI) at femur and tibia sites as measured by
peripheral quantitative computed tomography (pQCT) in girls (10.7±1.1 years) compared with
past physical activity questionnaire (PYPAQ). The BPAQ algorithms has been validated in a
small number of young adults (20 men and 20 women) [18] and BPAQ’s relation to BMD in
healthy college women has not been reported.
The purpose of this cross-sectional study was to investigate the relationship between
BPAQ-derived physical activity, body composition, and BMD in Korean college women. We

PLOS ONE | DOI:10.1371/journal.pone.0162127 September 2, 2016 2 / 10

 Bone-Specific Physical Activity Score and Bone Mineral Density

hypothesized that the BPAQ scores would have positive associations with total hip, FN, and
L2-L4 aBMD in healthy young college women.

Materials and Methods

Participants
Seventy-three college women between the ages of 19 and 26 years were recruited from the uni-
versities in Seoul and Gyeonggi province, South Korea. Healthy individuals who had regular
menstrual cycles participated in the study. The participants were excluded if they were smok-
ers, pregnant, on hormonal birth control, taking antihypertensive drugs or any medication that
could affect BMD. All participants visited the Seoul Sok Medical Center to complete an
informed consent form, the health and menstrual history questionnaires along with bone scans
and body composition assessments.
This study was approved by Korean Ministry of Health and Welfare Research Ethics Com-
mittee and written informed consent was obtained from each participant.

Body composition
We used X-scan plus II (Hospital body Composition Analyzer, Jawon Medical, Gyeongsan,
Korea) to measure height (cm), weight (kg), fat free mass (FFM) (kg), % body fat (%), and
body mass index (BMI). To avoid measurement errors, the participants were asked not to
drink alcohol for 48 hours before the testing or participate in any vigorous exercise 12 hours
prior to the testing. They were also asked not to have any meals including beverages 4 hours
before the testing. All participants changed into the scrubs that were provided by the Seoul Sok
Medical Center. The participants stood on the measure scale barefoot and held the measure-
ment bars with both hands and open arms.

Bone Mineral Density

We used dual energy X-ray absorptiometry (DXA, GE Lunar Prodigy) to measure L2-L4 and
the left side of proximal femur BMD (total hip, femoral neck; FN). The DXA was calibrated
daily following the Quality Assurance and qualified technicians conducted all procedures dur-
ing the study period. The participants removed all metal, plastic objects or other high density
objects associated with the participant’s clothes. The participants were asked to lie down on the
DXA table in the supine position. The standard scan mode was determined by the level of par-
ticipant’s umbilicus (Thick, >25 cm; Standard, 13–25 cm; and Thin, <13 cm). For lumbar
spine measurement, an appropriate positioning block was chosen and placed under the partici-
pant’s legs. For the proximal femur of non-dominant side leg, the participant’ feet were secured
by the DualFemurTM positioner to maintain the appropriate internal rotation of trochanter or
1 cm inferior to the pubic symphysis in the midline of the thigh. Two qualified technicians per-
formed all scans and analyses using encore 2002 Software (GE Lunar Prodigy).

24 hours recall
Participants were asked to complete a questionnaire, recalling food intake for the past 24
hours, and this included listing food/drink items with brand names, the amount ingested, and
method of preparation with as much specificity as possible. We also obtained information
regarding the supplements taken by the participants. A qualified dietitian analyzed total caloric
intake (kcal), protein (g), carbohydrate (g), fat (g), Vitamin D (mcg), calcium (mg), and mag-
nesium (mg) using the Computer Aided Nutritional analysis program (CAN-Pro 4.0, The
Korean Nutrition Society).

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 Bone-Specific Physical Activity Score and Bone Mineral Density

Bone-specific Physical Activity Questionnaire

The BPAQ assessment instrument was designed to estimate levels of physical activities that
impose mechanical loads on the skeleton [18]. The BPAQ consisted of three independent sec-
tions: the past period (pBPAQ, from one year of age to the current age), the current period
(cBPAQ, previous 12 months), and the total period (tBPAQ, average of pBPAQ and cBPAQ)
[28]. Participants were asked to complete the BPAQ questionnaire and a qualified researcher
analyzed all values using an online BPAQ calculator (www.fithdysign.com/BPAQ/). Algo-
rithms used to analyze BPAQ responses have been described in detail [18].

Statistical analyses
We performed all analyses using SPSS for Windows version 22 (SPSS Inc., Chicago, IL, USA)
and data are reported at mean ± SD. Pearson’s correlation tests were used to examine the asso-
ciation between the BPAQ scores (pBPAQ, cBPAQ, and tBPAQ), body composition, dietary
intake and BMD. We performed stepwise multiple regression analyses to determine the vari-
ables that predict variance in BMD. The predictor variables included FFM, Vitamin D intake,
BPAQ scores, and BMD (total hip, FN, L2-L4). We set the level of significance at p < 0.05.

Results
We provide physical characteristics, body composition variables, BPAQ scores, dietary intake
estimates and BMD for study participants in Table 1.

Table 1. Descriptive Data for the Study Population (N = 73).

Variables Mean ± SD Range
Age (years) 21.7 ± 1.8 19.0–25.8
Height (cm) 162.1 ± 4.6 151.7–172.4
Weight (kg) 53.9 ± 5.8 41.8–68.6
Menarche age (years) 12.4 ± 1.4 9.0–16.0
BMI (kg/m2) 21 ± 2 16–26
FFM (kg) 40.0 ± 2.9 33.9–47.4
% body fat (%) 25.4 ± 4.11 15.2–35.6
BPAQ
Current 3.8 ± 7.1 0.3–42.7
Past 40.5 ± 10.8 11.2–83.6
Total 22.2 ± 6.7 6.0–49.3
Dietary Intake
Total caloric intake (kcal) 1578.3 ± 478.1 736.7–2885.9
Protein (g) 63.0 ± 29.8 16.5–192.1
Carbohydrate (g) 211.3 ± 66.1 78.4–380.3
Fat (g) 54.5 ± 23.8 15.0–130.5
Vitamin D (mcg) 3.7 ± 3.9 0.0–18.4
Calcium (mg) 432.3 ± 236.7 72.3–1070.3
Magnesium (mg) 77.6 ± 54.0 0.0–238.7
BMD (g/cm2)
Total hip 0.979 ± 0.109 0.727–1.257
FN 0.969 ± 0.113 0.731–1.287
L2-L4 1.167 ± 0.118 0.924–1.262

BMI: body mass index, FFM: fat free mass, BPAQ: bone-specific physical activity score, BMD: bone mineral density, FN: femoral neck

doi:10.1371/journal.pone.0162127.t001

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 Bone-Specific Physical Activity Score and Bone Mineral Density

Table 2. Classification of the Participants by Bone Status (N = 73).

T-score Total hip FN L2-L4
n(%) n(%) n(%)
Normal (T-score  -1.0) 63(86) 55(75.3) 53(72.6)
Osteopenia (–2.5 < T-score < -1.0) 10(14) 18(24.7) 20(27.4)
Osteoporosis (T-score  -2.5) 0(0) 0(0) 0(0)

FN: femoral neck

doi:10.1371/journal.pone.0162127.t002

We found that none of the participants had less than or equal to a -2.5 T-score (classified as
osteoporosis) for total hip, FN, and L2-L4 (Table 2).
There were positive correlations between BPAQ scores and total hip (pBPAQ r = 0.308,
p = 0.008; tBPAQ, r = 0.286, p = 0.014) and FN BMD (pBPAQ r = 0.309, p = 0.008; tBPAQ,
r = 0.311, p = 0.007) while no significant relationship was found in cBPAQ (total hip, r = 0.076,
p = 0.520; FN, r = 0.122, p = 0.303) (Fig 1). No significant relationships were found between
cBPAQ (r = 0.045, p = 0.707), pBPAQ (r = 0.174, p = 0.141), tBPAQ (r = 0.116, p = 0.330) and
L2-L4. When FFM, Vitamin D intake, cBPAQ, pBPAQ, and tBPAQ were included in a step-
wise multiple linear regression analysis, FFM and pBPAQ were predictors of total hip, account-
ing for 16% (p = 0.024), while FFM and tBPAQ predicted 14% of the variance in FN
(p = 0.015). Only FFM predicted 15% of the variance in L2-L4 (p = 0.004).
The relationships between body composition variables and total hip, FN, and L2-L4 BMD
are shown in Table 3.
Significant positive relationships were found between weight, BMI, FFM, and total hip
BMD (p < 0.05). Pearson’s correlation tests showed positive relationships between weight,
BMI, FFM, and BMD at the left side of FN (p < 0.05). Also, weight (p < 0.01), BMI (p < 0.05),
and FFM (p = 0.001) were positively related to the L2-L4. There were no correlations between
% body fat and total hip, FN, and L2-L4 (p > 0.05). There was a positive correlation between
Vitamin D and L2-L4 (p = 0.025). All other dietary intake variables did not have significant
relationships with BMD variables (p > 0.05) (Table 4).

Discussion
The aim of this cross-sectional study was to determine the relationship between BPAQ scores
and body composition, and BMD in healthy young college women. Our study found that
BPAQ scores were positively related to total hip and FN BMD and no correlations were
detected in L2-L4. Also, the past and total component of BPAQ scores and FFM were signifi-
cant predictors of total hip (16%) and FN BMD (14%).
Weeks and Beck [18] reported that cBPAQ was a significant predictor of variance in FN,
lumbar spine, and whole body aBMD in young men (n = 20), but not in women (n = 20). How-
ever, our study showed that cBPAQ score was not sensitive to predict any relevant bone sites.
Bolam et al. [28] found that FN aBMD was positively related to all BPAQ scores, but total hip
and whole body aBMD were related to pBPAQ and tBPAQ in 36 healthy older men (n = 36).
Farr et al. [20] reported that BPAQ scores were not significantly associated with BSI or SSI at
femur and tibia sites, measured by pQCT in girls. A study by Kindler et al. [25] found that
BPAQ scores were correlated with all mid-tibia cortical bone architecture at the non-dominant
leg (r = 0.41–0.51), assessed by magnetic resonance imaging (MRI) and most aBMD (r = 0.47–
0.53) measures in non-Hispanic white adolescent females (n = 24).
The inconsistent results may be due to differences in bone measurements (DXA, pQCT,
and MRI) and bone parameters (aBMD, geometry, and microstructure). In addition, most

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 Bone-Specific Physical Activity Score and Bone Mineral Density

Fig 1. Correlation of BPAQ scores with total hip and FN BMD. A, pBPAQ score with total hip BMD (r = 0.308,
p = 0.008). B, FN BMD (r = 0.309, p = 0.008). C, cBPAQ score with total hip BMD (r = 0.286, p = 0.014). D, FN BMD
(r = 0.311, p = 0.007). E, cBPAQ score with total hip BMD (r = 0.076, p = 0.520). F, cBPAQ score with FN BMD
(r = 0.122, p = 0.303). FN: femoral neck
doi:10.1371/journal.pone.0162127.g001

previous BPAQ studies for women have used relatively small sample sizes and correlations
between the BPAQ scores and aBMD at common osteoporotic fracture sites may be age-depen-
dent (children, adolescent, and young women) [28]. In the current study, all three BPAQ scores
did not predict L2-L4 aBMD, and similar results were found in older men [28] and young
women [18]. As a result, BPAQ scores (past and total) would be strong predictors of FN and
total hip aBMD in healthy young college women.
Based on the World Health Organization (WHO) criteria for diagnosis of osteoporosis [29],
in the current study, 24.7% and 27.4% of the participants were classified as osteopenia FN and

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 Bone-Specific Physical Activity Score and Bone Mineral Density

Table 3. Correlation of Body Composition Variables with BMD (N = 73).

Variables Total hip FN L2-L4
Weight (kg) .297* .273* .343**
BMI (kg/m2) .289* .270* .283*
FFM (kg) .278* .238* .396***
% body fat (%) .215 .221 .158

BMI: body mass index, FFM: fat free mass

*p < 0.05
**p < 0.01
***p = 0.001

doi:10.1371/journal.pone.0162127.t003

L2-L4, respectively. Compared with previous results [30, 31], our participants had a lower risk
of osteopenia bones (24.7%-27.4% vs. 33.5%-45.9%), but over 70% of the participants with nor-
mal T-score (T-score  -1.0) had relatively lower mean T-scores (-0.37). Also, our participants
showed lower calcium (432.3 ± 236.7 mg) and Vitamin D intake (3.7 ± 3.9 mcg) and these
results did not meet the recommended dietary allowances for calcium (1000 mg/day) and Vita-
min D intake(15 mcg/day) [32]. Previous studies have shown similar results, suggesting that
college women with inadequate calcium consumption and Vitamin D intake increased the risk
of fractures and osteoporosis [11, 30, 31]. Considering that up to 90% of peak bone mass is
obtained by age 18 in girls, the importance of osteoporosis awareness and effective bone
healthy behaviors for college women would be needed to prevent serious bone diseases in later
life.
In the current study, weight, BMI, and FFM were positively related to the total hip, FN, and
L2-L4, but % body fat was not significantly correlated. These findings are consistent with previ-
ous studies showing lower BMI was associated with lower BMD [33, 34]. Also, among body
composition variables, our study showed that the FFM was a relevant factor related to bone
sites and was strongly associated with L2-L4 (r = 0.396, p = 0.001). We found that none of the
bone measurement sites was correlated with % body fat. Lee et al. [35] reported that lean body
mass, muscle mass, and fat mass had positive relationships with lumbar spine and FN aBMD,
but % body fat was only related to FN and not lumbar spine in young healthy women. How-
ever, another study showed that fat mass and BMD had a negative correlation in premeno-
pausal women [36]. Similarly, fat mass showed a negative association with FN and femur
aBMD in healthy Caucasian women [37]. Park et al. [38] suggested that both lean mass and fat
mass had positive genetic correlations, but increased lean mass would be more beneficial for
BMD in middle-aged Korean women. The relationships between fat components and BMD

Table 4. Correlation of Dietary Intake Variables with BMD (N = 73).

Variables Total hip FN L2-L4
Total caloric intake (kcal) .142 .052 .115
Protein (g) .165 .125 .208
Carbohydrate (g) .060 .025 .030
Fat (g) .165 .036 .105
Magnesium (mg) -.027 -.076 .084
Vitamin D (mcg) .065 .076 .262*
Calcium (mg) .062 .041 -.107

*p < 0.05

doi:10.1371/journal.pone.0162127.t004

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 Bone-Specific Physical Activity Score and Bone Mineral Density

have shown conflicting results, suggesting that the age, gender, and menopausal status would
differently affect the results [36]. Further studies are needed to determine effects of fat on bone
density and provide healthy body composition of maintaining bone health in young college
women.
There are several limitations to our study. Although a qualified researcher in detail
explained and assisted with the BPAQ questionnaire, the participants’ recall errors would affect
the individual BPAQ scores. We also used a 24-hour food intake recall questionnaire to identify
dietary factors that affect BMD in healthy young college women, but this method would not
represent participants’ normal diets. For future study, 3-day dietary log (two days during the
week and one day during the weekend) would be more useful to represent normal dietary
intake in this population. While most previous studies have widely used DXA to measure body
composition components to investigate their relation to BMD, X-scan plus II was used in the
current study. Even though the BIA has provided a relatively accurate prediction of % body fat
in individuals with normal weight, overweight or obesity [39] and FFM in healthy Asian indi-
viduals [40], several studies have reported that it is influenced by different ethnic groups [41]
and gender [42]. Therefore, ethnicity, age, and gender might be considerable factors to com-
pare results from different body composition measurement tools.

Conclusion
Our findings indicated that BPAQ scores were positively related to total hip and FN BMD and
no correlations were detected in L2-L4. Also, BPAQ scores (past and total) and FFM were sig-
nificant predictors of the proximal femur of non-dominant side leg. Except for % body fat,
body composition components were positively related to the relevant bone sites. Our study
suggests that osteoporosis awareness and effective bone healthy behaviors for college women
are required to prevent serious bone diseases later in life.

Supporting Information
S1 File. Raw data of Fig 1.
(XLSX)

Author Contributions
Conceived and designed the experiments: SJK DJS.
Performed the experiments: SJK.
Analyzed the data: SJK DJS.
Wrote the paper: SJK DJS.
Data interpretation: SJK WYS JK DJS.

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