A dietary pattern rich in calcium, potassium, and protein is associated
with tibia bone mineral content and strength in young adults entering
initial military training
Anna T Nakayama,1,3 Laura J Lutz,3 Adela Hruby,2,5 James P Karl,1 James P McClung,4 and Erin Gaffney-Stomberg3
1 OakRidge Institute for Science and Education supporting the Military Performance Division and; 2 Oak Ridge Institute for Science and Education supporting
the Military Nutrition Division and; 3 Military Performance and; 4 Military Nutrition Divisions, US Army Research Institute of Environmental Medicine, Natick,
MA; and 5 Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, MA
ABSTRACT
Background: Stress fracture risk is elevated during initial military
training (IMT), particularly in lower-extremity bones such as the
tibia. Although the etiology of stress fractures is multifactorial, lower
bone strength increases risk.
Objective: The objective of this study was to assess, through the use
of peripheral quantitative computed tomography, whether adherence
to a dietary pattern rich in calcium, potassium, and protein before
IMT is positively associated with bone indexes in young adults
entering IMT.
Design: A cross-sectional analysis was performed with the use of
baseline data from 3 randomized controlled trials in Army, Air
Force, and Marine recruits (n = 401; 179 men, 222 women).
Dietary intake was estimated from a food-frequency questionnaire.
A dietary pattern characterized by calcium, potassium, and protein
was derived via reduced rank regression and a pattern z score
was computed for each volunteer, where higher scores indicated
greater adherence to the pattern. At the 4% (metaphysis) and
14% (diaphysis) sites of the tibia, bone mineral content (BMC),
volumetric bone mineral density, robustness, and strength indexes
were evaluated. Associations between dietary pattern z score as the
predictor variable and bone indexes as the response variables were
evaluated by multiple linear regression.
Results: Pattern z score was positively associated with BMC
(P = 0.004) and strength (P = 0.01) at the metaphysis and with BMC
(P = 0.0002), strength (P = 0.0006), and robustness (P = 0.02) at
the diaphysis when controlling for age, sex, race, energy, smoking,
education, and exercise. Further adjustment for BMI attenuated the
associations, except with diaphyseal BMC (P = 0.005) and strength
(P = 0.01). When height and weight were used in place of body mass
index, the association with BMC remained (P = 0.046).
Conclusions: A dietary pattern rich in calcium, potassium, and
protein is positively associated with measures of tibia BMC and
strength in recruits entering IMT. Whether adherence to this dietary
pattern before IMT affects injury susceptibility during training
remains to be determined. These trials were registered at clinicaltr
ials.gov as NCT01617109 and NCT02636348. Am J Clin Nutr
2019;109:186–196.
186 Am J Clin Nutr 2019;109:186–196. Printed in USA. © 2019 American Society for Nutrition. This work is written by (a) US Government employee(s)
and is in the public domain in the US.
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Keywords: nutrition, bone, peripheral QCT, exercise, calcium
Introduction
Bone mineral density (BMD) is the single best predictor
of lifetime fracture risk. Thus, maximizing the attainment of
peak bone mass (PBM) and strength through lifestyle choices
including adequiate nutrition in late adolescence and early
adulthood is one of the primary prevention strategies for reducing
osteoporotic fracture risk in adulthood (1–3). Historically,
nutrition and bone-related research has followed a reductionist
approach to identify key individual nutrients that affect bone
health (4). Although it is valuable to understand the effects of
individual nutrients, this method fails to capture the synergy of
nutrients and may fail to elucidate individual nutrient effects
because of high correlations between nutrients within foods (5).
In addition, dietary recommendations are more easily translated
to the public in terms of foods, rather than in terms of nutrients.
Therefore, recent focus in the nutrition and bone health field has
Supported by the US Army Medical Research and Materiel Command.
The study sponsor had no role in study design; collection, analysis, and
interpretation of data; writing the report; nor the decision to submit the report
for publication. The views and assertions expressed herein are those of the
authors and do not reflect the official policy of the Department of Army,
Department of Defense, or the US government. Any citations of commercial
organizations and trade names in this report do not constitute an official
Department of the Army endorsement or approval of the products or services
of these organizations.
Address correspondence to EG-S (e-mail: erin.g.stomberg.civ@mail.mil).
Abbreviations used: BMC, bone mineral content; BMD, bone mineral
density; BSI, bone strength index; DXA, dual-energy X-ray absorptiometry;
FFQ, food-frequency questionnaire; IMT, initial military training; PBM,
peak bone mass; pQCT, peripheral quantitative computed tomography; RDA,
Recommended Dietary Allowance; RRR, reduced rank regression; SSIp,
polar stress strain index; vBMD, volumetric bone mineral density.
Received March 28, 2018. Accepted for publication July 20, 2018.
First published online January 5, 2019; doi: https://doi.org/10.1093/
ajcn/nqy199.
 Dietary patterns and bone health in recruits
shifted towards identifying dietary patterns that are associated
with BMD (6–15) and fracture risk (16, 17), primarily in older
individuals. In general, diets rich in fruits, vegetables, whole
grains, and low-fat dairy are associated with higher BMD, lower
risk of osteoporotic fracture, and decreased bone resorption (10,
12–15, 18–20), whereas diets characterized by higher intakes of
soft drinks, processed, fried, and refined foods are associated
with lower BMD (11, 14, 15, 18, 21, 22). However, there is a
paucity of information regarding dietary patterns associated with
bone health and bone accretion in adolescents or young adults
(9, 10, 23, 24), a critical life stage at which PBM is typically
achieved (25).
Dietary patterns can be derived from diet intake data through
the use of 2 main methods: a priori and a posteriori (26).
The a priori method uses already established dietary indexes to
assess an individual’s compliance with dietary recommendations,
whereas the a posteriori method uses statistical methods to
identify a dietary pattern based on the data. A posteriori methods
include the following: factor analysis, which statistically groups
like foods together, and cluster analysis, which statistically
groups volunteers together based on characteristics. Reduced
rank regression (RRR) combines each of these approaches in that
dietary patterns are derived a posteriori based on intake data, but
response variables are selected a priori based on prior knowledge
of the biological effects of these variables (e.g., specific nutrients)
on the health outcome of interest (e.g., bone health) (27). In
this way, RRR offers the advantage of building upon biological
pathways known to be associated with health outcomes. Although
the relations between certain dietary patterns derived with the
use of factor or cluster analyses, such as the healthy, Western,
and traditional patterns, are consistently related to bone health
in adult and elderly populations (12–14, 16, 28), the limited
results obtained from these a posteriori approaches in children
and adolescents have been mixed (8, 18, 23, 29). Three recent
studies used RRR to identify dietary patterns associated with
high calcium, potassium, and protein intake; one of these studies
also included vitamin D intake. Each study identified significant
positive associations between the resulting dietary pattern and
bone mineral content (BMC) or BMD in populations of older
(7, 30) and young (10) adults. However, none of these studies
evaluated the relation in young adults between a dietary pattern
rich in calcium, potassium, and protein and bone health indexes
at sites prone to stress fracture such as the tibia. Given the known
importance of these nutrients for bone health, and the inconsistent
findings relating dietary patterns derived with the use of factor
or cluster analyses, we sought to determine whether a dietary
pattern characterized by high intakes of calcium, potassium, and
protein identified via RRR was associated with bone health in
young adults.
Bone health is of particular concern during initial military
training (IMT) due to the relatively high incidence of stress
fractures (31). IMT is the period of time when civilian recruits
undergo intensive physical and mental training to become
military personnel and lasts 2–3 mo based on the military
branch. The majority of these fractures occur in the lower
extremities, with 39.6% occurring in the tibia or fibula (32).
Despite the importance of this issue, much work remains
regarding the pathophysiology of stress fracture and the risk
187
factors for poor bone health upon entrance to training (33).
To our knowledge, no study has evaluated whether dietary
patterns before training are associated with bone health in recruits
entering training. Few studies have evaluated bone site–specific
associations with dietary patterns through the use of peripheral
quantitative computed tomography (pQCT), which allows for
the quantification of strength and volumetric BMD (vBMD), as
opposed to the more common dual-energy X-ray absorptiometry
(DXA), which captures areal BMD (26, 34). In a scoping review
of dietary patterns and bone health, only 2 studies were noted to
use pQCT (6, 7); of these, only 1 evaluated the site of interest, the
tibia, and this was in elderly adults (26). Thus, there is a paucity
of data on the impact of dietary patterns on weight-bearing bones
in which stress fractures most commonly occur. The aim of the
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present study was to examine dietary patterns identified via RRR
in a sample of young adults entering IMT and evaluate whether
a pattern characterized by higher intakes of calcium, potassium,
and protein was associated with pQCT indexes of bone health at
the tibia.
Methods
Study design and volunteers
The present study was a retrospective analysis of data from
3 studies that assessed the efficacy of calcium and vitamin D
supplementation for optimizing bone health during IMT in Army,
Air Force, and Marine recruits (35). All studies were approved
by the Institutional Review Board at the US Army Research
Institute of Environmental Medicine and were registered at clin-
icaltrials.gov (NCT01617109 for the Army and Air Force trial;
NCT02636348 for the trial in Marines). Recruits were excluded
if they were pregnant or breastfeeding; had a history of kidney
stones, kidney disease, endocrine disorders, or bone-modifying
disorders; or were allergic to any component of the intervention
food product. For each branch of the military, 2 recruit classes
were briefed on study participation at the start of training: Army
(June 2012, February 2013), Air Force (October 2013, March
2014), and Marines (July 2015, February 2016). A total of 2194
recruits were briefed (890 Army, 369 Air Force, 935 Marines)
and 1214 recruits (492 Army, 342 Air Force, 380 Marines)
gave their free and informed written consent to participate in
the studies (Figure 1). Study sample sizes were based on the
primary objective related to nutrient supplementation and bone
health (35). Due to time constraints, not all volunteers could
receive pQCT scanning; thus, a subset of 480 volunteers (119
Army, 56 Air Force, 305 Marine recruits) were block-randomized
by race and sex by the principal investigator and/or project
coordinators to undergo pQCT scanning of the tibia and were
eligible for this analysis. However, 12 of these volunteers were
excluded because of an invalid pQCT scan. Volunteers were
also excluded for missing or incomplete dietary or covariate
information (n = 8) and implausible daily calorie intake (n = 59;
women, <300 or >4500 kcal; men, <800 or >5000 kcal) (36).
Only baseline data collected at the start of IMT, and before study
interventions or training were initiated, were used for the current
analysis. The final analytic sample consisted of 401 men and
women.
188 Nakayama et al.

Briefed (n = 2194): Army

(n = 890), Air Force (n = 369),
Marines (935)

Excluded (n = 980)
♦ Declined to participate (n = 980): Army

Randomized (n = 1214): Army

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(n = 492), Air Force (n = 342),
Marines (380)

Excluded from analysis (n = 734)

♦ Not randomized to receive pQCT
scan: Army (n = 373), Air Force
(n = 286), Marines (75)

Had pQCT scans (n = 480):

Army (n = 119), Air Force (n = 56),
Marines (305)

Excluded from analysis (n = 12):

♦ invalid pQCT scans due to

pQCT scans were valid

(n = 468): Army (n = 117), Air
Force (n = 49), Marines (n = 302)

Excluded from analysis (n = 67):

♦ Incomplete or missing dietary or
covariate data (n = 8)
♦ Implausible daily calorie intake

Analysed (n = 401): Army

(n = 97), Air Force (n = 40),
Marines (n = 264)

FIGURE 1 Study flow diagram. pQCT, peripheral quantitative computed tomography.

Dietary intake
Under the supervision of registered dietitians, volunteers
completed a validated food-frequency questionnaire (FFQ;
NutritionQuest) to estimate daily nutrient and food group intake.
Volunteers were asked to specify the quantity and frequency
of food and beverage items they typically consume with the
use of pictures to help estimate portion sizes. The questionnaire
also asked about use of dietary supplements; however, because
only 4.2% of all volunteers reported taking calcium supplements
(≥500 mg Ca/d), this was not included as a confounder. Two
versions of the FFQ, Block 2005 and Block 2014, were used,
 Dietary patterns and bone health in recruits
because an updated version was released before the completion
of all 3 studies. The Block 2005 was used for the Army and
Air Force and includes ˜110 food and beverage items to estimate
average daily nutrient intake over the past 3 mo. The food list
was developed from NHANES 1999–2002 dietary recall data,
and the nutrient database was developed from the USDA Food
and Nutrient Database for Dietary Studies (FNDDS) version 1.0
and MyPyramid Equivalents Database version 2.0. The Block
2014 was used for all the Marine recruits and includes ˜127 food
and beverage items and asks individuals to report intake over the
past 6 mo. The food list was developed from NHANES dietary
recall data 2007–2008 and 2009–2010, and the nutrient database
was developed from the USDA Food and Nutrient Database for
Dietary Studies (FNDDS 5.0), the Food Pyramid Equivalents
Database (FPED), and the Nutrient Database for Standard
Reference (SR27). All FFQs were analyzed by NutritionQuest.
Both versions yield comparable nutrient intake output variables;
however, Block 2014 provides a more expansive list. The
predetermined food group output variables differed between
versions by name and/or food item classifications within each
group. NutritionQuest was consulted in order to ensure data from
the 2 FFQ versions were merged appropriately.
Bone health
The subset of volunteers randomly assigned to undergo pQCT
scanning (Stratec XCT 2000, XCT 3000; Stratec Medizintechnik
GmbH) received scans of the metaphysis and diaphysis of
the nondominant tibia (4% and 14% sites, respectively, cor-
responding to the distance from the medial malleolus to the
tibial plateau) before initiating IMT. If there was a history
of bone injury, the contralateral limb was scanned. All scans
were performed by a credentialed technician. Image processing
and calculation of bone indexes were performed according to
the manufacturer’s software package (Stratec Medizintechnik)
as described previously (35). Briefly, slice thickness was 2
mm and voxel size was set at 0.4 mm with a scanning speed
of 20 mm/s. Contour mode 3 at 169 mg/cm3 was used to
define total bone and peel mode 4 at 650 mg/cm3 , with a 10%
peel used to identify trabecular bone; contour mode 1 at 710
mg/cm3 and cort mode 2 at 710 mg/cm3 were used to define
cortical markers. Bone indexes included BMC (total BMC at the
metaphysis, cortical BMC at the diaphysis), vBMD (total vBMD
at the metaphysis; cortical vBMD at the diaphysis), strength
[total bone strength index (BSI; = bone cross-sectional area ×
vBMD) at the metaphysis; polar stress strain index (SSIp) at the
diaphysis], and robustness (cross-sectional area/tibia length; both
sites) (37). All scans were assessed for validity and excluded
if high movement was noted (Visual Inspection Rating System
score >3.3) (38).
Covariates
Volunteers completed a background survey that quantified self-
reported age (years), sex (male, female), race (white, African
American, other), physical activity level (frequency of exercise
or sports per week over the last 3 mo), smoking history
(current/former or never), and educational level (some/all of high
189
school, some college). Standing height was measured with the
use of a stadiometer (Creative Health Products), and weight was
measured with the use of a calibrated electronic scale (Befour
Scales).
Dietary pattern
After combining the 2 versions of the FFQ, 27 food groups
remained. RRR was used to identify a single pattern, or factor,
related to the intake of specific nutrients with known relations to
bone health: calcium (grams per kilocalorie), potassium (grams
per kilocalorie), and protein (percentage of total energy) (3, 25,
39, 40). Although vitamin D has been shown to have a beneficial
relation with bone (25), it was not included because of minimal
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intake from food sources. Food groups were considered the
predictor variables in the RRR, and average intake densities of
the 3 nutrients of interest were the response variables. Factor
scores resulting from RRR were transformed into z scores and
assigned to each volunteer, which quantify how well a volunteer’s
intake fits a dietary pattern dense in calcium, potassium,
and protein. Regression was also performed on men and
women separately, although both sexes yielded similar patterns;
as such, the combined pattern was used for all subsequent
analyses.
Statistical analyses
Baseline characteristics are presented as means ± SDs or
percentages. Dietary pattern z scores were derived as described
previously and treated as a continuous variable in multivariate
linear regression estimating the association between pattern z
scores and bone indexes. z Scores were also categorized into
quartile categories, assigned the median values in each quartile
category, and used as a continuous variable to estimate least-
squares adjusted means (SEs) of bone indexes in increasing quar-
tiles of the dietary pattern z score. Model 1 adjusted for age, sex,
race, and energy intake. Model 2 further adjusted for smoking
history, educational level, and exercise. Model 3 included all of
the aforementioned covariates and BMI (in kg/m2 ). Finally, as an
alternate approach to account for body size, model 4 included all
covariates in model 2 and height and weight. All analyses were 2-
tailed with an α level of 0.05. All analyses were conducted in SAS
(version 9.4; SAS Institute). As a secondary analysis, this study
was not explicitly designed to answer the present study question
and post hoc calculations were used to determine the minimum
significant differences in the dependent variables that could be
expected with α = 0.05 and β = 0.80.
Results
Volunteer characteristics
Volunteer demographic and anthropometric characteristics are
shown in Table 1. Approximately half of the sample were women
and the majority were white. Most volunteers were physically
active, with 95% reporting physical activity ≥2 times/wk before
entering IMT. Consistent with military body-weight standards,
mean BMI was in the normal range, and no volunteer was
categorized as obese (BMI >30).
190 Nakayama et al.

TABLE 1 Anthropometric, demographic, and dietary characteristics by dietary pattern z score quartile1

z Score quartile (median)

Characteristic Total −1.05 −0.25 0.23 1.12 P-trend2

n 100 100 101 100
Female, % 55.4 47 60 59 55 0.30
Race, %
White 66.8 50 69 70 78 <0.001
Black 23.9 41 23 18 14
Other 9.2 9 8 12 8
Smoking, past or present, % 13.7 18 17 7 13 0.16
At least some college, % 35.4 23 33 42 44 0.001
Age, y 19.6 ± 2.7 19.5 ± 0.3 19.4 ± 0.3 19.6 ± 0.3 19.7 ± 0.3 0.48
BMI, kg/m2 24.0 ± 2.8 23.5 ± 0.3 23.7 ± 0.3 24.3 ± 0.3 24.7 ± 0.3 0.001
167.7 ± 9.1 169.0 ± 166.9 ± 166.0 ± 169.0 ±

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Height, cm 0.9 0.9 0.9 0.9 0.96
Weight, kg 68.1 ± 11.6 67.6 ± 1.2 66.5 ± 1.2 67.4 ± 1.2 70.9 ± 1.2 0.03
Physical activity (frequency of exercise per week) 5.5 ± 2.0 4.8 ± 0.2 5.1 ± 0.2 5.6 ± 0.2 6.4 ± 0.2 <0.001
at entry3
Dietary variables
Energy, kcal 2144 ± 979 2687 ± 92 1933 ± 92 1833 ± 92 2126 ± 92 <0.001
Calcium, mg 1050 ± 552 1026 ± 494 879 ± 436 906 ± 475 1392 ± 632 <0.001
Potassium, mg 2659 ± 1227 2695 ± 1128 2255 ± 1090 2417 ± 1175 3270 ± 1273 <0.001
Protein, g/kg body weight 1.2 ± 0.6 1.4 ± 0.1 1.1 ± 0.1 1.2 ± 0.1 1.3 ± 0.1 0.83
Calcium, g/1000 kcal 0.50 ± 0.02 0.37 ± 0.01 0.46 ± 0.01 0.51 ± 0.01 0.67 ± 0.01 <0.001
Potassium, g/1000 kcal 1.3 ± 0.03 0.99 ± 0.02 1.16 ± 0.02 1.35 ± 0.02 1.59 ± 0.02 <0.001
Protein, g/1000 kcal 38.8 ± 7.4 33.5 ± 0.6 36.9 ± 0.6 41.1 ± 0.6 43.9 ± 0.6 <0.001
Protein, % of energy 15.5 ± 2.9 13.4 ± 0.3 14.8 ± 0.3 16.4 ± 0.3 17.6 ± 0.3 <0.001
Carbohydrates, % of energy 48.4 ± 7.8 49.9 ± 0.8 47.8 ± 0.8 47.0 ± 0.8 48.8 ± 0.8 0.27
Fat, % of energy 36.8 ± 6.1 37.2 ± 0.6 37.8 ± 0.6 37.5 ± 0.6 34.5 ± 0.6 0.001
Added sugars, teaspoon equivalents 17.3 ± 11.7 27.7 ± 1.0 15.4 ± 1.0 11.8 ± 1.0 14.5 ± 1.0 <0.001
Oils, g 23.4 ± 14.8 31.7 ± 1.4 22.2 ± 1.4 19.9 ± 1.4 20.0 ± 1.4 <0.001
Solid fat, g 45.5 ± 25.0 58.1 ± 2.4 42.4 ± 2.4 39.1 ± 2.4 42.4 ± 2.4 <0.001
Cheese, milk-equivalent servings 0.8 ± 0.6 0.9 ± 0.1 0.8 ± 0.1 0.7 ± 0.1 0.8 ± 0.1 0.13
Milk, cups 1.0 ± 1.1 0.8 ± 0.1 0.7 ± 0.1 0.8 ± 0.1 2.0 ± 0.1 <0.001
Yogurt, cups 0.07 ± 0.1 0.04 ± 0.01 0.05 ± 0.01 0.06 ± 0.01 0.13 ± 0.01 <0.001
Fruit, cups
Citrus, melon, berries 0.4 ± 0.4 0.4 ± 0.0 0.3 ± 0.0 0.3 ± 0.0 0.5 ± 0.0 0.19
Other 0.7 ± 0.7 0.6 ± 0.1 0.5 ± 0.1 0.7 ± 0.1 0.9 ± 0.1 <0.001
Fruit juice, cups 0.5 ± 0.6 0.5 ± 0.1 0.4 ± 0.1 0.5 ± 0.1 0.5 ± 0.1 0.23
Refined grains, ounce equivalents 4.6 ± 3.1 7.0 ± 0.3 4.8 ± 0.3 4.2 ± 0.3 3.8 ± 0.3 <0.001
Whole grains, ounce equivalents 1.1 ± 1.0 1.2 ± 0.1 1.0 ± 0.1 1.0 ± 0.1 1.3 ± 0.1 0.39
Legumes, cups 0.11 ± 0.16 0.11 ± 0.02 0.09 ± 0.02 0.13 ± 0.02 0.11 ± 0.02 0.50
Eggs, lean meat ounce equivalents 0.7 ± 0.6 0.6 ± 0.1 0.6 ± 0.1 0.6 ± 0.1 0.8 ± 0.1 0.09
Seafood, ounces
High in ω-3 0.2 ± 0.3 0.1 ± 0.0 0.1 ± 0.0 0.2 ± 0.0 0.3 ± 0.0 <0.001
Low in ω-3 0.4 ± 0.6 0.4 ± 0.1 0.3 ± 0.1 0.4 ± 0.1 0.5 ± 0.1 0.40
Cured meat, ounces 0.9 ± 0.8 1.1 ± 0.1 0.8 ± 0.1 0.8 ± 0.1 0.9 ± 0.1 0.16
Red meat, ounces 1.8 ± 1.7 2.2 ± 0.2 1.6 ± 0.2 1.7 ± 0.2 1.7 ± 0.2 0.046
Nuts and seeds, lean meat ounce equivalents 0.8 ± 1.0 1.0 ± 0.1 0.5 ± 0.1 0.7 ± 0.1 0.9 ± 0.1 0.83
Organ meats, ounces 0.03 ± 0.1 0.04 ± 0.01 0.04 ± 0.01 0.02 ± 0.01 0.02 ± 0.01 0.13
Poultry, ounces 1.0 ± 1.2 1.1 ± 0.1 0.9 ± 0.1 1.2 ± 0.1 0.9 ± 0.1 0.20
Soy products, cups 0.19 ± 0.7 0.12 ± 0.07 0.12 ± 0.07 0.19 ± 0.07 0.33 ± 0.07 0.03
Vegetables, cups
Red, orange, yellow 0.11 ± 0.14 0.08 ± 0.01 0.08 ± 0.01 0.12 ± 0.01 0.16 ± 0.01 <0.001
Dark-green 0.22 ± 0.31 0.13 ± 0.03 0.14 ± 0.03 0.24 ± 0.03 0.39 ± 0.03 <0.001
Other 0.45 ± 0.38 0.36 ± 0.04 0.35 ± 0.04 0.48 ± 0.04 0.61 ± 0.04 <0.001
Potatoes, cups 0.28 ± 0.24 0.36 ± 0.02 0.30 ± 0.02 0.22 ± 0.02 0.24 ± 0.02 <0.001
Vegetables—starchy, cups 0.09 ± 0.10 0.09 ± 0.01 0.07 ± 0.01 0.10 ± 0.01 0.11 ± 0.01 0.08
Vegetables—tomatoes and tomato products, cups 0.25 ± 0.21 0.27 ± 0.02 0.22 ± 0.02 0.25 ± 0.02 0.27 ± 0.02 0.76
Total dairy, milk-equivalent servings 1.9 ± 1.3 1.7 ± 0.1 1.6 ± 0.1 1.5 ± 0.1 2.9 ± 0.1 <0.001
Total fruit, cups 1.3 ± 1.1 1.2 ± 0.1 1.0 ± 0.1 1.3 ± 0.1 1.7 ± 0.1 0.003
Total grains, ounce equivalents 6.1 ± 3.6 8.2 ± 0.3 5.8 ± 0.3 5.2 ± 0.3 5.1 ± 0.3 <0.001
Total meat, ounces 4.4 ± 3.1 5.1 ± 0.3 3.9 ± 0.3 4.4 ± 0.3 4.3 ± 0.3 0.15
Total vegetables, cups 1.4 ± 0.94 1.29 ± 0.09 1.16 ± 0.09 1.42 ± 0.09 1.78 ± 0.09 <0.001
1n = 401. Values are means ± SDs unless otherwise indicated. 1 cup = 8 fluid ounces or 240 mL; 1 fluid ounce = 30 mL; 1 solid ounce = 28 g; 1
teaspoon = 5 mL. Conversion for nonfluid items varies based on density. Conversion to metric units for individual food items can be found at
https://ndb.nal.usda.gov/ndb/search/list.
2 P-trends were derived from 1-factor ANOVA, except for race, which was derived from chi-square test.
3 One volunteer was missing a physical activity value.
 Dietary patterns and bone health in recruits
Dietary patterns
RRR yielded a dietary pattern explaining 44% of the variance
in the 3 response variables (calcium, potassium, and protein).
In addition, calcium, potassium, and protein were all positively
weighted (58%, 63%, and 52%, respectively), meaning that
this pattern was characterized by higher intakes of calcium,
potassium, and protein. The food groups and their factor loadings
indicated that this dietary pattern was characterized by higher
consumption of milk; dark-green, red, orange, and yellow
vegetables; yogurt; and other vegetables and lower consumption
of oils, refined grains, and added sugars (Figure 2).
Baseline characteristics of volunteers according to quartile
are presented in Table 1. Notably, the proportion of males
and black volunteers was higher in lower z score quartiles.
In addition, frequency of weekly physical activity was higher
across increasing quartiles. As expected, density of calcium
(g/1000 kcal), potassium (g/1000 kcal), and protein (percentage
of energy) intakes were higher across increasing quartiles. The
highest quartile had the highest intakes of milk; yogurt; fruits (not
including juice); soy products; dark-green, red, orange, yellow,
and other vegetables; and high-ω-3 seafood. Conversely, the
lowest quartile had the highest intake of added sugars, oils, and
refined grains.
Dietary pattern and bone health
There was a positive association between the dietary pattern
z score and BMC and BSI at the metaphysis in the group as
a whole, although these relations were no longer significant
once body-size measures were included in the model (models 3
and 4) (Table 2). At the diaphysis, the dietary pattern z score
was positively associated with BMC in all models. Positive
associations with SSIp were observed in models 1–3 but were
attenuated when weight and height were used to control for
body size, although there was a trend. Positive associations with
robustness were only observed in models that did not include
corrections for body size. In contrast, no relations between dietary
pattern z score and vBMD were observed at either site. The same
relations were observed when looking at the quartile categories
of dietary pattern z score (Table 2). In separate analyses of men
and women, there were no significant relations when body size
was added as a covariate, although there was a trend for BMC
(P = 0.057) and SSIp (P = 0.088) in women when BMI was
added (Table 3).
Post hoc power calculations based on the observed SDs
of the dependent variables indicated that the current analyses
were powered to detect unadjusted mean percentage differences
between extreme quartile categories of the pattern z score of
between 1% and 13%, depending on bone outcome measure. For
example, mean percentage difference was ˜9% (33.8 mg/mm) for
total BMC at the metaphysis, ˜7% (16.5 mg/mm) for BMC at the
diaphysis, and ˜10% (165 mm3 ) for SSIp.
Discussion
The main finding of this study was that a dietary pattern
characterized by higher densities of calcium, potassium, and
protein derived from higher intakes of milk, yogurt, and dark-
green, red, orange, yellow, and other vegetables and lower intakes
191
of oils, refined grains, and added sugars was positively associated
with tibia BMC and a trend toward strength in young adults
entering IMT. The association between adherence to this dietary
pattern and bone health was most notable in the cortical envelope
because these associations persisted even after controlling for all
covariates at the diaphysis. These results are consistent with other
studies that have beneficially related dietary patterns to bone
health (10, 12–14, 18–20). Specifically, other studies that used
similar RRR methodology found positive associations between
dietary patterns rich in calcium, potassium and protein and
indexes of bone health (7, 10). In one longitudinal study in older
women, greater adherence to a diet rich in calcium, potassium,
and protein over time was positively associated with greater BMC
and vBMD at the spine, hip, and radius as measured by DXA
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and pQCT (7). In a longitudinal study in 14- to 20-y-olds, the
dietary pattern was associated with higher whole-body BMD and
BMC as measured by DXA (10). The foods that characterized the
patterns in these 2 studies were similar to the pattern identified
in the present study, despite the use of different populations and
food-group classifications. Using a factor loading cutoff value of
|0.2|, the pattern identified by Ward et al. (7) was characterized
by greater intakes of low-fat milk, fruit, and low-fat yogurt and
reduced intakes of alcohol, potatoes, processed meats, sweet
cereal products, animal-based fats, white bread, and sugar and
preserves, whereas the pattern identified by van den Hooven et
al. (10) was characterized by increased intakes of low-fat dairy
products and whole grains and lower intakes of fried potatoes,
takeaway foods, soft drinks, confectionery, and chips. As such,
our findings are consistent with prior work showing positive
associations between a dietary pattern characterized by greater
intakes of calcium, potassium, and protein and measures of bone
health. The current study thus both strengthens and extends the
existing work evaluating dietary patterns and bone health because
it focuses on a site at high risk of stress fracture.
When body size was included in the statistical models, the
relations between dietary pattern z score and BMC, BSI, and
robustness at the metaphysis were no longer significant, whereas
the relations persisted for BMC at the diaphysis, along with SSIp
when BMI was used to indicate body size. These findings suggest
that body size may be mediating the effect of diet at the distal
tibia and/or adherence to the dietary pattern is not related to
bone strength independent of body size at this site. The young
adults entering military training were all categorized as having a
normal BMI (18.5–24.9) and reported being at least moderately
active; thus, higher BMI in this population may represent greater
lean mass or be a surrogate for starting fitness status. Higher
BMI and greater body size result in greater mechanical loading,
particularly at the distal site where compressive stress is sustained
during running and walking. As such, the distal site may be more
sensitive to recent changes in training as recruits prepare to meet
body-composition standards in preparation for entrance to the
military. The finding that dietary pattern z score was associated
with BMC and a trend toward strength at the diaphysis even when
body size was included suggests a direct effect of diet at this
site. This may indicate that diet affects skeletal sites differently
depending on the pattern of mechanical loading or may be related
to time course of tissue turnover, which is slower in cortical
compartments as compared with the trabecular envelope. This
relation could therefore reflect dietary intake over the previous
3–6 mo, the period that was evaluated with the FFQ. To our
192 Nakayama et al.

Factor Loadings

Milk*
Vegetables – dark green*
Yogurt*
Vegetables – other*
Vegetables – red, orange, yellow*
Seafood high in n-3 fatty acids
Fruit – other
Eggs
Soy products
Vegetables – starchy
Seafood low in n-3 fatty acids
Whole grains
Vegetables – tomatoes and tomato products

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Fruit juice
Legumes
Fruit – Citrus, melon, berries
Nuts and seeds
Cured meat
Cheese
Red meat
Organ meats
Poultry
Potatoes
Solid fat
Oils*
Refined grains*
Added sugars*
-0.50 -0.40 -0.30 -0.20 -0.10 0.00 0.10 0.20 0.30 0.40 0.50

FIGURE 2 Factor loadings for the dietary pattern. Dietary pattern was derived via reduced rank regression based on n = 401. ∗ Food groups with factor
loadings >|0.2| and considered characteristic of the dietary pattern.

knowledge, the site-specific effects of dietary pattern on tibia
variables in young adults is a novel finding.
In the present analysis, we identified a dietary pattern defined
by higher intake densities of selected nutrients, specifically
calcium, potassium, and protein, because prior research has
shown positive influences of these nutrients individually and
collectively on bone health (3, 25, 39, 40). One of the advantages
of dietary pattern research is the ability to translate nutrient intake
into food servings to provide applicable dietary recommendations
to the public. For example, the highest quartile of the score
in our study corresponded to a mean energy intake of ˜2100
kcal; milk intake of 2 cups; yogurt intake of 0.13 cups; dark-
green vegetable intake of was ˜0.4 cups; red, orange, and yellow
vegetables intake of 0.16 cups; and other vegetable intake of
0.6 cups. In addition, average daily intake of added sugars was
15 teaspoons, oil was ˜4 teaspoons, and refined grains was ˜4
ounces. When comparing these quantities to the USDA Healthy
US-Style Eating Pattern guidelines based on a 2000-kcal daily
intake level, the highest quartile of the present dietary pattern
showed a much higher intake of dark-green vegetables, a slightly
higher intake of refined grains and oils, and a much lower intake
of red, orange, and yellow vegetables (41). The highest quartile
was also the only quartile in which median calcium intake met the
Recommended Dietary Allowance (RDA) (42). Intakes of other
vegetables and added sugars were consistent with the USDA
healthy eating pattern. Whereas median protein intakes met the
RDA (0.8 g · kg−1 · d−1 ) in all quartiles, median potassium
intake did not reach the RDA in any quartile (43, 44). These
findings are consistent with NHANES data, which reported that
calcium and potassium are 2 shortfall nutrients in the general
population.
The current study has many strengths, including a robust
sample size and a racially diverse sample of young adults.
Interestingly, quartile 1 had the greatest proportion of black
volunteers compared with the other quartiles, indicating that more
blacks did not adhere to the dietary pattern rich in calcium,
potassium, and protein. This likely reduced the association
between dietary pattern and bone variables because black
individuals generally have greater bone mass and strength than
other ethnicities (45, 46). The current study was not powered
to look at interactions between dietary pattern and race on bone
indexes, but given the racial differences in bone health, this is
an important area for future study. Our study captured an age
range when PBM is attained, although characteristics such as
cortical density and structural strength are still adapting (25). To
our knowledge, this is the first report of associations between
dietary patterns and bone health in this age group. In addition,
the current study used pQCT to image the tibia which is able
to provide vBMD at a clinically relevant site as opposed to the
commonly used areal BMD obtained by DXA. Although we
identified a relation between overall diet and BMC and a trend
toward strength of the distal tibia, whether these relations affect
 Dietary patterns and bone health in recruits 193
TABLE 2 Least-squares adjusted means of outcomes, by quartile category of dietary pattern z score and continuous β per unit of dietary pattern z score1

Quartile category of dietary pattern z score, adjusted mean (SE)

1 2 3 4 P-linear Continuous β per

Dependent variable and model −1.05 (median) −0.25 (median) 0.23 (median) 1.12 (median) trend unit z score (SE) P
Metaphysis
Total BMC, mg/mm
1 350.50 (6.16) 355.64 (6.14) 359.21 (6.09) 374.07 (6.24) 0.003 9.184 (2.857) 0.001
2 349.78 (7.28) 354.75 (6.97) 357.63 (7.18) 372.12 (7.06) 0.007 8.702 (3.001) 0.004
3 351.89 (6.71) 354.04 (6.41) 352.22 (6.64) 364.57 (6.56) 0.11 5.378 (2.792) 0.06
4 352.58 (6.10) 354.08 (5.82) 355.29 (6.03) 359.74 (5.97) 0.31 2.939 (2.546) 0.25
Total vBMD, mg/cm3
1 342.98 (4.57) 345.53 (4.55) 348.79 (4.51) 350.23 (4.63) 0.20 3.197 (2.118) 0.13
2 343.34 (5.40) 345.22 (5.16) 347.50 (5.32) 348.66 (5.23) 0.38 2.571 (2.223) 0.25

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3 344.22 (5.27) 344.92 (5.04) 345.22 (5.22) 345.46 (5.15) 0.84 1.170 (2.192) 0.59
4 344.22 (5.26) 345.05 (5.02) 344.98 (5.20) 346.64 (5.15) 0.70 1.685 (2.196) 0.44
Total BSI, mg/mm4
1 122.65 (3.39) 124.69 (3.38) 127.75 (3.36) 133.16 (3.44) 0.013 4.512 (1.572) 0.004
2 122.33 (4.01) 124.10 (3.84) 126.56 (3.96) 131.79 (3.89) 0.035 4.157 (1.652) 0.01
3 123.41 (3.74) 123.74 (3.57) 123.76 (3.70) 127.89 (3.65) 0.29 2.445 (1.554) 0.12
4 123.67 (3.67) 123.80 (3.51) 124.72 (3.63) 126.67 (3.60) 0.46 1.803 (1.534) 0.24
Robustness, mm
1 2.66 (0.04) 2.66 (0.04) 2.73 (0.04) 2.75 (0.04) 0.037 0.031 (0.017) 0.08
2 2.66 (0.04) 2.66 (0.04) 2.72 (0.04) 2.75 (0.04) 0.041 0.031 (0.018) 0.09
3 2.66 (0.04) 2.65 (0.04) 2.70 (0.04) 2.72 (0.04) 0.21 0.017 (0.018) 0.34
4 2.67 (0.04) 2.65 (0.04) 2.71 (0.04) 2.70 (0.04) 0.36 0.009 (0.018) 0.62
Diaphysis
Cortical BMC, mg/mm
1 205.73 (3.20) 212.82 (3.22) 216.67 (3.18) 221.45 (3.28) 0.0002 6.000 (1.491) <0.0001
2 205.93 (3.80) 212.82 (3.64) 216.43 (3.75) 221.10 (3.71) 0.001 5.806 (1.563) 0.0002
3 207.11 (3.51) 212.32 (3.36) 213.36 (3.48) 217.45 (3.45) 0.01 4.132 (1.456) 0.005
4 207.60 (3.36) 212.19 (3.21) 214.42 (3.32) 215.68 (3.31) 0.046 3.175 (1.402) 0.02
Cortical vBMD, mg/cm3
1 1131.35 (2.09) 1133.42 (2.11) 1135.67 (2.08) 1131.94 (2.15) 0.81 0.090 (0.983) 0.93
2 1131.85 (2.49) 1133.71 (2.38) 1135.87 (2.46) 1132.12 (2.43) 0.93 − 0.027 (1.030) 0.98
3 1131.65 (2.48) 1133.80 (2.37) 1136.39 (2.46) 1132.74 (2.44) 0.71 0.240 (1.036) 0.82
4 1131.67 (2.46) 1133.80 (2.35) 1135.95 (2.44) 1133.35 (2.43) 0.56 0.564 (1.031) 0.58
SSIp, mm3
1 1502.59 (33.36) 1578.17 (33.60) 1591.91 (33.18) 1669.76 (34.21) 0.0002 59.032 (15.600) 0.0002
2 1512.28 (39.56) 1586.93 (37.87) 1600.92 (39.05) 1673.78 (38.66) 0.001 56.377 (16.314) 0.0006
3 1524.18 (36.70) 1581.89 (35.11) 1569.82 (36.41) 1636.85 (36.14) 0.014 39.418 (15.277) 0.01
4 1532.76 (31.01) 1578.24 (29.62) 1585.63 (30.70) 1602.10 (30.58) 0.07 21.159 (12.978) 0.10
Robustness, mm
1 1.15 (0.02) 1.17 (0.02) 1.20 (0.02) 1.22 (0.02) 0.004 0.023 (0.009) 0.01
2 1.16 (0.02) 1.18 (0.02) 1.21 (0.02) 1.22 (0.02) 0.006 0.022 (0.009) 0.02
3 1.16 (0.02) 1.18 (0.02) 1.19 (0.02) 1.21 (0.02) 0.07 0.013 (0.009) 0.13
4 1.17 (0.02) 1.17 (0.02) 1.20 (0.02) 1.20 (0.02) 0.18 0.008 (0.008) 0.35
1 n = 401. Reduced rank regression was used for analysis. Model 1: adjusted for age, sex, race, and energy intake; model 2: adjusted as for model 1, plus

smoking, education, and exercise; model 3: adjusted as for model 2 plus BMI; model 4: adjusted as for model 2 plus weight and height. BMC, bone mineral
content; BSI, bone strength index; SSIp, polar stress strength index; vBMD, volumetric bone mineral density.

bone adaptation and/or injury risk during IMT remains to be
determined. There were also several limitations of our study. The
cross-sectional nature of the analysis cannot speak to a temporal
relation between dietary patterns and bone health. Given the large
size of the parent study, diet information was collected with an
FFQ, which inherently lacks precision given its fixed food list
and quantity options. The FFQ reflects intake from the previous
3–6 mo, and it is possible that individuals changed eating habits in
preparation for IMT immediately before this time frame. Despite
the use of relatively recent dietary intake data to create a dietary
pattern, an association with bone health emerged. In addition,
dietary intake was assessed with the use of 2 different versions of
the FFQ and it is possible that the present analysis was affected.
However, distribution of the FFQ versions between the quartiles
of dietary pattern z score did not significantly differ. When men
and women were analyzed separately, z score was associated with
bone robustness in men, but not in women, but once body size was
included in the models this relation was no longer observed. This
finding suggests that dietary impacts on bone may be mediated
through effects on body size, at least in men. In sex-stratified
194 Nakayama et al.

TABLE 3 Relation between dietary pattern z score and pQCT bone markers by sex1

Men Women

Dependent variable and model β (SE) P β (SE) P

Metaphysis
Total BMC, mg/mm
1 11.270 (5.006) 0.03 6.400 (3.207) 0.047
2 12.057 (5.364) 0.03 5.076 (3.318) 0.13
3 4.523 (4.873) 0.35 4.300 (3.190) 0.18
4 4.331 (4.477) 0.33 0.933 (2.923) 0.75
Total vBMD, mg/cm3
1 2.331 (3.286) 0.48 3.860 (2.802) 0.17
2 1.993 (3.495) 0.57 2.956 (2.909) 0.31
3 − 0.765 (3.469) 0.83 2.549 (2.876) 0.38
− 0.492 (3.407)

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4 0.89 2.777 (2.927) 0.34
Total BSI, mg/mm4
1 5.149 (2.797) 0.07 3.272 (1.699) 0.06
2 5.205 (2.991) 0.08 2.600 (1.757) 0.14
3 1.282 (2.767) 0.64 2.227 (1.702) 0.19
4 1.337 (2.756) 0.63 1.164 (1.675) 0.49
Robustness, mm
1 0.060 (0.029) 0.04 0.003 (0.021) 0.91
2 0.067 (0.031) 0.03 − 0.001 (0.022) 0.95
3 0.041 (0.030) 0.18 − 0.006 (0.022) 0.79
4 0.039 (0.029) 0.18 − 0.013 (0.022) 0.57
Diaphysis
Cortical BMC, mg/mm
1 7.396 (2.559) 0.004 4.147 (1.746) 0.02
2 7.525 (2.721) 0.006 3.675 (1.816) 0.04
3 3.635 (2.458) 0.14 3.368 (1.762) 0.057
4 3.583 (2.403) 0.14 1.828 (1.683) 0.28
Cortical vBMD, mg/cm3
1 − 0.335 (1.417) 0.81 0.496 (1.379) 0.72
2 − 0.347 (1.510) 0.82 0.355 (1.437) 0.80
3 − 0.059 (1.552) 0.97 0.516 (1.421) 0.72
4 0.077 (1.504) 0.96 0.753 (1.443) 0.60
SSIp, mm3
1 76.819 (27.995) 0.007 38.836 (16.900) 0.02
2 81.252 (29.795) 0.007 32.003 (17.497) 0.07
3 39.407 (27.055) 0.15 29.074 (16.985) 0.088
4 35.573 (22.822) 0.12 6.131 (14.598) 0.67
Robustness, mm
1 0.034 (0.014) 0.02 0.012 (0.011) 0.27
2 0.037 (0.015) 0.01 0.009 (0.012) 0.41
3 0.019 (0.014) 0.17 0.007 (0.011) 0.52
4 0.018 (0.013) 0.17 0.002 (0.011) 0.86
1 n = 401. β per unit increase in the dietary pattern z score on bone indexes. Data were analyzed through the use of multivariate linear regression with

dietary pattern z score included as a continuous variable. Model 1: adjusted for age, race, and energy intake; model 2: adjusted as for model 1, plus smoking,
education, and exercise; model 3: adjusted as for model 2 plus BMI; model 4: adjusted as for model 2 plus weight and height. BMC, bone mineral content;
BSI, bone strength index; pQCT, peripheral quantitative computed tomography; SSIp, polar stress strength index; vBMD, volumetric bone mineral density.

analyses, the strength of the relations between dietary pattern z
score and BMC and SSIp was also attenuated, although the β
coefficients were similar and CIs largely positive, indicating that
we were likely underpowered for sex-stratified analyses. These
weaknesses associated with the current study would bias in the
direction of the null, and thus likely result in underestimations of
the true relations between this dietary pattern and bone variables
in this population.
In summary, our study of bone health in this underresearched
age group suggests that a diet rich in milk, yogurt, and vegetables
and lower in intakes of oils, refined grains, and added sugars,
resulting in higher intakes of calcium, potassium, and protein,
was associated with higher tibia BMC and perhaps strength in
young adults. This information may provide a foundation for
the development of recommendations for improving bone health
before entrance to IMT and other intensive physical training
that could potentially affect the risk of stress fracture in the
longer term. Because the data associated with the present study
were collected from young adults before they received any
intervention, these results are likely generalizable to healthy,
young adults during the period in which PBM is attained. In
the future, these results could inform focused diet education for
 Dietary patterns and bone health in recruits
young adults seeking to optimize bone health throughout the life
span.
We appreciate the support of the training sites and military leadership,
including COL SJ Cable and TL Cropper.
The authors’ responsibilities were as follows—EG-S, JPM, JPK, and ATN:
designed the research; EG-S, JPM, LJL, and ATN: conducted the research;
AH: analyzed the data; EG-S, AH, and ATN: drafted the manuscript; EG-
S: had primary responsibility for final content; and all authors: read and
approved the final manuscript content. None of the authors reported a conflict
of interest related to the study.
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