ARTICLE IN PRESS

Appetite 48 (2007) 359–367

www.elsevier.com/locate/appet

Research Report

Drive for thinness score is a proxy indicator of energy deficiency in

exercising women
Mary Jane De Souzaa,, Rayisa Hontscharuka, Marion Olmstedb,
Gretchen Kerra, Nancy I. Williamsc
a
Women’s Exercise and Bone Health Laboratory, Faculty of Physical Education and Health, University of Toronto, Toronto, Ont., Canada
b
Department of Psychiatry, University of Toronto, Toronto, Ont., Canada
c
Noll Laboratory, Department of Kinesiology, Penn State University, University Park, PA, USA
Received 8 August 2006; received in revised form 11 October 2006; accepted 13 October 2006

Abstract

The purpose of this study was to determine the association between drive for thinness (DT) and adaptations to energy deficiency in
exercising women. This observational study evaluated psychometric and metabolic factors in sedentary (n ¼ 9, 27.972.0 yr) and
exercising women (n ¼ 43, 24.071.1 yr). Volunteers were retrospectively grouped according to exercise status (sedentary or exercising)
and a DT score of normal (sedentary or exercising) or high (exercising only). Resting energy expenditure (REE) and metabolic hormones
(triiodothyronine, (TT3), ghrelin, leptin, insulin) were measured repeatedly over a 2–3 month period. The DT subscale successfully
discriminated the groups based on energy status. Although the groups did not differ in body weight, the high DT group exhibited
adaptations to chronic energy deficiency, including a REE below 90% of their predicted REE (8673.0%), significantly lower TT3 levels
and significantly higher ghrelin levels than the normal DT groups. Since energy deficiency plays a causal role in the Female Athlete Triad,
DT may serve as a proxy indicator of underlying energy deficiency and may be useful for identifying individuals at risk for Triad
disorders prior to the development of serious clinical sequelae.
r 2006 Elsevier Ltd. All rights reserved.

Keywords: Resting energy expenditure; Female athlete triad; Amenorrhea; Dietary cognitive restraint; Triiodothyronine

Introduction & Hirsch, 1995). The suppression of reproductive function

Energy deficiency causes weight loss as well as a cascade of
metabolic shifts that act to conserve energy, including a
decrease in resting energy expenditure (REE), and alterations
in metabolic hormone concentrations, including triiodothyr-
onine (TT3), insulin-like growth factor-1 (IGF-1) and ghrelin
(Danforth & Burger, 1984; Danforth & Burger, 1989;
De Souza, Leidy, O’Donnell, Lasley, & Williams, 2004a;
Laughlin & Yen, 1996). Low body weight is not always an
indicator of chronic energy deficiency, as the aforementioned
metabolic adaptations to lower energy expenditure can
reduce weight loss and result in weight stability and the
restoration in energy balance, albeit with alterations in
metabolic and endocrine homeostasis (Leibel, Rosenbaum,
Corresponding author.
E-mail address: maryjane.desouza@utoronto.ca (M.J. De Souza).
during conditions of energy deficiency is well recognized in
the animal literature and is thought to be an adaptive
response to conserve fuel for more vital bodily processes,
such as cellular maintenance and locomotion (Wade,
Schneider, & Li, 1996). In many exercising women, chronic
energy deficiency and the metabolic adaptations that result
are thought to begin with the conscious restriction of food
intake to achieve an ideal body weight or shape (Cobb et al.,
2003; Otis, Drinkwater, Johnson, Loucks, & Wilmore, 1997).
In humans and in non-human primates, chronic energy
deficiency, in turn, results in prolonged reproductive
quiescence causing severe energy-related menstrual distur-
bances (ERMD), such as amenorrhea (De Souza &
Williams, 2004b, 2005; Williams, Helmreich, Parfitt, Cas-
ton-Balderrama, & Cameron, 2001). In exercising women
with ERMD, and in particular, amenorrhea associated with
energy deficiency, the likelihood of bone loss and stress

0195-6663/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.appet.2006.10.009
 ARTICLE IN PRESS
360 M.J. De Souza et al. / Appetite 48 (2007) 359–367
fractures is greater than that observed in exercising women
who are energy replete and have normal menstrual cycles
(De Souza & Williams, 2005; Zanker & Cooke, 2004). The
medical condition describing the interrelated problems of
disordered eating, menstrual irregularities, and bone loss
among athletes is termed the Female Athlete Triad (Otis
et al., 1997).
The prevalence of disordered eating among female
athletes has been reported to be higher than that observed
in sedentary women (Beals & Hill, 2006; Beals & Manore,
1994). Drive for thinness (DT), a subscale of the eating
disorder inventory (EDI) (Garner & Olmsted, 1991) is a
widely used and well validated psychometric self-report
measure of disordered eating attitudes about body image,
weight, and shape. DT consists of perceptual, behavioral,
and attitudinal components, is likely triggered when there
is a discrepancy between the actual and ideal body weight
which exceeds the specific idealized preference of cultural
thinness, and involves body image dissatisfaction (Sands,
2000). Elevated DT scores have been observed in exercising
women in concert with severe ERMD to include oligome-
norrhea and amenorrhea (Cobb et al., 2003; O’Connor,
Lewis, & Kirchner, 1995). Individuals with a strong DT are
typically preoccupied with their body weight and body
shape, have a fear of gaining weight, and associate their
achieved thinness with their self-esteem and self-worth
(Garner, Olmsted, Polivy, & Garfinkel, 1984; Sands, 2000).
In exercising women, disordered eating attitudes reflected
by a high DT may contribute to behavioral changes leading
to a conscious restriction of food intake, and or excessive
exercise, potentially leading to the development of the
Female Athlete Triad (Sundgot-Borgen, 1994). Interest-
ingly, differences in body weight between amenorrheic and
eumenorrheic exercising women are often not observed (De
Souza et al., 2004a; Laughlin & Yen, 1996; Kaufman et al.,
2002; Myerson et al., 1991) suggesting that endocrine and
metabolic adaptations to conserve energy and reduce
weight loss should be closely examined to better under-
stand the physiology of the Triad.
Prevention strategies targeted at decreasing the preva-
lence and negative consequences of the Triad must reliably
capture those aspects of the Triad that are seminal to its
etiology (Livingstone & Black, 2003). Because a large body
of evidence supports strong correlations between disor-
dered eating, DT and amenorrhea in female athletes, we
reasoned that these correlations might be related to the
impact of energy deficiency that can be the physiological
underpinning of prolonged reproductive suppression (De
Souza et al., 2004a; De Souza & Williams 2004b; Loucks &
Thuma, 2003). If this were true, psychometric indices may
represent a reliable ‘‘first pass’’ indicator of energy
deficiency and might be used to identify individuals at risk
for the Triad. We chose to investigate the association
between DT and adaptations to energy deficiency since this
particular subscale is commonly associated with severe
ERMD (Cobb et al., 2003). Thus, the primary purpose of
this study was to determine whether DT is an indicator of
the presence of adaptations to energy deficiency in
exercising women. We hypothesized that exercising women
with a high DT will present with physiological signs of
energy deficiency, as defined by a lower REE, and a lower
ratio of actual to predicted REE. As corroborative
measures of adaptations to energy deficiency, secondary
outcomes were fasting concentrations of key metabolic
hormones that are associated with energy homeostasis. As
a corroborative measure of eating attitudes, the three
factor eating questionnaire (TFEQ) (Stunkard & Messick,
1985), another psychometric inventory reflective of eating
attitudes, was also utilized.
Methods
Experimental design: We conducted a large observational
study to examine relationships between physical activity,
metabolism, and reproductive function. Volunteers were
followed over a 2–3 month period while repeated assess-
ments of physical activity, diet, eating attitudes, metabolic
status, and menstrual status were performed. Volunteers
were recruited on a rolling basis over three years. A total of
87 volunteers were recruited, and 52 completed the entire
study, 32 either failed screening or declined study
participation and 3 women dropped out due to time
constraints. The current study is one of the several
substudies performed using the data from this large
observational study. This study specifically explores the
relationship between DT and energy deficiency, and utilizes
data from all the volunteers from the larger study. For this
study, volunteers were retrospectively grouped according
to their exercise status, i.e., exercising or sedentary, and
according to their scores for DT obtained from the EDI.
The details of this classification scheme are outlined in the
Data Analysis section.
Volunteers: Volunteers were recruited by posters target-
ing both sedentary and physically active women for a study
on women’s health. Screening procedures included general
questionnaires on exercise, eating, menstrual cycle, and
medical health history. Eligibility criteria for the study
included: (1) aged 18–35 yr; (2) good health as determined
by a medical exam; (3) no chronic illness, including
hyperprolactinemia and thyroid disease; (4) stable men-
strual status over preceding 3 months; (5) non-smoker; (6)
not currently dieting and weight stable for the preceding 3
months, as determined by self-report; (7) not taking any
form of hormonal therapy for at least 12 months; (8) no
history or current clinical diagnosis of eating disorders and
(9) no other contraindications that would preclude
participation in the study. The study was approved by
the Ethics Review Board at the University of Toronto and
all volunteers signed an approved Informed Consent
document.
Observational time periods: If participants self-reported
that (1) they menstruated regularly, they were monitored
for 2 to 3 menstrual cycles; (2) they were oligomenorrheic
(menses at intervals of 36–100 days), they were followed
 ARTICLE IN PRESS
M.J. De Souza et al. / Appetite 48 (2007) 359–367
until their first menses or for 100 days, whichever came first
and (3) they were amenorrheic (no menses for 3 months),
they were followed for 2–3 30-day periods. Five women
were monitored for only one menstrual cycle or one 30-day
monitoring period including 3 amenorrheic women and 2
menstruating women. Menstrual cycle length and presence
or absence of menses was monitored throughout this study
via self-report. Although detailed menstrual profiles of
daily ovarian steroids were generated, these data are
beyond the scope of this paper.
Anthropometric data: Total body mass was measured to
the nearest 0.1 kg on a physician’s scale weekly throughout
the study, and the mean of these measurements is presented
(Detecto, Webb City, MO). Height was measured to the
nearest 1.0 cm at the beginning of the study period. Body
mass index (BMI) was calculated as average weekly weight
throughout the study period divided by height2 (kg/m2).
Body composition: Dual-energy X-ray absorptiometry
(DXA) was utilized to determine body composition once
during the course of the study (General Electric Lunar
Corporation, Madison, WI, enCORE 2002, version
6.50.069). The DXA scanner has a precision of o1%
coefficient of variation for body composition measure-
ments. A 28 subject precision study was performed in
premenopausal women, and the precision was 0.6% for the
total body. The division of soft tissue into fat (g) and lean
tissue (g) is based on an attenuation ratio of high-energy
and low-energy photons or R-value.
Resting energy expenditure: REE was measured during
the early follicular phase (day 2–6) of each menstrual cycle
for menstruating volunteers and during the first 6 days of
each 30-day monitoring period for oligomenorrheic and
amenorrheic volunteers. REE was determined by indirect
calorimetry using a ventilated hood system (SensorMedics
Vmax Series, Yorba Linda, CA). Room temperature (1C),
humidity (%H2O), and barometric pressure (mmHg) were
measured. Volunteers were instructed not to exercise or
ingest caffeine within 24 h, refrain from ingesting food and
alcohol within 12 h prior to testing and arrive at the lab
within 90 min after awakening. Before conducting the REE
analysis, weight (kg), height (cm) and age (yr) were
recorded, and predicted REE (pREE; kJ/day) was calcu-
lated using the Harris–Benedict equation (Harris &
Benedict, 1919) ¼ 655.0955+9.5634 (weight)+1.8495
(height)4.6756 (age). REE measurements were performed
between 0830 and 1100 h in a lit room at a comfortable
temperature setting (20–241C). After the volunteers lay
quietly for 45 min, a transparent canopy was placed over
their head. Volunteers were instructed to lie flat on their
back and remain awake during the 30-min measurement
period. Oxygen consumption (VO2; mL/min) and carbon
dioxide production (VCO2; mL/min) were measured every
20 s. To calculate REE, data for VO2 and VCO2 were only
used if steady state was attained. Steady state was achieved
when the volume of expired air, VO2, and respiratory
quotient values were not varying by more than 10%. REE
was calculated using the Weir equation (Weir, 1990): REE
361
(kcal/day) ¼ [3.94(VO2)+1.11 (VCO2)]  1.44, and then
converted to kJ. A ratio of the actual REE to predicted
REE (REE/pREE) was calculated once during each
monitoring period using the Harris–Benedict equation
(Harris & Benedict, 1919) and then averaged for the
entire study period. To further examine differences among
groups with respect to indices of energy deficiency, we
expressed REE as a ratio of actual to predicted based on
the predicted calculated using the Harris–Benedict equa-
tion (Harris & Benedict, 1919). Although there is
variability associated with pREE as estimated from
Harris–Benedict (Harris & Benedict, 1919), this variability
was expected to be distributed randomly among all three
groups.
Dietary energy intake: Dietary energy intake was
assessed from 3-day nutritional logs recorded for two
weekdays and one weekend day during each week of REE
determination. Three day recordings of food intake have
been demonstrated to provide comparable data to 7 day
records in women who may underreport their food intake,
to include lean women (Goris & Westerterp, 1999).
Dietary energy intake was measured 2–3 times in each
subject on days 2–6 of the follicular phase for the
menstruating volunteers, and on days 1–5 of a defined 30
day monitoring period for volunteers who were oligome-
norrheic and amenorrheic. Each volunteer weighed (ECKO
Kitchen Scale) or measured (using standard measuring
cups) all food and beverages consumed and was carefully
instructed how to measure and report food and beverage
items by qualified personnel. The nutrient data from the 3-
day logs were coded and analyzed for total kilocalories
using Nutritionist Pro (Version 1.3.36; First DataBank
Inc., Indianapolis, IN). Daily kilocalories consumed over
the 3-day recording period for each menstrual cycle
or monitoring period were averaged. Daily energy intake
(kJ/day) was expressed as the mean value of all menstrual
cycles or monitoring periods recorded throughout the
study.
Physical activity logs: Volunteers kept logs of their daily
physical activity and their purposeful exercise if applicable.
Heart rate, via manual palpation of an artery, was
immediately taken upon the completion of 3 min or more
of continuous physical activity and was recorded on daily
physical activity logs.
Peak aerobic capacity: VO2 peak was measured during a
progressive treadmill test to volitional exhaustion using
open-circuit spirometry on a single occasion. After a warm-
up, the VO2 peak test was initiated at a comfortable
running speed at 0.0% grade for 2 min and the grade was
increased by 2.0% every 2 min for the first 8 min, and then
increased by 1.0% for each subsequent minute. To collect
expired air, subjects breathed continuously through a Hans
Rudolph valve and corrugated plastic tubing connected to
a flow transducer that measured inspired air volumes.
Expired air samples were measured using an online Moxus
Modular VO2 System (Applied Electrochemistry Inc.,
Pittsburgh, PA).
 ARTICLE IN PRESS
362 M.J. De Souza et al. / Appetite 48 (2007) 359–367
Drive for thinness: DT was assessed as part of the entire
EDI, which was completed once during the study. The EDI
is a 91-item self-report measure of multidimensional
symptom clusters associated with eating disorders (Garner
& Olmsted, 1991). The subscales of the EDI are com-
prised of 3 subscales assessing attitudes and behaviors
concerning eating, weight, and shape (DT, Bulimia, Body
Dissatisfaction), 5 subscales assessing organizing con-
structs or psychological traits relevant to eating disorders
(Ineffectiveness, Perfectionism, Interpersonal Distrust,
Interoceptive Awareness, Maturity Fears), and 3 provi-
sional subscales (Asceticism, Impulse Regulation, Social
Insecurity).
Three factor eating questionnaire (TFEQ): The TFEQ is a
51-item questionnaire that measures three dimensions of
human eating behavior: (1) dietary cognitive restraint, (2)
disinhibition, and (3) hunger (Stunkard & Messick, 1985).
This questionnaire was administered once during the
monitoring period.
Blood sampling and storage: Blood samples were
collected between 0730 and 1000 h during the early
follicular (days 2–6) phase of the menstrual cycle for
menstruating exercising and sedentary volunteers. For
amenorrheic and oligomenorrheic volunteers, blood sam-
ples were collected during the first 6 days of each 30 day
monitoring period. All hormone measurements obtained
from repeated blood samples on a given volunteer were
averaged during data analysis. Volunteers were instructed
not to exercise or consume food within 12 h prior to
blood sampling. Antecubital blood samples were drawn
using a blood collection needle (21 gauge, 19 mm) and
blood collection tubes (Vacutainer, Franklin Lakes, NJ).
Samples were allowed to clot for 30 min at room
temperature (20–241C) and then centrifuged at 3000 rpm
for 15 min at 41C. The serum was aliquoted into 2-mL
polyethylene storage tubes and stored frozen at 801C
until analysis.
Serum hormone measurements: TT3 was analyzed using a
chemiluminescence immunoassay analyzer (Immulite, Di-
agnostic Products Corporation, Los Angeles, CA) through
competitive immunoassay. Analytical sensitivity for the TT3
assay was 0.54 nmol/L (35 ng/dL). The intraassay and
interassay coefficients of variation were 13.2% and
15.6%, respectively. Insulin was analyzed using a chemilu-
minescence immunoassay analyzer (Immulite, Diagnostic
Products Corporation, Los Angeles, CA) through immuno-
metric (sandwich) assay. Analytical sensitivity for the
insulin assay was 13.89 pmol/L (2 mIU/mL). The intraassay
and interassay coefficients of variation were 6.4% and
8.0%, respectively. Serum leptin levels were measured using
a direct sandwich enzyme-linked immunosorbent assay
(ELISA; Linco Research, Inc., St. Charles, MO). Analytical
sensitivity for the leptin assay was 0.5 mg/L (0.5 ng/mL). The
intraassay and interassay coefficients of variation were
4.6% and 6.2%, respectively. Total serum ghrelin was
measured using radioimmunoassay (RIA; Linco Research,
Inc., St. Charles, MO). The sensitivity for the total ghrelin
assay was 29.7 pmol/L (100 pg/mL). The intraassay and
interassay coefficients of variation were 6.4% and 16%,
respectively.
Data analysis: To address the relationship between DT
and energy deficiency, participants were retrospectively
grouped according to exercise status and DT score, and
categorized into one of the 3 groups: (1) Exercising high
DT group (ExHigh-DT, n ¼ 9), (2) exercising normal DT
group (ExNormal-DT n ¼ 34), and (3) sedentary normal
DT group (SedNormal-DT n ¼ 9). Since only one seden-
tary volunteer had a high DT score, a ‘‘SedHigh-DT’’
group was not included in the analyses.
Exercise status was defined a priori as ‘‘sedentary’’ when
purposeful exercise was less than 2 h per week and
‘‘exercising’’ when purposeful exercise was more than 2 h
per week. Purposeful exercise was defined as exercise that
elicited an HR greater than 55% of maximal HR for 3 min
or more as documented in exercise logs (ACSM’s Guide-
lines for Exercise Testing and Prescription, 2006; De Souza
et al., 1998).
A normal DT score was defined as less than or equal to
6; about 75% of college women have scores in this range,
with a representative mean score of 5.5 (Garner & Olmsted,
1991). DT was defined a priori as high when the score was
(1) 7 or greater which corresponds to the 73rd percentile
for college women (Garner & Olmsted, 1991) and utilized
by others to discriminate high and low/normal DT scores
(Ramacciotti et al., 2002), or (2) equal to 0 in the presence
of all other EDI subscale scores equal to or less than 2,
except for perfectionism, which was greater than 9; this
profile is indicative of a ‘‘fake’’ response style, as described
by O’Connor et al. (1995). The decision to utilize this
strategy was also made a priori since some women may
adjust their responses to fit a normative behavior profile.
In the current study, we incorporated this notion into
our classification of volunteers as high DT by including
two individuals who scored 0 on the DT subscale and
had a profile consistent with ‘‘faking’’ on the remaining
subscales.
Statistical analysis: All data sets were tested for non-
normality, homogeneity of variance, and outliers before
statistical hypothesis tests are performed. Outliers detected
were rejected; all data sets were normally distributed. Data
were expressed as mean 7 SEM. Demographic data and
training characteristics (i.e., age, height, weight, BMI, body
composition, VO2 max, age of menarche, gynecological
age) and data for all metabolic, reproductive, and
psychological parameters were compared among the
groups using an analysis of variance (ANOVA). Post hoc
tests (Least Significant Difference) were used when
main effects of ANOVA were detected. Pearson correla-
tion coefficient analyses were performed to assess associa-
tions between variables of interest. Chi-square analyses
were performed to compare menstrual category among
the groups. All data were analyzed using SPSS for
Windows (version 12.0; Chicago, IL) statistical software
package.
 ARTICLE IN PRESS
M.J. De Souza et al. / Appetite 48 (2007) 359–367 363

Results subscale of Asceticism ðp ¼ 0:017Þ were significantly higher

in the ExHigh-DT group compared to the SedNormal-DT
Demographic and anthropometric characteristics: The group only. No differences were observed between the
demographic characteristics of the volunteers are presented groups for TFEQ disinhibition and hunger scores, how-
in Table 1. As expected, the ExHigh-DT and the ever, dietary cognitive restraint scores were higher
ExNormal-DT groups had a higher VO2 max (po0.001),
total volume of purposeful and non-purposeful activity
minutes per week (po0.001), total volume of purposeful Table 2
activity that elicited a heart rate greater than 55% of Psychometric data of the sedentary and exercising women grouped by
maximal heart rate ðp ¼ 0:003Þ, and a lower ðp ¼ 0:004Þ High and Normal Drive for Thinness scores
percentage of body fat than the SedNormal-DT group. SedNormal-DT ExNormal-DT ExHigh-DT p-value
Average VO2 max for the sedentary women was considered ðn ¼ 9Þ ðn ¼ 34Þ ðn ¼ 9Þ (group
effect)
to be of ‘‘average’’ fitness, while the exercising women
exhibited VO2 max averages considered to be ‘‘above EDI-2
average’’ by ACSM classification (ACSM’s Guidelines for Drive for Thinness 1.070.7 1.470.4 11.370.6a o0.001
Bulimia 0.470.3 0.470.2 2.371.0a 0.012
Exercise Testing and Prescription, 2006). Body dissatisfaction 5.371.5 5.371.0 9.472.4 0.165
Menstrual categories: Menstrual category was deemed to Ineffectiveness 1.470.8 1.270.3 5.971.7a o0.001
Perfectionism 5.471.0 5.570.5 6.871.7 0.612
be abnormal if volunteers experienced no menses during Interpersonal distrust 2.670.9 1.670.4 3.971.3 0.080
the observation period or if menstrual cycle length was Interoceptive awareness 0.970.4 1.370.4 3.271.3 0.075
36–100 days. Menstrual category was deemed to be normal Maturity fears 4.571.8 2.270.5 3.170.9 0.229
Asceticism 1.570.3 2.570.3 3.770.7b 0.017
if the menstrual cycle intervals were between 26 and 35 Social insecurity 3.270.9 1.870.3 3.670.9 0.062
days during the observation period. Significantly more Impulse regulation 0.670.4 1.470.5 0.870.5 0.688
TFEQ
abnormal cycles (amenorrhea or oligomenorrhea) were Disinhibition 4.670.8 5.470.6 6.071.2 0.652
observed in the ExHigh-DT group compared to the other Hunger 6.470.7 6.670.5 7.071.1 0.890
groups (w2 ¼ 16:1, po0.001). Cognitive restraint 6.471.6 8.470.8 15.371.3a o0.001

Psychometric parameters: The psychometric profile data Values are mean7SEM.

of the volunteers are presented in Table 2. By study design,
DT scores were higher (po0.001) in the ExHigh-DT group
compared to the normal-DT groups. Scores on the EDI
subscales of Bulimia ðp ¼ 0:012Þ, and Ineffectiveness
(po0.001) were significantly higher in the ExHigh-DT
group compared to the normal-DT groups. Scores on the
TFEQ ¼ Three Factor Eating Questionnaire.
Exercising High Drive for Thinness group ¼ ExHigh-DT (DTX7).
Exercising Normal Drive for Thinness group ¼ ExNormal-DT (DTo7).
Sedentary Normal Drive for Thinness group ¼ SedNormal-DT (DTo7).
a
ExHigh-DT vs SedNormal-DT and ExNormal-DT; ANOVA with
LSD post hoc test.
b
ExHigh-DT vs SedNormal-DT; ANOVA with LSD post hoc test.

Table 1
Demographic characteristics of the sedentary and exercising women grouped by High and Normal Drive for Thinness scores

SedNormal-DT ExNormal-DT ExHigh-DT p

ðn ¼ 9Þ ðn ¼ 34Þ ðn ¼ 9Þ (group effect)

Age (yr) 27.972.0 23.970.7 24.071.5 0.062

Height (cm) 161.971.7 165.770.9 165.771.1 0.123
Weight (kg) 58.472.4 58.471.0 57.072.1 0.827
BMI (kg/m2) 22.770.8 21.370.3 20.870.7 0.100
Body fat (%) 31.372.5 23.171.0a 21.972.1a 0.004
VO2 peak (mL/kg.min1) 39.271.5 46.370.8a 45.071.4a o0.001
Total activity volume (min/wk) 191.3776.8 519.7736.4a 664.77118.3a o0.001
Total purposeful activity volume (min/wk) 113.2723.4 294.9726.0a 255.7765.2a 0.003
Age of menarche (yr) 12.670.3 12.870.3 12.670.5 0.871
Gynecological age (yr) 15.372.0 11.070.8 11.471.7 0.066

Values are mean7SEM.

Exercising High Drive for Thinness group ¼ ExHigh-DT (DTX7).
Exercising Normal Drive for Thinness group ¼ ExNormal-DT (DTo7).
Sedentary Normal Drive for Thinness group ¼ SedNormal-DT (DTo7).
VO2 max ¼ Maximal oxygen uptake.
BMI ¼ Body Mass Index.
 Total activity volume (min/wk) is defined as any physical activity, including purposeful and nonpurposeful activity, greater than 5 min duration.
Total purposeful activity volume (min/wk) is defined as any physical activity that elicited a heart rate greater than 55% of maximal heart rate, defined
as 220-age.
a
ExHigh-DT and ExNormal-DT vs SedNormal-DT; ANOVA with LSD post hoc test.
 ARTICLE IN PRESS
364 M.J. De Souza et al. / Appetite 48 (2007) 359–367
(po0.001) and in the clinical range of 14 or greater, as
established by Stunkard and Messick (1985) in the ExHigh-
DT group compared to the normal-DT groups. This is
consistent with previous data reported in exercising women
(McLean, Barr, & Prior, 2001). A significant positive
correlation was found between DT and dietary cognitive
restraint (r ¼ 0:602, po0.001), indicating how tightly
coupled these psychometric measures are.
Energy status and metabolic hormones: Energy balance
indices and metabolic hormones of the volunteers are
presented in Table 3 and Fig. 1. Adjusted REE, expressed
as kJ/kg FFM ðp ¼ 0:003Þ, and REE expressed as a ratio of
actual to predicted REE ðp ¼ 0:023Þ, were significantly
lower in the ExHigh-DT group compared to both the
sedentary and exercising normal-DT groups (Fig. 1). The
ExNormal-DT group also had a significantly lower REE/
FFM than the SedNormal-DT group. Additionally,
examination of the ratio of actual to predicted REE, we
found that 66% of the volunteers in the ExHigh-DT group
could be classified as ‘‘energy deficient’’. In contrast, 27%
in the SedNormal-DT and ExNormal-DT groups were
classified as energy deficient (w2 ¼ 4:940, p ¼ 0:026). Daily
caloric intake was not different ðp ¼ 0:630Þ among the
groups (Table 3).
TT3 was lower ðp ¼ 0:007Þ and ghrelin concentrations
were higher ðp ¼ 0:044Þ in the ExHigh-DT group compared
to both the sedentary and exercising normal-DT groups
(Fig. 1). Leptin concentrations were lower ðp ¼ 0:002Þ in
both exercising groups, compared to the SedNormal-DT
group, presumably attributable to the lower percentage
of body fat observed. No differences (p40.05) were
observed among the groups for insulin concentrations. A
significant negative relationship was observed between DT
scores and TT3 concentrations (r ¼ 0:356, p ¼ 0:010),
adjusted REE (kJ/kg/FFM) (r ¼ 0:325, p ¼ 0:023), and
Table 3
Bioenergetic profile data of the sedentary and exercising women grouped
by High and Normal Drive for Thinness scores
SedNormal-DT ExNormal-DT ExHigh-DT
ðn ¼ 9Þ ðn ¼ 34Þ ðn ¼ 9Þ
Energy status
REE (kJ) 53227209 5519797 50127195
Daily intake (kJ/day) 84687540 80507343 750171053
Metabolic hormones
Leptin (mg/L) 9.572.0 4.570.4a 5.571.2a
Insulin (pmol/L) 34.774.2 33.372.1 31.374.9
Values are mean7SEM.
All values are the average score for two or three measurement periods.
Exercising High Drive for Thinness group ¼ ExHigh-DT (DTX7).
Exercising Normal Drive for Thinness group ¼ ExNormal-DT (DTo7).
Sedentary Normal Drive for Thinness group ¼ SedNormal-DT (DTo7).
Resting energy expenditure (REE).
Leptin, conversion ng/mL  1 ¼ mg/L.
Insulin, conversion mIU/mL  6.945 pmol/L.
a
ExHigh-DT and ExNormal-DT vs SedNormal-DT; ANOVA with
LSD post hoc test.
the ratio of actual to predicted REE (r ¼ 0:331,
p ¼ 0:018), indicating a significant inverse relationship of
DT scores and key markers of an energy deficiency. In
addition, a positive correlation (r ¼ 0:398, p ¼ 0:004) was
observed for DT score and ghrelin concentrations, another
likely marker of a chronic energy deficiency (De Souza
et al., 2004a).
Discussion
This is the first study to evaluate whether the use of the
DT subscale, (in conjunction with the use of other EDI
scores to identify fake responders), can discriminate
individuals with signs of chronic energy deficiency. The
high DT and dietary cognitive restraint scores in the
ExHigh-DT group are consistent with a psychological
profile of an individual at risk for disordered eating
(Garner & Olmsted, 1991; Garner, Garfinkel, Rockert, &
Olmsted, 1987; McLean et al., 2001). Our findings indicate
that a clinical classification of high DT is significantly
associated with reduced REE and hormonal indicators of
compensatory adaptations to energy deficiency and there-
fore establish a link between this psychometric measure
and the physiological underpinnings of the Female Athlete
Triad. The average measured REE of the high DT group
was 86% of predicted and is consistent with the clinical use
of REE to assess metabolic status in anorexic women; that
is a reduced REE of 60–80% of pREE is often reported in
clinical models of starvation, such as anorexia nervosa,
during periods of low body weight and prior to refeeding
(Marra et al., 2002; Melchior, Rigaud, Rozen, Malon, &
Apfelbaum, 1989; Polito et al., 2000). Additionally, low
REE has been repeatedly associated with reproductive
suppression in exercising women who maintain a normal
weight (Myerson, et al., 1991; Kaufman, et al., 2002).
The percentage of individuals who would be clinically
classified as energy deficient was 66% in the ExHigh-DT
group, and 27% in the normal DT groups. This finding
establishes the clinical significance of this degree of change
in REE, and underscores the parallels between seemingly
p-value healthy exercising women and individuals with clinical
(group eating disorders. The average ratios of actual to pREE in
effect)
the ExNormal-DT and the SedNormal-DT groups were
above this 90% criterion. Metabolic hormone profiles, i.e.,
0.088 TT3 and ghrelin (De Souza et al., 2004a; De Souza &
0.630
Williams, 2004b; Laughlin & Yen, 1996) are consistent
0.002
with adaptations to energy deficiency and are thus
0.824 corroborative. Taken together, these findings underscore
the premise that subclinical disordered eating behaviors
and attitudes, as represented by a high DT, are important
etiological factors for chronic energy deficiency.
Others (Ramacciotti et al., 2002) have also used a score
of 7 to be representative of a ‘‘high’’ DT score, and have
shown that high DT is observed in exercising women. The
published normative mean for 205 college students
reported by Garner and Olmstead (1991) is 5.571.0.
O’Connor et al. (1995) reported that gymnasts had a mean
 ARTICLE IN PRESS
M.J. De Souza et al. / Appetite 48 (2007) 359–367 365

A B
0.96
160

Actual:Predicted REE
0.92
150 a
REE/FFM (kJ/kg)

140 b 0.88
a
130
0.84
120
0.8
110
= =

SedNormal-DT ExNormal-DT ExHigh-DT SedNormal-DT ExNormal-DT ExHigh-DT

Mean DT=1.0±0.7 Mean DT=1.4±0.4 MeanDT=11.3±0.6 Mean DT=1.0±0.7 Mean DT=1.4±0.4 MeanDT=11.3±0.6

C D
1.8 2350 a

2100
1.6

Ghrelin (pmol/L)
TT3 (nmol/L)

1850
a
1.4
1600

1.2
1350
= =

SedNormal-DT ExNormal-DT ExHigh-DT SedNormal-DT ExNormal-DT ExHigh-DT

Mean DT=1.0±0.7 Mean DT=1.4±0.4 MeanDT=11.3±0.6 Mean DT=1.0±0.7 Mean DT=1.4±0.4 MeanDT=11.3±0.6

Fig. 1. Data for resting energy expenditure (REE) in sedentary and exercising subjects grouped according to drive for thinness (DT) scores. Panel A is
REE adjusted for fat free mass (FFM) in sedentary and exercising subjects grouped according to DT scores. Panel B is the ratio of measured to predicted
REE in sedentary and exercising subjects grouped according to DT scores. Panels C and D are concentrations of total triiodothyronine (TT3) and ghrelin
in sedentary and exercising subjects grouped according to DT scores. a ¼ po0.05 ExHigh-DT vs SedNormal-DT and ExNormal-DT (ANOVA with
LSD). b ¼ po0.05 ExNormal-DT vs SedNormal-DT (ANOVA with LSD).

DT score of 9.070.7; a score that is above the criterion of 7
utilized in the current study, but below the mean score
observed in our ExHigh-DT group of 11.370.6. Recently,
Torstveit and Sundgot-Borgen (2005) have suggested the
use of a DT score of 15 or greater should be used for
classifying athletes as being ‘‘at risk’’ for the Female
Athlete Triad. Based on our findings, a DT score of 15 or
greater is far too high a threshold to establish and is more
indicative of clinical eating disorders, as described by
Garner and Olmsted (1991). As indicated by the current
study, a DT score of 14 or greater would result in the
failure to identify many athletes who may be energy
deficient. We suggest a lower DT score is likely more
appropriate for the identification of subclinical ‘‘at risk’’
disordered eating behaviors indicative of an energy
deficiency.
Disordered eating attitudes, like a high DT, present on a
continuum in association with conscious restriction of food
intake, as indicated by the strong association with high
dietary cognitive restraint (McLean et al., 2001; O’Connor
et al., 1995; Otis et al., 1997; Sundgot-Borgen, 1994). In the
current study, a high DT score was also strongly related to
a high score on the dietary cognitive restraint scale, which
is a stable disposition to limit food intake (Stunkard &
Messick, 1985). Exercising women in the high DT group
displayed 90–120% higher dietary cognitive restraint
scores than the Normal DT groups. Dietary cognitive
restraint was, however, not as successful at discriminating
the energy deficient women from the energy stable women.
There are many confounding factors that can impact
dietary cognitive restraint (McLean et al., 2001), making it
difficult to use these scores as an indicator of energy
deficiency. As demonstrated in this study, a high DT
coupled with high dietary cognitive restraint was related to
energy deficiency, however, high dietary cognitive restraint,
in the absence of high DT, may not necessarily reflect poor
energy status. Indeed, high dietary cognitive restraint may
be more so related to chronic dieting to prevent weight gain
than dieting to promote weight loss (Safer, Agras, Lowe, &
Bryson, 2004). Thus, DT score may be a more sensitive
psychometric variable to consider when identifying exercis-
ing women with an energy deficiency or a propensity to
become energy deficient due to the fact that not all women
that exhibit high dietary cognitive restraint scores are
successful restrainers (Lowe, 1994; Stunkard & Messick,
1985).
 ARTICLE IN PRESS
366 M.J. De Souza et al. / Appetite 48 (2007) 359–367
While this study supports a strong association between
DT and energy deficiency, it is important to note that some
women may develop energy deficiency but may not
necessarily have the characteristic restricted or subclinical
disordered eating behaviors described. Some women may
simply fail to balance energy intake and expenditure in a
manner necessary to sustain metabolic and menstrual
function independent of any subclinical or clinical eating
pathology. Inadequate food intake may be linked to as yet
undefined disturbances in peripheral or central cues of food
intake. In any case, inadequate food intake should be
considered as an etiological factor in terms of treatment of
Triad disorders, where menstrual disturbances exist with-
out other known causes in exercising women.
Our finding that a reduced REE is associated with high
DT is reinforced by other hormonal indicators of energy
deficiency. Thyroid status is a major determinant of REE
and TT3 is a classic marker of energy deficiency (Danforth
& Burger, 1984, 1989). Low TT3 syndrome is observed in
severely undernourished individuals like anorexic patients,
secondary to food restriction (Onur et al., 2005; Polito et
al., 2000). Some investigators have also speculated that low
TT3 status contributes to the energy sparing or energy
conservation effect typically observed in undernourished or
energy deficit individuals (Onur et al., 2005). Thus, in the
current study, it is likely that the low TT3 ‘‘like’’ syndrome
observed in the high DT group plays a key role in the
energy conserving reduction in REE. TT3 levels in the high
DT group were 17.7% lower than that observed in the
exercising normal DT group and 26.6% lower than that
observed in the sedentary normal DT group.
Ghrelin, an orexigenic gut related peptide, is proposed to
be a primary peripheral metabolic signal for hunger, meal
initiation, and energy homeostasis. We have previously
reported elevated fasting ghrelin levels in amenorrheic
athletes (De Souza et al., 2004a) in a manner similar to
observations of elevated ghrelin with amenorrhea that
accompanies anorexia nervosa (Tanaka et al., 2003). In this
study, ghrelin levels were significantly elevated in the
exercising women with a high DT score, indicative of an
adaptation to energy deficiency in these women, and the
propensity of the system to provide a compensatory
peripheral stimulus to increase food intake. This is the
first report that has associated perturbations in ghrelin
homeostasis with a psychometric variable, such as DT.
Thus, in addition to the metabolic responses to the
energetic challenge of these exercising women which
includes a reduction in circulating levels of TT3 and
REE, elevated ghrelin concentrations are another distin-
guishing physiological finding.
In concert with our findings of a strong relationship
between high DT and energy deficiency, we also observed a
high DT to be associated with abnormal menstrual cycles.
The clustering of these characteristics in the current study
is supportive of the premise that chronic energy deficiency
is causally related to menstrual disturbances (De Souza &
Williams, 2005). This latter finding in conjunction with
recent evidence suggesting that energy deficiency is related
to acute signs of skeletal demineralization (De Souza &
Williams, 2005) is supportive of significant physiological
interrelationships of the components of the Female Athlete
Triad, i.e., disordered eating, menstrual disturbances and
bone loss.
Future studies should be aimed at testing the efficacy of
DT to identify individuals with energy deficiency and
concomitant menstrual disturbances. A strong association
between elevations in DT and signs of energy deficiency in
exercising women with subtle menstrual disturbances like
luteal phase defects and anovulation might be particularly
useful because it might allow for an intervention prior to
the development of more severe and obvious clinical
perturbations like oligomenorrhea and amenorrhea. At
present there exists no practical means to identify these
women, and since it is unfeasible and likely cost prohibitive
to measure REE and/or a hormonal panel in large numbers
of recreational and competitive athletes, this strategy may
very well prove helpful to health practitioners and frontline
athletic personnel striving to identify at risk individuals
and provide an opportunity for early therapeutic interven-
tion. The potential usefulness of this scale is appealing, as it
can be administered in a field setting, is cost-effective, non-
invasive, and easy. Caution is warranted until studies with
larger numbers of volunteers can demonstrate the efficacy
of this tool for use with a single individual, i.e., the
demonstration of high sensitivity and specificity.
Acknowledgments
We are very grateful to the women who participated in
this study. We are also very grateful to our source of
support, the Arthur Thornton Cardiopulmonary Fund,
New Britain General Hospital, Connecticut.
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