COLLEGE OF PUBLIC HEALTH AND HUMAN SCIENCES
REMEDY: “Reversing menstrual dysfunction”: Examining differences in
energy density in amenorrheic (AM) and eumenorrheic (EU) active women.
Authors: W.A. Lay; T.M. Hand, RD; W.M. Sweat, MS, RD; M.M. Manore, PhD, RD, CSSD
Introduction
It is estimated that menstrual dysfunction, including AM, affects anywhere from
6-79% of active women1. AM is defined as the absence of a menstrual cycle
lasting more than three months2. Secondary AM occurs after menarche, while
primary AM is the delay of menarche until after the age of 15y2. Menstrual
dysfunction can negatively impact health by reducing the achievement of peak
bone mineral density (BMD) or increasing the loss of BMD5. Energy
imbalance, due to insufficient energy intake to fuel high levels of exercise
energy expenditure, is hypothesized as one of the primary contributors to AM in
athletic women3. On contributor to lower energy intakes in active women with
menstrual dysfunction may be due to the consumption of low-energy dense
foods4.
Energy density is a ratio of the energy (kcals) in a food and its weight
(g)6. A low energy dense diet is often associated with a lower energy intake and
a higher quality diet7. This type of diet is high in fruits and vegetables, low-fat
dairy, and whole grains, which can be filling due to the volume of food
consumed. A low energy dense diet is recommended for weight loss or
maintenance due to the satiety factor of the volume of food, while being low in
overall calories. Research has found that participants consume more energy
when provided with energy dense food in a lab setting where ad libitum food is
available for consumption6. However, for active women with high-energy
needs, a low energy dense diet may not provide enough energy to fuel all their
energy needs, thus, leading to AM.
The purpose of this research was to measure the energy density of the
diets of AM active women before and after a 6-month intervention designed to
restore menstrual dysfunction and this to the diets of EU active controls. It was
hypothesized that active AM athletes would have diets lower in energy density
vs. active EU controls. We also hypothesized that the 6-month intervention,
designed to restore menstrual function, would increase dietary energy density
from pre-intervention levels. Macronutrient and micronutrient (calcium, iron,
folate, vitamin B6, and vitamin B12) intakes of these women were also
measured.
Study Design/Methods Used
This study examined the diet records of active women from the REMEDY:
Reversing Menstrual Dysfunction Study8. We calculated energy density for
AM (pre and post 6-month intervention) and EU active women (baseline
only). The REMEDY study examined the effects of an energy replacement
beverage (Gatorade Nutrition Shake; energy density 1.1 kcal/g) on reversing
menstrual dysfunction in the AM women. This shake included an additional
360 kcal, 54 g of carbohydrate, 20 g of protein and 8 g of fat. Seven-day
weighed food records were collected before (pre) and after (post) the 6month intervention (AM women) and at baseline for the EU women. Diets
were analyzed for energy and nutrient intakes with the software program
Food Processor.
Calculating the energy density of a diet can be done with or without
calorically dense beverages. The method used in this study included only
food and liquid meal-replacement beverages as determined by Ledikwe and
colleagues (2005). This method excludes all non-caloric beverages, such as
water, diet sodas and most caloric beverages such as alcohol, juice, and milk.
Beverages are excluded because they may show a disproportionately low
energy density that may not be reflective of the individual’s actual diet6.
Liquid meal replacement beverages are included in this method of calculating
energy density because they can be as satiating and have a macronutrient
composition similar to whole food6.
Energy density was calculated from the 7-day weighed diet records of the AM
active women pre- and post-intervention and the EU active women (baseline).
The energy replacement beverage (82 g/d) was included in the calculation of the
post-intervention AM diets. The number of servings of fruits, vegetables and low
fat or fat-free dairy was determined according to the USDA’s MyPlate
definitions of serving sizes.
Table 2. Diet Composition and Energy Density
Fruits &
Vegetables
Low-fat/fatfree dairy
Energy from
Beverages
Energy
Density
Results
For the AM group, the energy density of the diet did not change significantly
due to the intervention. Energy density at baseline (pre) was 1.60 kcal/g, while
energy density was 1.54 kcal/g at post-intervention. The energy density diet of
the EU group was 1.84 kcal/g. For both groups, mean energy density could be
categorized as medium (Energy Density: 1.5-4.0 kcal/g). Mean energy intake
for the groups is given in Table 1. The intervention increased mean energy
intake in the AM women from 2101 kcal/d to 2451 kcal/d, but this increase was
not significantly different. The intervention added an additional 360 kcal/d to
the diets of the AM women. For the EU women, mean energy intake was 2309
kcal/d, which was higher than the AM women at baseline, but not significantly
different. Mean protein intake for the AM group increased from 1.3 g/kg at preintervention to 1.7 g/kg at post-intervention, with the addition of the nutrition
shake that contained 20 g of protein/d. The mean protein intake in the EU group
was 1.3 g/kg, which was similar to that the AM group at baseline. In Table 1,
carbohydrate (g/kg) was similar for the AM group at pre and post and the EU
group. Fat intake was the lowest at baseline in the pre-AM women (1.2g/kg),
but similar between the AM group at post (1.4 g/kg) and the EU (1.4 g/kg)
women. Fiber was the highest in the AM group at pre (13 g/1000 kcal).
Pre AM
Post AM
EM
2.4(±2.0)
2.3(±1.6)
2.8(±1.5)
1.1(±0.8)
1.2(±0.5)
1.4(±0.7)
286(±143)
270(±202)
189(±876)
1.6(±0.2)
1.4(±0.2)
1.8(±0.3)
serv/d
serv/d
Total Energy
kcals/d
Protein
g/kg
1.3(±0.2)
1.7(±0.5)
1.33(±0.3)
15.5%(±8.2)
17.1%(±6.5)
14.0%(±3.5)
81(±16.0)
4.6(±1.4)
105(±24.4)
5.0(±0.9)
89(±20.7)
4.6(±1.0)
% energy
52.9(±24.1) 50.98%(±18.5)
52.62%(±6.1)
g/day
278(±64.1)
312(±39.4)
304(±68.8)
1.2(±0.3)
31.7%(±12.1)
1.4(±0.5)
32.5%(±12.9)
1.4(±0.4)
36.1%(±5.9)
74.0(±15.8)
88.4(±29.6)
92.7(±26.8)
0.2(±0.2)
3.3%(±0.04)
0.2(±0.2)
2.8%(±0.04)
0.1(±0.2)
1.7%(±0.02)
11.2(±13.8)
10.6(±14.4)
6.5(±9.5)
% energy
g/day
Carbohydrate g/kg
Fat
g/kg
% energy
g/d
Alcohol
g/kg
% energy
g/d
Range: 1.522.54 kcal/g
kcal/d
kcal/g
Range: 1.251.89 kcal/g
Energy density is a ratio of the energy in kilocalories to the weight in grams. The calculation included all
food and liquid meal replacement type beverages. There were no differences in energy density between
groups. Serv/d = Servings/day
Demographics
Description
v
Eumen (n=10)
0-mos
Mean (SD)
Amen (n=8)
0-mos
6-mos
Age (y)
23.1 (4.3)
22.6 (3.3)
N/A
Age at Menarche (y)
12.7 (1.3)
13.5 (2.0)
N/A
Weight (kg)
66.8 (9.3)
62.4 (7.8)
64.0 (8.0)
Lean Body Mass (kg)
48.5 (4.7)
46.2 (4.4)
46.1 (4.7)
Fat Free Mass (kg)
51.0 (5.0)
48.5 (4.6)
48.4 (4.8)
Body Mass Index (kg/m2)
23.2 (2.8)
22.3 (2.5)
22.9 (2.5)
Body Fat (%)
23.2 (4.4)
22.0 (4.7)
24.1 (3.9)
Exercise >4.0 METs (h/wk)
7.4 (3.6)
7.4 (3.2)
7.1 (3.4)
Table 4. Examples of Very Low, Low-, Medium-, and HighEnergy-Dense Foods
N/A
Summary/Conclusion
In conclusion, active women with amenorrhea consumed diets lower in energy
density compared to their EU counterparts, but these differences were not
significantly different. Both groups consumed energy intakes at the low end of
the ‘medium’ energy density food category (1.5-4.0 kcal/g). It has been
hypothesized that AM women may consume diets lower in energy density,
which may contribute to their lower energy intakes4. We did not find this to be
true. At post-intervention, the diets of the AM women did not increase, which
may have been due to the increased satiety from the nutrition shake consumed
daily in the intervention. It may be necessary to recommend that active women
with menstrual dysfunction consume a more energy dense diet to fuel their
high-energy expenditure. This may decrease their risk for developing
amenorrhea and its negative health effects
N/A
N/A
N/A
References
1.
Fiber
g/1000kcal
g/d
13.0(±3.2)
27.8(±10.3)
10.7(±4.1)
25.1(±8.6)
12.1(±11.4)
2.
28.6(±3.3)
Calcium
mg/d
2313(±581)
1423(±499)
1210(±385)
1000 mg
3.
4.
Magnesium
mg/d
243(±109)
286(±78)
364(±194)
310 mg
5.
Iron
mg/d
29(±14)
21(±6)
23(±9)
18 mg
6.
Folate
Vitamin B6
mcg/d
mg/d
517(±467)
3.4(±2.8)
404(±234)
16.4(±40.1)
449(±207)
3.4(±2.3)
400 mcg
1.3 mg
7.
Vitamin B12
mcg/d
13.3(±25.0)
6.2(±3.7)
8.0(±5.2
2.4 mcg
316(±308)
303(±296)
385(±314)
600 IU
Vitamin D
IU
% en = % of energy
Range: 1.271.82 kcal/g
Table 3. Participant Demographics (mean ±SD)
Table 1. Energy and Nutrient Information
Pre AM
Post AM
EM
RDA/DRI
2101(±309)
2451(±483)
2309(±472)
N/A
Figure 1. Energy Density of Amenorrheic active women at
Pre- and Post-Intervention and Eumenorrheic Active
Women at baseline (pre)
8.
Adapted from: Sweat, W., Manore, M. (2012). Low Energy-Dense Diets: Can you really eat more
and lose weight? ACSM Health & Fitness Journal, 16, 1-7.
9.
10.
Beals KA, Manore MM. Disorders of the female athlete triad among collegiate athletes. Internation Journal of Sport
Nutrition and Exercise Metabolism. 2002; 12: 281-293.
Nattiy A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. Position Stand: The Female Athlete Triad.
American College of Sports Medicine. 2007.
Manore MM. Dietary recommendations and athletic menstrual dysfunction. Sports Med. 2002; 32:887-901.
De Souza MJ, Maguire MS, Maresh CM, Kraemer WJ, Rubin KR, Loucks AB. Adrenal activation and the prolactin response
to exercise in eumenorrheic and amenorrheic runners. Journal of Applied Physiology. 1991; 70: 2378-2387.
Drinkwater BL, Nilson K, Chesnut CH, et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med.
1984; 311: 277-81.
Ledikwe JH, Blanck HM, Khan LK, Serdula MK, Seymour JD, Tohill BC, Rolls BJ. Dietary energy density determined by
eight calculation methods in a nationally representative United States population. J. Nutr. 2005; 135: 273-278.
Ledikwe JH, Blanck HM, Khan LK, Serdula MK, Seymour JD, Tohill BC, Rolls BJ. Low-energy-density diets are associated
with high diet quality in adults in the United States. J Am Diet Assoc. 2006; 106:1172-1180.
Kam LC. Reversing Menstrual Dysfunction (REMEDY): The impact of menstrual status on musculoskeletal and hormonal
health. Corvallis, OR: Oregon State University; 2011.
Institute of Medicine, Food and Nutrition Board. Dietary Reference Intakes for Micronutrients. Washington, DC: National
Academy Press, 2010.
Sweat, W., Manore, M. (2012). Low Energy-Dense Diets: Can you really eat more and lose weight? ACSM Health & Fitness
Journal, 16, 1-7.
Demographics
Description
Age (y)
Age at Menarche
(y)
Weight (kg)
Lean Body Mass
(kg)
Fat Free Mass (kg)
Body Mass Index
(kg/m2)
Body Fat (%)
Exercise >4.0
METs (h/wk)
Mean (SD)
Eumen (n=10)
Amen (n=8) Pre AM
Fruits & Vegetables
serv/d
2.4(±2.0)
0-mos
0-mos
6-mos
Low-fat/fat-free dairy
serv/d
1.1(±0.8)
23.1
(4.3)
(3.3)
N/A 286(±143)
Energy
from Beverages 22.6
kcal/d
Energy Density
kcal/g
1.6(±0.2)
12.7 (1.3)
66.8 (9.3)
13.5 (2.0)
62.4 (7.8)
N/A
64.0 (8.0)
48.5 (4.7)
51.0 (5.0)
46.2 (4.4)
48.5 (4.6)
46.1 (4.7)
48.4 (4.8)
23.2 (2.8)
23.2 (4.4)
22.3 (2.5)
22.0 (4.7)
22.9 (2.5)
24.1 (3.9)
7.4 (3.6)
7.4 (3.2)
7.1 (3.4)
Post AM
2.3(±1.6)
1.2(±0.5)
270(±202)
1.4(±0.2)
EM
2.8(±1.5)
1.4(±0.7)
189(±876)
1.8(±0.3)
v
Pre AM
Total Energy
Protein
Carbohydrate
Fat
Alcohol
Fiber
Calcium
Magnesium
Iron
Folate
Vitamin B6
Vitamin B12
Vitamin D
kcals/d
g/kg
% energy
g/day
g/kg
% energy
g/day
g/kg
% energy
g/d
g/kg
% energy
g/d
g/1000kcal
g/d
mg/d
mg/d
mg/d
mcg/d
mg/d
mcg/d
IU
Post AM
2101(±309)
1.3(±0.2)
15.5%(±8.2)
81(±16.0)
4.6(±1.4)
52.9(±24.1)
278(±64.1)
1.2(±0.3)
31.7%(±12.1)
74.0(±15.8)
0.2(±0.2)
3.3%(±0.04)
11.2(±13.8)
13.0(±3.2)
27.8(±10.3)
2313(±581)
243(±109)
29(±14)
517(±467)
3.4(±2.8)
13.3(±25.0)
316(±308)
EM
2451(±483)
1.7(±0.5)
17.1%(±6.5)
105(±24.4)
5.0(±0.9)
50.98%(±18.5)
312(±39.4)
1.4(±0.5)
32.5%(±12.9)
88.4(±29.6)
0.2(±0.2)
2.8%(±0.04)
10.6(±14.4)
10.7(±4.1)
25.1(±8.6)
1423(±499)
286(±78)
21(±6)
404(±234)
16.4(±40.1)
6.2(±3.7)
303(±296)
v
RDA/DRI
2309(±472)
1.33(±0.3)
14.0%(±3.5)
89(±20.7)
4.6(±1.0)
52.62%(±6.1)
304(±68.8)
1.4(±0.4)
36.1%(±5.9)
92.7(±26.8)
0.1(±0.2)
1.7%(±0.02)
6.5(±9.5)
12.1(±11.4)
28.6(±3.3)
1210(±385)
364(±194)
23(±9)
449(±207)
3.4(±2.3)
8.0(±5.2
385(±314)
N/A
N/A
N/A
N/A
N/A
1000 mg
310 mg
18 mg
400 mcg
1.3 mg
2.4 mcg
600 IU