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Annotated Bibliography

The research that I intend to propose is a new tool to estimate energy deficiency in

women. The following bibliography gives relevant evidence of variables related to and

altered by low energy availability.

De Souza, M. J., Miller, B. E., Loucks, A. B., Luciano, A. A., Pescatello, L. S., Campbell,

C. G., & Lasley, B. L. (1998). High frequency of luteal phase deficiency and anovulation

in recreational women runners: blunted elevation in follicle-stimulating hormone

observed during luteal-follicular transition. The Journal of Clinical Endocrinology &

Metabolism, 83(12), 4220-4232.

Recreational runners and sedentary women with regular menstrual cycles were

tested for hormone secretion and energy expenditure and intake. Luteal phase deficiency

(LPD) and anovulation was frequently observed in runners, both conditions showing low

progesterone excretion. In LPD, follicular phase was longer and luteal phase was shorter,

and increase of FSH secretion was lower, compared to sedentary group. Runners also had

lower E1C secretion during follicular phase. Anovulatory women had the lowest energy

intake and the greatest daily energy expenditure, therefore the lowest energy balance.

This relationship between menstrual dysfunction and low energy intake could indicate

that the variables used in this study could be part of a tool to assess energy deficiency.

De Souza, M. J., Toombs, R. J., Scheid, J. L., O'Donnell, E., West, S. L., & Williams, N.

I. (2010). High prevalence of subtle and severe menstrual disturbances in exercising

women: confirmation using daily hormone measures. Human reproduction, 25(2), 491-

503.

The prevalence of amenorrhoeic and oligomenorrheic women in exercising and

sedentary group was assessed. Exercising anovulatory, oligomenorrheic and

amenorrhoeic women tended to have lower gynecological age compared to sedentary and

exercising ovulatory women, and to exercising women with luteal phase defects. In the

sedentary group, most women were eumenorrheic and there were no anovulatory women,

whereas in the exercising group more than half of the subjects were anovulatory or had

luteal phase defects. This group also had lower progesterone excretion. By giving

evidence that exercising women are more likely to have menstrual disturbances, this study

supports the idea that assessing energy deficiency should include menstrual cycle data.

Gibbs, J. C., Nattiv, A., Barrack, M. T., Williams, N. I., Rauh, M. J., Nichols, J. F., & De

Souza, M. J. (2014). Low bone density risk is higher in exercising women with multiple

triad risk factors. Medicine and science in sports and exercise, 46(1), 167-176.

The association between Female Athlete Triad risk factors and low bone mineral

density (BMD) was investigated in exercising women. Subjects with low BMD had lower

weight, body mass index, fat mass, lean body mass and fat-free mass, had their menarche

later, and exercised more than women with normal BMD. The percentage of women with

low BMD was higher among the subjects who had more risk factors for the Triad. In

addition to a later menarche, which could indicate menstrual disturbances, this study

includes bone health as a variable related to energy deficiency.

Melin, A., Tornberg, Å. B., Skouby, S., Faber, J., Ritz, C., Sjödin, A., & Sundgot-Borgen,

J. (2014). The LEAF questionnaire: a screening tool for the identification of female

athletes at risk for the female athlete triad. British journal of sports medicine, 48(7), 540-

545.

The study presents the Low Energy Availability in Females Questionnaire (LEAF-

Q). The tool was developed to easily identify subjects with low energy availability,

reproductive disorders, and bone health, based on questions about menstrual function, use

of contraceptive methods, injuries, and gastrointestinal function. It was validated with

clinical verification of energy expenditure, energy intake, blood pressure,

hypothyroidism, reproductive function, and bone health, as well as with an eating

disorders/disordered eating questionnaire. The questionnaire presented in this study is the

tool currently used to estimate low energy availability in women, however this variable

is less accurate than energy deficiency. Therefore, analyzing this study is relevant for

understanding the LEAF-Q’s weaknesses and strengths, in order to develop a more

precise tool.

Williams, N. I., Mallinson, R. J., & De Souza, M. J. (2019). Rationale and study design

of an intervention of increased energy intake in women with exercise-associated

menstrual disturbances to improve menstrual function and bone health: The REFUEL

study. Contemporary clinical trials communications, 14, 100325.

This article presents the study design of a randomized controlled trial that

attempted to treat conditions associated with the Female Athlete Triad with increased

energy intake instead of hormonal contraceptives for 12 months. Changes in diet might

be a good alternative for women going through menstrual disturbances probably

associated with low energy availability. Bone health would likely need to be investigated

for a period longer than 12 months. The outcomes of this study can improve the

understanding of menstrual disturbances and bone health in exercising women and how

it is related to diet alone. In other words, how they are or not a direct outcome of energy

deficiency and how reversible they can be.

Strock, N. C., Koltun, K. J., Southmayd, E. A., Williams, N. I., & De Souza, M. J. (2020).

Indices of resting metabolic rate accurately reflect energy deficiency in exercising

women. International journal of sport nutrition and exercise metabolism, 30(1), 14-24.

The RMRratio was tested as a predictor of indicators of the Female Athlete Triad

and energy deficiency (ED) in women who were eumenorrheic, amenorrhoeic and with

subclinical menstrual dysfunction. Equations used were Harris-Benedict, DXA,

Cunningham-1980 and Cunningham-1991. RMRratio was correlated with TT3

concentration, and it had reliable sensitivity and specificity for ED, especially the

Cunningham-1991 and DXA. The RMRratio could be either used as a variable to validate

a tool to assess energy deficiency, or it could be mathematically improved for the same

purpose.

Strock, N. C., Koltun, K. J., Mallinson, R. J., Williams, N. I., & De Souza, M. J. (2020).

Characterizing the resting metabolic rate ratio in ovulatory exercising women over 12

months. Scandinavian journal of medicine & science in sports, 30(8), 1337-1347.

The RMRratio was tested as a predictor of TT3 longitudinally in healthy women. In

five tests throughout a year, RMRratio was consistent and showed good sensitivity and

specificity for all RMR predictive equations: Harris-Benedict, DXA, Cunningham-1980,

and Cunningham-1991. As the above-cited study, this ratio could be improved or used as

a tool. In addition, associations of the RMRratio with other energy deficiency-related

variables can be investigated to improve the efficacy in estimating energy deficiency.

Strock, N. C., De Souza, M. J., & Williams, N. I. (2020). Eating behaviours related to

psychological stress are associated with functional hypothalamic amenorrhoea in

exercising women. Journal of Sports Sciences, 38(21), 2396-2406.

Metabolic and psychological characteristics were compared between exercising

women with and without functional hypothalamic amenorrhoea (FHA). Subjects with

FHA had lower blood concentration levels of T3, T4, leptin, and PYY, and greater

cognitive restraint, drive for thinness, and need for social approval. Therefore, FHA

exercising women had evidence of greater energy deficiency, even with similar energy

availability. The physiological and psychological variables in this study, which indicate

energy deficiency, could be used to validate and to develop a tool to assess energy

deficiency.

Barrack, M., Fredericson, M., Dizon, F., Tenforde, A., Kim, B., Kraus, E., Kussman, A.,

Singh, S., & Nattiv, A. (2021). Dietary Supplement Use According to Sex and Triad Risk

Factors in Collegiate Endurance Runners. The Journal of Strength & Conditioning

Research, 35(2), 404-410.

Supplement intake was assessed in male and female collegiate runners. Most

athletes reported taking dietary supplements. Calcium and iron intake was higher in

women than in men. Calcium and vitamin D intake was associated with low bone mineral

density, and it was higher in subjects who had already had bone stress injury. Supplement

intake is easily obtained as a variable and it could be an indicator of energy deficiency

and low bone health.

De Souza, M. J., Mallinson, R. J., Strock, N. C., Koltun, K. J., Olmsted, M. P., Ricker, E.

A., Scheid, J. L., Allaway, H. C., Mallinson, D. J., Don, P. K., & Williams, N. I. (2021).

Randomised controlled trial of the effects of increased energy intake on menstrual

recovery in exercising women with menstrual disturbances: the ‘REFUEL’ study. Human

Reproduction, 36(8), 2285-2297.

This study showed some of the results of the randomized controlled trial that was

referred to above (Williams et al., 2019). Oligomenorrhoeic and amenorrhoeic women in

the study group (i.e. who were having increased energy intake) were more likely to

experience menses than the control group for the 12 months of study. In addition, 64% of

the study group had their menstrual function improved, which was observed in 19% of

control group. The results show the relevance of understanding and estimating energy

deficiency, which can lead to menstrual dysfunction, and which can probably be treated

without the prescription of hormones.