The Impact of Nutritional Intervention on Menstrual Dysfunction in Female Athletes: a Systematic Review
Menstrual function is strongly affected by nutritional status and energy availability in female athletes, and impaired menstrual function can impact bone mineral density. Nutritional interventions have been proposed to mitigate menstrual dysfunction. The purpose of this systematic review was to assess the ability of nutritional interventions, directed at improving energy availability, to restore normal menstrual status in female athletes. PubMed, Cinahl, and SportDiscus databases were comprehensively searched. Included studies had to investigate the impact of increasing energy availability in female athletes through a nutritional intervention. The primary outcome measure of interest was menstrual status. Included studies were reviewed for methodological rigor using the American Academy of Dietetics Quality Criteria Checklist. Five studies met the inclusion criteria. Of the athletes who completed the interventions in the studies, 0–100% resumed normal menses. For those that improved, the mean length of time for return to menses ranged from 2.63 to 15.6 months. The length of the interventions (3–9 months), mean ages of the participants (17–1-22.6 years), and particular dietary intervention(s) (counseling, education, and nutritional supplementation) varied between the studies. Nutritional interventions may restore normal menses in some female athletes. Educational strategies targeted at improved eating and understanding the energy demands of sport, as well as weekly interaction with athletes should be considered.
KeywordsFemale athlete triad syndrome Amenorrhea Nutrition Systematic review Energy availability
Over three million high school females and 200,000 collegiate females participate in sports in the USA . Thus, the female athlete triad (the triad) has continued to receive attention in recent years. The triad is defined as the inter-relationship among energy availability (EA), menstrual function, and bone mineral density [2, 3]. A systematic review including studies from 12 different countries reported the prevalence of all three components in female high school, collegiate, and elite athletes to be between 0 and 16%. The prevalence of two components was 3 to 27%, and the prevalence of any single component was 16 to 60% . Each component condition can occur on a spectrum from normal function to dysfunction, with EA thought to be at the crux of the problem [1, 2, 3, 5, 6].
EA is calculated by taking the dietary energy intake (in kilocalories) and subtracting the energy (in kilocalories) expended during exercise, normalized to fat-free body mass [3, 7, 8]. The result, known as EA, is the amount of energy that remains for performance of other body functions. Low EA may be intentional through restricted intake as seen in an eating disorder or varied forms of disordered eating, or unintentional when an athlete’s energy demands exceed her caloric intake, resulting in impaired health as the energy required for basic physiological functions of the body is not available .
One of the physiological functions low EA may impact is menstruation. Women over the age of 15 are expected to have normal menses that occurs every 28 ± 7 days . This is considered “normal menses,” or eumenorrhea. Menstrual dysfunction incorporates a spectrum of disorders from oligomenorrhea (menstrual cycle greater than 35 days) to amenorrhea (the absence of menstruation for greater than 3 months) . Amenorrhea after the onset of menses (menarche) is referred to as secondary amenorrhea. Primary amenorrhea refers to the delay of menarche until after the age of 15 [3, 7, 8].
Menstrual dysfunction may contribute to decreased bone density . Low bone mineral density in female athletes is defined by the American College of Sports Medicine (ACSM) as a bone mineral density (BMD) Z-score between − 1.0 and − 2.0 along with prior stress fractures or another risk factor such as nutritional deficiency or hypoestrogenism; while osteoporosis is defined as BMD Z-score below − 2.0 . Menstrual dysfunction has been found to be a significant predictor of stress fractures in cross-country runners [3, 9]. Low energy availability and menstrual dysfunction combined may compromise bone health by suppressing bone formation and upregulating bone resorption which can lead to low bone mass, structural bone changes, and unfavorable adaptations to bone geometry . In a study of young oligoamenorrheic athletes and eumenorrheic athletes, Ackerman et al. found that total hip BMD was 8% lower and cross-sectional area of the femoral neck, trochanter, and femoral shaft were 9, 15, and 15% lower in oligoamenorrheic athletes compared to eumenorrheic athletes . Menstrual dysfunction has been found to be a significant predictor of stress fractures in cross-country runners . There is a link between weight restoration, resumption of menses, and recovery of bone mass. Southmayd et al. reported on a study by Karen Miller on women with anorexia nervosa which found that resumption of menstrual function predicted an increase in lumbar spine bone mineral density and weight gain predicted an increase in hip bone mineral density .
Energy deficiency or low EA has been suggested to be the main contributing factor to menstrual dysfunction occurring in athletes with the triad [1, 2, 3, 6]. Due to the focus on energy deficiency in triad-related investigations conducted only with female athletes, the International Olympic Committee proposed the concept of Relative Energy Deficit in Sport (RED-S) . RED-S is described as a syndrome resulting from energy deficit that impacts many physiological functions (metabolic rate, menstrual function, bone health, immunity, and protein synthesis), cardiovascular health, and psychological health in both female and male athletes . Thus, RED-S may be a more comprehensive way to describe the multitude of problems that can potentially occur from a lack of available energy.
Regardless of whether the triad or RED-S is used to describe this spectrum of health problems, energy deficit can clearly be a problem in athletes and can be related to menstrual dysfunction. In a study of high school female athletes, 70% of whom were endurance runners, 30% experienced menstrual dysfunction . Those that were at less than 85% of their ideal body weight or had a low body mass index (BMI) (less than 18.5 kg/m2) were four times as likely to report menstrual dysfunction . Several theories exist regarding the relationship between energy availability and menstrual dysfunction [7, 15]; however, it is beyond the focus of this systematic review to discuss these mechanisms.
Authors of clinical commentaries and review articles suggest that the first step in treatment of the triad and menstrual dysfunction is to restore energy balance through modification of diet and exercise [2, 3, 5, 8, 13, 16]. Restoration of menses has been linked to recovery of bone mass . Yet, to date, we know of no systematic reviews that have addressed the impact of dietary changes or nutritional interventions on menstrual dysfunction. Thus, the purpose of this systematic review was to assess the ability of nutritional interventions, directed at improving energy availability, to restore normal menstrual status in female athletes.
A Preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) compliant systematic review was performed . The database search took place on January 9, 2018, and included PubMed, CINAHL Plus with full text, and SportDiscus with full text. Search terms included the following: athlete* OR sport* AND menst* OR amenorrh* OR oligomenorrh* AND nutrition OR diet* OR eat* OR energy OR food. A research librarian assisted in development of the search terms, and a hand search was performed to determine whether any additional relevant publications existed.
No systematic reviews on this topic were found. There were no date restrictions on the search. Only studies published in English were reviewed.
All studies had to include athletes, competitive or non-competitive (i.e., some were dancers and did not compete, rather were performing athletes), as defined by each individual study. Additionally, studies had to investigate the impact of increasing energy availability through a nutritional intervention. Only peer-reviewed studies that were randomized controlled, quasi-experimental, or cohort studies with pre-post testing were included. The primary outcome measure of interest was menstrual status. Secondary outcomes included weight gain, changes in body composition or body mass index, and changes in hormonal status.
Evidence level overview 
Evidence level criteria
Systematic review of randomized trials
Randomized trial or observational study with dramatic effect
Non-randomized controlled cohort/follow-up study
Case series, case-control, or historically controlled studies
Methodological rigor of the studies, or risk of bias, was evaluated using criteria adapted from the Quality Criteria Checklist for Primary Research from the Academy of Nutrition and Dietetics . With this tool, an overall negative, neutral, or positive ranking is given based on criteria met. One of the 10 questions was eliminated for this systematic review as none of the included studies were randomized controlled studies. Two authors independently ranked the articles to minimize bias.
Data was extracted and placed in a table by the lead author and reviewed for accuracy by the secondary authors. Data extracted included the following: study design, sample size, age range or mean age, sport, intervention type and duration, outcome measure(s), and results.
Description of Studies
ADA Rigor Score
Relevant outcome measures
Length of study
Arends et al. 
Retrospective chart review
n = 51 female collegiate DI athletes, various sports (373 charts reviewed); avg. age not reported
Counseling by physician and sport dietitian; individualized plan to ↑ EA. Most common was ↑ kcal 250/350 per day
Self-reported menstrual status; lab test to rule out other causes
n = 51; 17.6% resumed menses.
Avg. time to return, 15.6 ± 2.6 months
Greater weight gain in those who resumed menses, 5.3 ± 1.1 kg vs. 1.3 ± 1.1 kg
n = 12 endurance trained female athletes; avg. age 22.6 ± 3.3 years
Dietary supplement (360 kcal/day); weekly meetings with researchers to ensure compliance and discuss issues
Self-reported menstrual status; ovulation status by Clearblue Easy®; blood hormone levels
n = 8 (4 dropouts); all remaining 8 resumed menses; 7/8 ovulating: mean = 2.63 mo.
LH 5.6 ± 4.1 at start, increased to 15.3 ± 16.3 after interventions (significance not reported)
Weight gain, 1.64 ± 0.2 kg
Lagowska, Kapczuk, Friebe et al. 
n = 45 female “professional” athletes; avg. age 18.1 ± 2.6 years
Education on health consequences of dietary deficiencies and individualized diet; dietary counseling by dietitian
Self-reported menstrual status and blood hormone levels
n = 31 (14 dropouts); no change in menstrual status.
↑ energy intake of 234 kcal/day; no significant change in BMI or body comp.
LH (p = 0.009) and LH to FSH ratio (p = 0.001) significantly higher after 3 months.
Positive correlation between EA and LH concentration (r = 0.26, p < 0.05)
Lagowska, Kapczuk, Jeszka 
n = 72 female athletes (45), dancers (27); avg. age of dancers 17.1 ± 0.9 years; avg. age of athletes 18.1 ± 2.6 years
Education on health consequences of dietary deficiencies and individualized diet; dietary counseling by dietitian
Self-reported menstrual status and blood hormone levels
N = 55 (20 dropouts); 10 resumed normal menses: 3 dancers, 7 athletes.
Dancers ↑ BW and BMI after 6 months, no change in BW or BMI in athletes.
LH concentration significantly higher after 9 months (dancers, p = 0.026; athletes, p = 0.0001). LH to FSH ratio improved in athletes only (p = 0.033)
The included studies spanned multiple types of athletes with variable detail reported regarding what specific sports the athletes participated in, and the individual demands of the athletes. A total of 145 female athletes were considered in the five articles. The participants in the studies were chosen solely based on having menstrual dysfunction; however, the length of time menstrual dysfunction was present was not specified. Athletes taking birth control were excluded in all of the studies. In three out of the four studies, athletes with diagnosed eating disorders were excluded [20, 21, 23, 24]. In the fourth study, disordered eating was reported but presence or absence of eating disorders was not addressed .
Study Design and Outcomes
The interventions intended to impact EA varied widely between studies and included counseling [22, 23, 24], weekly meetings , and educational strategies [23, 24]. All four studies used various nutritional interventions including the use of dietary supplements  and individualized eating plans [22, 23, 24] in order to increase energy intake. Similarly, outcome measures used to assess menstrual function also varied widely and included self-report [21, 22, 23, 24], lab tests  or blood hormone levels [21, 23, 24], and ovulation status detectors . Due to the widely variant interventions and outcomes, studies will be discussed individually.
Only one study  was retrospective in nature. Covering a 5-year time span, 373 medical charts from Division I female athletes were reviewed. Fifty-one athletes were identified as having menstrual dysfunction, of whom 23.5% had disordered eating. Non-pharmacological treatment was implemented with all of the athletes. Physician counseling stressed increasing EA, and a sports dietician assessed individual energy needs and used educational strategies to increase EA. Athletes who needed to increase their EA increased caloric intake by 250–350 kcal/day. Nine of the 51 athletes resumed menses with an average time to resumption of menses of 15.6 ± 2.6 months. Those who resumed menses had a significant increase in body weight (5.5 ± 1.1 kg, p = 0.02) and BMI (1.9 ± 0.4 kg/m2, p = 0.02) compared to those who did not resume menses . No significant difference in resumption of menses was identified based on disordered eating status.
Two studies [23, 24] focused on increasing energy intake 20–30% per month until energy balance was neutral and energy availability > 40 kcal/kg FFM/day was obtained. Recommended diets ranged from 2500 to 3500 kcal per day. Additionally, education on the health consequences of nutritional deficiencies and tips for food preparation, shopping, and dining out was emphasized. The first study by Lagowska et al.  recruited 45 female athletes (mean age 18.1 years) from club sports; 31 athletes completed the study over a 3-month period. No changes were identified in menstrual status over 3 months. However, luteinizing hormone (LH) and LH to follicle stimulating hormone (FSH) ratio did improve significantly, by means of 41.55 ml U/ml and 0.12 respectively (p = 0.009 and p = 0.001) . In the second study by Lagowska et al. , 27 ballet dancers (mean age 17.1 years) were added to the 31 athletes who completed the first study by Lagowska et al. . Twenty-one dancers completed the long-term study. The dancers, who started with lower EA, had significant increases in body weight and BMI at the 6-month assessment; no changes in body weight or BMI occurred in the athletes . However, at the completion of the 9-month study, seven club sport athletes and three dancers resumed normal menses .
In the study by Cialdella-Kam et al.  and Guebels et al. , 12 endurance athletes began the study, and eight athletes completed the 6-month study. Athletes were required to drink a daily dietary supplement equivalent to 360 kcal (Gatorade nutrition drink: 54-g carbohydrates, 20-g protein, and 8-g fat) and meet weekly with the researchers to discuss compliance and any other issues. Seventy-five percent (6/8) of the subjects with exercise-related menstrual dysfunction gained weight, and trends for increased mean body weight (1.6 ± 2.0 kg), body fat (2.1 ± 2.1%), and BMI (0.6 ± 0.7 kg/m2) were observed over the 6-month study period (p > 0.11). All eight participants resumed normal menses after a mean of 2.6 months (range 1 to 7 months) .
In summary, of the athletes who completed the interventions in the studies, 0–100% resumed normal menses. If the short-term (3 months) results from Lagowska et al.  are not included, the range of return to menstruation improves to 17–100%. The mean length of time for return to menses ranged from 2.6  to 15.6 months . The length of the studies, age of the participants, and particular dietary and educational intervention varied from study to study.
The purpose of this systematic review was to assess the effectiveness of nutritional interventions directed at improving energy availability in restoring normal menstrual status in female athletes. All but one study of 3-month duration  (operationally defined as a short-term intervention) reported demonstrated improvement in menstrual status in some athletes; however, there are many considerations for interpreting this evidence based on the widely variant study methodology.
Effects of the Addition of a Nutritional Supplement on Return to Menses
The only study [20, 21] that added a standard daily nutritional supplement (360 kcal) found that the eight athletes who did complete the protocol all resumed normal menses within the 6-month time frame. The benefit of the supplement is the consistent calories it provides. However, comparison to the results of other studies is difficult because the average age of the athletes in this study [20, 21] was 22.6 years of age. This mean age must be contrasted with the athletes and dancers in the Lagowska et al. studies [23, 24] who were reported to have an average age of 18.1 and 17.1 years respectively, and the athletes in the Arends et al.  study who were reported as “college-aged” which likely ranged from 18 to 22 years of age. Furthermore, the older athletes that received the nutritional supplement started with a higher BMI than the groups of younger athletes [20, 21]. Additionally, these older athletes only had to average greater than 7 h per week of exercise, while the dancers in the study by Lagowska et al.  averaged over 4 h per day of exercise. Thus, the energy demands of the athlete may play a role in the length of time needed to resume menses. Also, a 22-year-old athlete may be more emotionally mature than a 17-year-old athlete and demonstrate greater understanding of the health consequences associated with menstrual dysfunction, thereby making better decisions.
All studies included some type of educational intervention, ranging from individualized counseling to general information regarding health consequences of dietary deficiencies. Only the study by Cialdella-Kam et al./Guebels et al. [20, 21] included methodology reporting the use of weekly meetings with the athletes, which may have encouraged compliance. The optimal way to achieve changes in dietary behavior has not yet been determined; however, Abood, Black, and Birnbaum  reported positive changes in collegiate soccer players’ eating habits by focusing education on self-efficacy and promoting confidence. Thus, discussions that go beyond provision of basic factual knowledge and include individualized information on how to achieve change may be beneficial.
Three of the included studies had dropout rates of 28–33% [20, 21, 23, 24], and athletes in two case reports  experienced a period of non-compliance to nutritional interventions prior to resuming menses. This demonstrates the difficulty of helping athletes’ “buy in” to the importance of nutrition and suggests the need for a supportive team approach to treatment to improve compliance. A cohesive and skilled team is essential for re-establishing balance among systems [27, 28] and establishing trust with the athlete. This team may include a physician, registered dietitian, mental health expert [5, 7, 8], physical therapist [5, 8, 28], athletic trainer, and coach .
Time frame Return of Menses Following Nutritional Interventions
The time frame needed to resume menses in athletic females also remains somewhat unknown. Although the older endurance athletes resumed menses in an average of under 3 months [20, 21], others showed no improvement in menstrual status in a 3-month time span  In fact, in the 5-year retrospective study, the average length of time to resume menses was reported to be 15.6 months . Arends et al.  suggest that there may be multiple factors influencing the return of menses including genetics, psychology, neuroendocrine status, metabolic profile, and the duration of menstrual dysfunction. Of note, the duration of menstrual dysfunction in the athletes included in these studies was not reported; thus, the impact of sustained loss of menses on menstrual return cannot be determined.
Meeting the Nutritional Demands of Total Energy Expenditure for Return to Menses
Based on the results of the studies in this systematic review, compliance with nutritional intervention, type of intervention, energy expenditure, and weight gain also may be factors. With regard to energy expenditure and rest, a case series  and a case report  both included a day of rest in addition to a nutritional supplement as part of the intervention. Thus, control of energy expenditure also may play a role in resuming menses as it affects energy balance. However, energy expenditure was not a reported part of intervention in the studies contained in this systematic review.
Despite the varying results, improvements in dietary intake do appear to have the potential to increase hormone levels and allow athletes to resume menses. Energy availability is difficult to measure and provides only a short-term picture of the overall nutritional status of an athlete . Conversely, change in body weight (and/or BMI) provides a broader, potentially longer-term representation of alterations in energy intake and EA. In the study by Arends et al. , those who gained 5 lb or more were twice as likely to resume normal menses. Additionally, the endurance athletes in the study by Cialdella-Kam et al.]/Guebels et al. [20, 21], who all resumed menses, had an average weight gain of 1.64 kg. These findings support the work of Thralls et al.  who, in studying predictors of the triad in adolescent athletes, reported that those at less than 85% of their ideal body weight were four times more likely to report menstrual dysfunction. These results support the suggestion that nutritional interventions should likely aim to not only increase EA which might not be sustained over a prolonged period of time, but also to allow for controlled weight gain. These suggestions can only be applied to those with low EA not due to a diagnosed eating disorder. Athletes with eating disorders were not included in these studies and they may require a more intensive intervention.
Despite the varying methodology and the complexity of treating athletes with various needs, there are several useful points that can be taken from this systematic review. First, it appears that increases in body weight and/or BMI are beneficial in resuming menses [20, 21, 22]. At this time, it is difficult to suggest exact numbers for changes in body weight or BMI, as this may be confounded by other factors including fat mass . Second, compliance with nutritional interventions in competitive athletes is challenging. Programs that include weekly follow-up, use of a specified energy dense food or drink as a supplement, and education regarding long-term consequences may improve outcomes. Third, there are multiple factors beyond food intake that may impact menses and referral to a sports psychologist or other health care provider may be necessary.
Limitations and Recommendations for Future Research
Limitations of this systematic review include the overall rigor of the included articles, as only one article received a positive rating on the Quality Criteria Checklist. Additionally, methods of interventions and reporting of outcomes varied among the studies making it difficult to accurately discern the methods by which changes may have occurred. The lack of clear description of specific sports the athletes were involved in and specific sport demands make it difficult to identify whether specific sports or sport types were related to resumption of menses. Furthermore, athletes on birth control were not included in the study and the length of menstrual dysfunction was not reported; thus, the impact of these factors cannot be assessed.
Long-term prospective studies with increased number of participants would be beneficial to continue to determine the time frame needed for nutritionally based interventions to affect menstruation status. Quasi-experimental or cohort studies could begin to determine the best method of intervention (supplement versus nutritional education). Long-term follow-up also would be beneficial to see if athletes who resumed menses maintained this status over time. Further, the issue of compliance needs to be addressed. Studies that investigate the factors affecting eating and health decisions in athletes are warranted.
Menstrual dysfunction is a complex issue, and the “best” treatment may not be easily identifiable due to individual needs of each athlete. The results of this systematic review indicate that 0–100% of female athletes resumed menses and, of those who did, the mean length of time for return to menses ranged from 2.63  to 15.6 months . Furthermore, there is some support for the use of nutritional interventions combined with educational strategies for the treatment of menstrual dysfunction in female athletes. Weight gain or increased BMI may be an important factor in resumption of menses.
LS contributed to study design, data collection, data analysis and interpretation, drafting and article revision, and approval of the final manuscript. JB contributed to data collection and analysis, drafting of article, and approval of the final manuscript. BH contributed to data analysis and interpretation, drafting and revision, and approval of the final manuscript.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
IRB approval is not needed for a systematic review.
No informed consent is needed for a systematic review.
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