Abstract
Aim & objectives
Females who engage in high levels of sports have a high prevalence of menstrual cycle disorders and bone stress injuries (BSI). In this study, we determined the prevalence of menstrual disorders and fractures in female athletes and their association with bone mineral density (BMD) parameters.
Material & methods
Cross-Sectional Study. Forty-one female athletes from a public High-Performance Regional Centre; 24 high-endurance athletes (HEA) and 17 other athletes, were included. To form the control group, we invited medical students from a public University. Twenty-nine non-athletes (NA) were included. A health surveys and a dual-energy X-ray absorptiometry (DXA) were conducted for all participants.
Results
Among the participants (median age, 24 years; body mass index, 21 kg/m2), the percentage of long-term amenorrhoea was 42 % in HEA vs. 0 % in NHEA (OR 25.35; 95 % CI 1.37–470.50, p = 0.008) or 10 % in NA (OR 6.20; 95 % CI 1.46–26.24, p = 0.022), and the percentage of BSI was 29 % in HEA vs. 0 % in NHEA or NA. Both groups of female athletes (HEA and NHEA) showed higher Z-scores than those of NA in the femur; however, only NHEA had a significant increase in the BMD on lumbar spine than that of NA.
Conclusion
The prevalence of long-term amenorrhoea and/or BSI was significantly higher in the HEA than in the NHEA or NA females. In contrast, HEA, like NHEA, had higher BMD values in the femur than those of controls. It is unlikely that DXA parameters can be used to estimate cortical BSI risk in this population.
Keywords: Sport, Bone density, Amenorrhoea, Fractures, Young women
Graphical abstract
1. Introduction
Failure to achieve the maximum potential peak bone mass around the second decade of life predisposes patients to osteoporosis and resulting senile fractures. Professor Charles Dent summarised this idea, describing senile osteoporosis as a paediatric disease.1
Physical activity is a key factor in attaining high peak bone mass. The effects of physical activity on bone mass are most pronounced in adolescents and children.2 This is one of the reasons because the World Health Organization recommends physical activity for children and adolescents.3 This positive effect of sports on bone mass, measured as bone mineral density (BMD), persists in young females (20–35 years).4,5 However, the gain in BMD, is associated with weight-bearing and/or high-impact sports, but not with non-weight-bearing sports,6,7 and there are differences between male and females athletes, with a higher influence of sport on BMD values in males than in females.8 Therefore, young females performing high-endurance sports, especially lean sports, where there is a major concern about body weight and appearance, probably will not achieve any benefit for sport performance over bone mass or will even experience negative impact on their BMD.9,10
Another key factor in increasing the peak bone mass is maintaining regular menstrual cycles.11 In young females, amenorrhoea is associated with low BMD12 and with bone stress injuries (BSI).13,14 The relative energy deficiency in sport (RED-S), the menstrual irregularities, and/or low BMD, are common in elite athletes.9 Both, menstrual irregularity, and low BMD were independently associated with an increased risk of BSI.15 In addition, these BSI of the youth are associated with post-menopausal fractures.16
Based on the above, it is easy to understand why young female athletes, especially high endurance female athletes, face the conundrum of maintaining the highest level of training or tailoring their training sessions and diet to maintain weight and menstrual regularity, regardless of cost of their personal records, to reduce current BSI and/or future osteoporotic fractures. In a recent study, low BMD was more common in female athletes with BSI17 when compared with other athletes without BSI. There are no data for comparison with non-athletes.
The aims of this study were: 1) to evaluate the prevalence of amenorrhoea and BSI using self-report, 2) to show the BMD values of a cohort of young female high-endurance athletes compared to non-high endurance athletes and non-athlete peers, and 3) to assess the association between BMD and BSI.
2. Methods
This study was an investigator-initiated, single-centre, quasi-experimental study to assess bone and menstrual health parameters in female athletes and their associations with bone mineral density. This study was approved by the Research Ethics Committee Health Area (21-PI171). Study consent was obtained from all participants.
2.1. Study design
This was a Cross-Sectional Study which included three groups of participants. Two groups of athletes: 1) high-endurance female athletes (HEA), 2) athletes practising non endurance sports (NHEA), and a control group of non-athletes (NA) females. To be included in the NA group, the participants should be females who did not perform regular physical activities.
2.2. Definitions
High-intensity regular physical activity: A participant was considered to have regular physical activity when she performed at least 4 weekly sessions of sports or physical activity lasting more than 45 min on an intensity scale of 7–8 over 10.
High-endurance sports: High-endurance sports are defined as those in which continuous fatigue, of more than 5 min, is supported through aerobic metabolism for most of the duration of the sports activity. The following sports were considered high-endurance sports: athletics (distance), swimming, cycling, and triathlon.
Non-high endurance sports: Non-high endurance sports are defined as sports in which alternate aerobic-anaerobic efforts are made. The following sports were considered as non-high-endurance sports: athletics (speed), basketball, canoeing (speed), football, handball, rugby, and volleyball.
2.3. Setting and participants
Fifty female athletes from the High-Performance Regional Centre were invited to participate in this study (ages 18–38 years). To form the control group, we invited the 111 medical students from the sixth-grade School of Medicine (aged 22–24 years) to participate. Announcements were made using Instagram® to increase the sample size. Invitations to participate included an explanation of the study, instructions, and the risks and benefits of participation. A flow diagram of the study participants is shown in Fig. 1.
Fig. 1.
Flow diagram.
2.4. Study interventions
Students were asked to complete a survey that assessed their clinical characteristics as well as menstrual and bone health parameters. The survey was conducted using Google Forms® and comprised four sections (epidemiological characteristics, sport practicing characteristics, menstrual and bone health history). On bone health section, participants were asked to self-report their BSI. It was required that the BSI was confirmed on image at diagnosis to include a previous history of BSI on the questionnaire. All participants were invited to perform a Dual-Energy X-ray Absorptiometry (DXA) scan. A General Electric Lunar Prodigy Dexa Bone Densitometer (United States) was used to measure bone mineral density by regional scan during. T- and Z-scores for the BMD of the lumbar vertebrae L1–L4 and total femoral neck were recorded.
2.5. Outcomes
The primary outcome was to establish the percentage of stress bone fractures and long-term amenorrhoea in HEA and compare these values with those of other athletes and non-athletes. The secondary outcome was the association between BMD and the prevalence of both, stress bone fractures and long-term amenorrhoea.
2.6. Study size
Owing to the exploratory nature of the study and the lack of previous data, we did not calculate the sample size. The sample size was established for convenience based on the actual number of volunteers who agreed to participate.
2.7. Statistical method
All the participants who completed the survey and underwent DXA scan were included in the analysis. The median and interquartile range (IQR) were calculated to summarise continuous variables. The frequencies and percentages of the total were calculated to summarise the categorical data. Differences between the HEA and the other two groups were analysed using the non-parametric test, Mann–Whitney U test for continuous variables and the Chi-squared test with continuity correction for categorical variables. All p-values were two-sided and are shown without adjustment for multiple testing. Statistical significance was set at p < 0.05. The jamovi project (2021) (Jamovi, Version 1.6.23 [Computer Software]; retrieved from https://www.jamovi.org 1.6.23) was used for statistical analyses.
3. Results
3.1. Participants' characteristics
A total of 70 participants were included in this study. Of the 70 participants, 41 (58.6 %) were athletes, 24 HEA (58.5 %), and 17 NHEA (41.5 %), and 29 were NA controls (41.4 %). Most of the athletes were associated with the High-Performance Regional Centre. NA controls were medical student volunteers from the Medical School (n = 29). Group characteristics are presented in Table 1, Table 2. There were significant group differences in weight and body mass index (BMI) between the NHEA and HEA or NA groups. All participants completed the questionnaire. All participants, except one in the NHEA group, underwent DXA.
Table 1.
Summary of baseline characteristics of participants.
| All (n = 70) | HEA (n = 24) | NHEA (n = 17) | HEA vs NHEA p | NA (n = 29) | HEA vs NA p | |
|---|---|---|---|---|---|---|
| Age, median (IQR), y | 25 (5) | 27 (8) | 24 (4) | 0.114 | 24 (1) | 0.017 |
| Weight, median (IQR), kg | 58 (10) | 56 (6) | 67 (13) | 0.000 | 57 (8) | 0.531 |
| Height, median (IQR), cm | 166 (6) | 165 (5) | 169 (7) | 0.141 | 166 (7) | 0.809 |
| BMI, median (IQR), kg/m2 | 21 (3) | 20 (3) | 24 (4) | 0.000 | 20 (3) | 0.532 |
| Daily stress, No. (%) | ||||||
| Not at all stressed | 3 (4) | 1 (4) | 1 (6) | 0.145 | 1 (3) | 0.432 |
| Somewhat stressed | 33 (47) | 9 (38) | 11 (65) | 13 (45) | ||
| Mostly stressed | 27 (39) | 10 (42) | 3 (18) | 14 (48) | ||
| Completely stressed | 7 (10) | 4 (17) | 2 (12) | 1 (3) | ||
HEA: High-endurance athletes, NA: Non-athletes, NHEA: Non-high-endurance athletes.
Table 2.
Summary of sports characteristics of participants.
| HEA (n = 24) | NHEA (n = 17) | HEA vs NHEA P | |
|---|---|---|---|
| Starting age in sports, median (IQR), y |
7 (5) |
8 (5) |
0.299 |
| Competition level, No. (%) | |||
| Regional | 0 | 8 (50) | 0.000 |
| National | 18 (75) | 6 (38) | |
| International |
6 (25) |
2 (13) |
|
| Weekly hours of training, No. (%) | |||
| < 10 weekly hours | 7 (29) | 7 (44) | 0.440 |
| 10 to 15 weekly h | 13 (54) | 6 (38) | |
| > 15 weekly hours |
4 (17) |
3 (19) |
|
| Type of exercise, No. (%) | |||
| Aerobic | 24 (100) | 10 (63) | 0.001 |
| Anaerobic | 18 (75) | 13 (81) | 0.914 |
| Jumps | 15 (63) | 10 (63) | 0.812 |
| Gym | 15 (63) | 13 (81) | 0.344 |
| Core |
22 (92) |
9 (56) |
0.004 |
| Sport. No. (%) | |||
| Athletics (endurance) | 15 (63) | 0 | – |
| Athletics (speed) | 0 | 3 (18) | |
| Basketball | 0 | 1 (6) | |
| Canoeing | 0 | 1 (6) | |
| Cycling | 6 (25) | 0 | |
| Handball | 0 | 2 (12) | |
| Rugby | 0 | 10 (59) | |
| Swimming | 2 (8) | 0 | |
| Triathlon | 1 (4) | 0 | |
HEA: High-endurance athletes, NHEA: Non-high-endurance athletes.
3.2. Factors related to menstruation
There were no significant group differences in age at menarche, duration of cycles, menstrual flow, or prevalence of gynaecological pathology. Painful menstruation was more frequent in NA patients (48 %) than in athletes (22 %) (p = 0.021). Group differences in amenorrhoea lasting six or more months and the use of oral contraceptives were statistically significant. Furthermore, 42 % of HEA suffered long term amenorrhoea vs 10 % in NA (OR 6.20; 95 % CI 1.46–26.24, p = 0.022) or 0 % in NHEA (OR 25.35; 95 % CI 1.37–470.50, p = 0.008). Nearly seven of 10 HEA were currently using or used oral contraceptives in the past, whereas only 25 % of NHEA (p = 0.011) and 42 % of NA (p = 0.015) were currently using or used them in the past. Group characteristics are presented in Table 3.
Table 3.
Summary of menstrual cycle characteristics of participants.
| All (n = 70) | HEA (n = 24) | NHEA (n = 17) | HEA vs NHEA p | NA (n = 29) | HEA vs NA p | |
|---|---|---|---|---|---|---|
| Menarche, median (IQR),y | 13 (2) | 13 (2) | 12 (3) | 0.067 | 12 (2) | 0.057 |
| Cycles every 23–35 days | 54 (78) | 19 (79) | 10 (63) | 0.158 | 25 (86) | 0.497 |
| Menstrual flow | 0.394 | 0.681 | ||||
| Very low | 3 (4) | 2 (8) | 0 (0) | 1 (3) | ||
| Below average | 8 (12) | 3 (13) | 1 (6) | 4 (14) | ||
| Average | 38 (55) | 15 (63) | 8 (50) | 15 (52) | ||
| Above average | 16 (23) | 3 (13) | 5 (31) | 8 (28) | ||
| Very high | 4 (6) | 1 (4) | 2 (13) | 1 (3) | ||
| Painful menstruation |
23 (33) |
4 (17) |
5 (31) |
0.331 |
14 (48) |
0.016 |
| Amenorrhoea, No. (%) | ||||||
| No amenorrhoea. | 49 (70) | 11 (46) | 12 (71) | 0.008 |
26 (90) | 0.022 |
| <6months | 11 (16) | 3 (13) | 5 (29) | 3 (10) | ||
| ≥6 months |
10 (14) |
10 (42) |
0 |
0 |
||
| Use of oral contraceptives, No. (%) | ||||||
| Never | 36 (52) | 7 (29) | 12 (75) | 0.011 |
17 (59) | 0.015 |
| At present | 14 (20) | 5 (21) | 1 (6) | 8 (28) | ||
| In the past |
19 (28) |
12 (50) |
3 (19) |
4 (14) |
||
| Gynecological pathology | 10 (14) | 3 (13) | 2 (13) | 0.943 | 5 (17) | 0.631 |
HEA: High-endurance athletes, NA: Non-athletes, NHEA: Non-high-endurance athletes.
3.3. Factors related to BMD and bone fractures
The BMD Z- and T-scores were significantly higher in HEA than in NA in the total femur (p = 0.001 and p = 0.003, respectively), but not in the lumbar spine (p = 0.148 and p = 0.067, respectively) (Table 4). In contrast, there were no differences in the Z- or T-scores for the total femur when the HEA were compared with the NHEA, whereas the BMD T-scores were lower in the HEA on L1-L4 than in the NHEA (p = 0.013).
Table 4.
Summary of bone health characteristics of participants.
| All (n = 70) | HEA (n = 24) | NHEA (n = 17) | HEA vs NHEA p | NA (n = 29) | HEA vs NA p | |
|---|---|---|---|---|---|---|
| BMD L1-L4, median (IQR), g/cm2 | 1.21 (0.25) | 1.24 (0.28) | 1.36 (0.22) | 0.007 | 1.14 (0.18) | 0.344 |
| Z-score, median (IQR), SD | 0.20 (1.80) | 1.00 (1.70) | 1.40 (2.00) | 0.114 | −0.10 (1.25) | 0.148 |
| T-score, median (IQR), SD |
0.30 (1.85) |
0.80 (1.55) |
1.70 (1.98) |
0.013 |
−0.35 (1.85) |
0.067 |
| BMD Total femur, median (IQR), g/cm2 | 1.07 (0.17) | 1.12 (0.17) | 1.15 (0.12) | 0.128 | 0.98 (0.17) | 0.002 |
| Z-score, median (IQR), SD | 0.60 (1.65) | 1.10 (1.15) | 0.90 (0.80) | 0.874 | −0.05 (1.48) | 0.001 |
| T-score, median (IQR), SD |
0.60 (1.50) |
1.00 (1.35) |
1.20 (1.63) |
0.130 |
−0.15 (1.70) |
0.003 |
| Bone fractures, No. (%) | ||||||
| No fractures | 45 (65) | 15 (63) | 8 (50) | 0.004 | 22 (76) | 0.005 |
| Stress fractures | 7 (10) | 7 (29) | 0 | 0 | ||
| Traumatic fractures | 17 (25) | 2 (8) | 8 (50) | 7 (24) | ||
HEA: High-endurance athletes, NA: Non-athletes, NHEA: Non-high-endurance athletes.
None of the controls or the NHEA reported a stress fracture whereas seven of the 24 HEA (29 %) had a stress fracture (p = 0.005 and 0.004, respectively). Nearly half of the NHEA had traumatic fractures (75 % of them played rugby), whereas only 8 % of the HEA and 24 % of the NA had traumatic fractures.
4. Discussion
In our sample of 70 young females, playing high-endurance sports was associated with a higher prevalence of stress fractures and amenorrhoea compared to non-high-endurance sports or with non-athlete females. Regarding BMD, the HEA had a higher BMD in the femur than that of the NA, but there were no differences in the lumbar spine, whereas the NHEA did had a higher BMD in both locations than that of the NA. In addition, the HEA had a lower BMD in the lumbar spine than that of the NHEA. In BMD higher scores are desirable.
Playing sports has been associated with improvements in BMD,4, 5, 6 especially in sports with impact loading7,18,19 and in men.8 However, the magnitude of this beneficial effect is lower in high-endurance sports than in non-high endurance sports. In endurance runners, this increase in BMD is predominantly observed in the hip and femur necks, with lower BMD in the lumbar spine.20 Low lumbar spine BMD in HEA has been attributed to hormonal imbalances.21 In men, the alterations in bone health of athletes who play high-endurance sports are associated with testosterone loss.22 In women, oligomenorrhoea and amenorrhoea are associated with playing sports.23 These menstrual abnormalities are associated with low BMD and reduced bone mineral content in female athletes.24 Our study confirmed the high prevalence of menstrual cycle abnormalities in HEA, as amenorrhoea lasted for more than six months in 42 % of the HEA in our series. We speculate that this long-term amenorrhoea could have affected reproductive and bone health of the HEA. In these athletes, the expected improvement in BMD associated with sports should be reduced owing to the impact of the long-term amenorrhoea and the consequent reduction in endogenous oestrogen exposure. In addition, we should pay attention to the high percentage of HEA that require to take contraceptive pills to control menstrual cycle dysfunction when compared with NA or NHEA.
As a secondary objective, the association between BMD parameters and BSI was assessed. In the present study, stress fractures were not associated with a reduction in BMD. Our study agrees previous studies showing that the BSI are independent of BMD measured using DXA.25,26 However, a recent cohort study in male athletes differentiated the value of BMD measured using DXA according the anatomical site of the BSI; cortical-rich locations (tibia, fibula, femur, metatarsal, or tarsal navicular) vs. trabecular-rich locations (pelvis, femoral neck, or calcaneus).17 The authors identified a low BMD in athletes with trabecular-rich BSI. A recent cohort study does not reproduce these outcomes, with neither BMD nor bone microarchitecture related to the bone localization of the BSI.27
We did not assess the hypothesis of a difference between cortical or trabecular fractures, as all the identified BSI in our study were cortical-rich locations, mostly metatarsal BSI.
The high prevalence of menstrual cycle disorders in our study, makes amenorrhoea a major problem for female athletes. Menstrual dysfunction is frequent in young female athletes and early intervention is essential to prevent its progression to amenorrohea.28 Future research should be focused on the development of programs designed to reduce the impact of high-endurance sports on menstrual cycles, which will allow athletes to maintain high-level performance without sacrificing their bone and menstrual health. The REFUEL randomized trial29 is an example of the correct approach. The authors proposed a 12-month intervention with a higher dietary energy intake in female athletes with oligomenorrhoea/amenorrhoea. Nutritional intervention increased menstrual cycle frequency but not BMD.
In addition to implementing programs to reduce the high prevalence of oligomenorrhoea or amenorrhoea among female athletes, parents and trainers should focus athletes’ awareness on this subject. Most female athletes are unaware of the negative impact of menstrual alterations on their health. Even amenorrhoea should be considered as an advantage for maintaining a high-level sports performance. In a recent study, only players in top soccer leagues were aware of female athlete triad and took preventive measures to prevent it.30
4.1. Limitations
This study has several limitations. Firstly, the study was conducted on HEA from a single high-performance centre, and the results may not be generalisable. Second, a convenience sample of young volunteers was used. Third, participants in the three groups were not matched. However, as Table 1 shows, most of the characteristics are comparable, except for the weight in the NHEA. In addition, data on Z- or T-scores were standardised according to age, height, and weight facilitating its comparison.
5. Conclusion
In young female athletes, participation in high-endurance sports was associated with a high prevalence of BSI and menstrual cycle disorders. A high prevalence of amenorrhoea may negatively affect bone health and reduce the expected improvement in lumbar BMD in females who play sports. A focused training approach that manages to maintain menstrual regularity is needed in young female athletes to improve bone health.
In contrast, the HEA achieved higher BMD values in the femur than NA did. It is unlikely that DXA parameters can be used to estimate cortical BSI risk in this population.
Ethical statement
This study was approved by the Research Ethics Committee of West Valladolid Health Area (21-PI171). Study consent was obtained from all participants.
Funding
No funding.
Availability of data and materials
The data that support the findings of this study are available from the corresponding author, upon reasonable request.
CRediT authorship contribution statement
M. García-Alonso: Conceptualization, Investigation, Data adquisition, Writing – original draft, Writing – review & editing. L. Corral-Gudino: Conceptualization, Methodology, Data curation, Formal analysis, Writing – original draft, Writing – review & editing.
Declaration of competing interest
All authors declare that they have no conflict of interest.
Acknowledgements
We thank the female athletes and medical students involved in the study for their efforts and contributions. We thank Asunción Robles Sánchez, María Jesús Rodríguez Gómez, Mauricia García Lesmes, Rosario Bueno Bautista and Carmen García García who performed the densitometry. We thank J. Ignacio Rodríguez Calvo, director of the High-Performance Regional Centre Rio Esgueva-Valladolid, and Professor Uriel Reguero Ribera, middle-distance coach and Sport Sciences, for their help.
Contributor Information
M. García-Alonso, Email: emebe.inte@gmail.com.
L. Corral-Gudino, Email: lcorral@saludcastillayleon.es.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author, upon reasonable request.