Discussion
Our main finding was that compared with runners, cyclists had significantly lower BMD for all measured sites. This extends previous research done in the UK and the USA.5 23 24 Ten of 19 cyclists had BMD Z-scores ≤−1, despite that all, but one rider, reported to train heavy resistance training on the lower extremities in the previous 2 years. Low BMD was not confined to females. One male rider was classified as osteoporotic (Z-score ≤−2) and he had secondary clinical risk factors for fracture (previous spinal fracture).18 In contrast, none of the runners had low BMD for any of the measured sites. The logistic regression model revealed no significant relationship with any independent variables, except type of sport. Thus, the difference in BMD observed between runners and cyclists appears to be attributed to the difference in mechanical strain exerted on the skeleton by gravitational forces.
BMD and strength training
There is currently limited research regarding the prevalence of strength training in elite cyclists and its effect on BMD. To the best of our knowledge, this is the first study to demonstrate that a high proportion of elite cyclists have BMD Z-scores ≤−1, despite reporting to train heavy resistance training on the lower extremities. It should be acknowledged that similar results have been reported in recreational cyclists.10 Unfortunately, no information regarding intensity or frequency was given in the aforementioned study, or in ours, which makes it difficult to compare the results. Furthermore, the findings in the present study contradict recent research by Mathis and Caputo,25 who found that resistance training was positively associated with BMD in the lumbar spine and hip bone in recreational male road cyclists (age 31–69 years). It is possible that the large amount of non-weight-bearing training conducted by the athletes in the present study attenuated the osteogenic effect elicited by the resistance training. Most studies documenting a beneficial effect of resistance training on bone mass are longitudinal studies, lasting for minimum 7–12 months, with two to three sessions per week.26 27 Usually, cyclists perform strength training during off-season, which is the winter months from October to January. Thus, 2–4 months of strength training might not be sufficient to elicit the bone modelling process.
Low BMD (Z-score <−1) was site specific
The prevalence of low BMD in the present study was site specific, having occurred in the lumbar spine and the femoral neck. In contrast, only one rider had low total body BMD. Previous research has shown that both the lumbar spine and the femoral neck are risk areas of low BMD in cyclists.9 11 23 24 The spine and, to some extent, the femoral neck consist of trabecular bone. This has a higher metabolism compared with cortical bone, which is the main constituent of the skeleton. Thus, it is hypothesised that trabecular bone responds to loading and unloading earlier than cortical bone.
Cycling performance depends on power-to-weight ratio
Elite cyclists, as well as long-distance runners, have a reputation of an unhealthy focus on leanness and low body mass. Sundgot-Borgen and Torstveit28 reported that 8% of Norwegian male athletes suffered from eating disorders, and an alternative terminology to the female athlete triad, relative energy deficiency in sport (RED-S), has been proposed, in part to acknowledge male athletes.1 The syndrome involves energy deficit as the main component. In cycling, the most important performance marker is power-to-weight ratio, or watt per kilogram. Thus, a reduction in body mass will increase cycling performance if power is sustained. There are reports of cyclists trying to enhance their power-to-weight ratio at the expense of energy intake.29 Furthermore, due to prolonged exercise, cyclists may be at risk of having suboptimal energy intake during training, which has been associated with low bone mass.1 30 Unfortunately, eating habits and the prevalence of RED-S are unknown in our sample.
Calcium intake is closely linked to the total energy intake. In the present study, all athletes had an adequate calcium intake and calcium was not associated with low BMD in cyclists. This is consistent with previous research, which has not been able to demonstrate a significant relationship between calcium intake and BMD in cyclists.7 9 23 Recent research has shifted focus from total calcium consumption to the timing of calcium intake. The dermal loss of calcium during prolonged exercise has shown to elevate the expression of parathyroid hormone (PTH) and cross linked C-telopeptide of type 1 collagen (CTX-1) in serum, which are biomarkers associated with higher osteoclastic activity and bone loss. Haakonssen and colleagues31 demonstrated that a calcium-rich meal 90 min prior to intensive exercise decreased the expression of PTH and CTX-1. This is especially relevant for cyclists who often compete for several hours in warm climate and the dermal loss of calcium is thought to be substantial. We did not investigate the timing of calcium intake in our study.
Secondary amenorrhoea
Energy deficits have been linked to secondary amenorrhoea in female athletes.32 Sixty-seven per cent of the female athletes in the present study reported that they, at some point during their career, had experienced secondary amenorrhoea. The distribution was similar in cyclists and runners. We found no relationship between secondary amenorrhoea and prevalence of low BMD. Furthermore, none of the female runners with secondary amenorrhoea and previous stress fractures displayed low levels of BMD. This is surprising as both stress fractures and secondary amenorrhoea have been associated with low BMD in previous research.12 33–35 Thus, it is possible that our study was underpowered to show this relationship. In addition, several other nutritional and hormonal factors, such as vitamin D, oestrogen, steroidal contraceptives, cortisol and testosterone, are thought to influence BMD.36–38 Unfortunately, we were not able to measure these markers, which potentially could have given valuable insight to the differences observed in BMD.
Strength and limitations
The sample consisted of homogenous and highly trained individuals. Note that all cyclists competed at an international level. Thus, it is likely that they share similar characteristics of elite cyclists in other countries, making the results of the present study generalisable to elite Caucasian cyclists. Although elite athletes are more challenging to recruit than lower level/recreational athletes, we chose to limit our inclusion to a homogenous group of high-level athletes, at the expense of a larger sample size and statistical limitations. This priority may have resulted in that some associations between independent variables and BMD being overlooked. In this study, we did not identify any runners with BMD Z-scores ≤−1. This could speak to high-quality management and education of these athletes in Norway’s specialised elite training programme (Olympiatoppen). It would be erroneous to conclude that elite runners are not at risk of having low BMD. A study including larger number of participants would be able to estimate the actual difference in risk between groups more accurately.
The participants in the present study are likely to be lighter and smaller compared with the norms in the DXA database. DXA measures BMD in a two-dimensional frame, and is influenced by bone size. Larger bones will have higher areal BMD, compared with smaller bones, even with the same volumetric density.39 To account for this confounding effect, bone mineral apparent density has been introduced, and it is recommended to be applied when assessing BMD in children.39–41 In the present study, we did not correct for bone size, which could result in an overdiagnosing of low BMD. However, the participants in the present study cannot be regarded as individuals with short stature. Thus, it is debatable how meaningful such an adjustment would have been.42 43 Future research should consider the use of quantitative CT, as it measures BMD in a three-dimensional frame and can more accurately measure bone microarchitecture and bone strength.44
The DXA scans were obtained by using several, but experienced technicians. All but two DXA scans were performed on the same equipment (Lunar Prodigy). The remaining two were measured on a Hologic scanner. However, a rerun of the analysis excluding the Hologic results did not alter our results. Furthermore, all health, nutrition and fracture history was based on a questionnaire. Thus, a potential recall bias should be acknowledged.
Practical implications
Our findings extend previous studies that reported a proportion of cyclists to have low BMD (Z-score ≤−1). The novelty is, however, that elite cyclists report to have been performing heavy resistance training and still display low BMD. Unfortunately, due to the study design, it is not possible to assess whether the strength training performed has had a positive effect on the skeleton.
Little is known regarding the prevalence of osteoporotic fractures later in life in elite cyclists, or if low BMD (Z-score ≤−1) is associated with an increased prevalence of fractures in this population. However, what is known from research is that competitive cyclists display lower levels of BMD compared with their active peers already during adolescence.45 Furthermore, both male and female cyclists have been observed to lose as much as 1%–1.5% of BMD in the lumbar spine and femoral neck during the course of a competitive season.11 This corresponds to the accelerated bone loss observed in postmenopausal women.46 Moreover, a higher prevalence of osteopenia and osteoporosis has been displayed in highly trained master cyclists, when compared with inactive controls (89.5% vs 61.1%, respectively).47 Although a Z-score ≤−1 cannot be considered a disease, existing evidence warrants close monitoring of cyclists with low BMD. Further, it raises the question whether interventions to increase BMD in this population should be considered.