One Season in Professional Cycling Is Enough to Negatively Affect Bone Health

a very popular sport worldwide, and several studies have already indicated that cycling at various levels has a negative impact on bone health. This is of concern to both performance and health managers of many cycling teams at different levels because of its economic and social impact. Based on the scienti c literature, we hypothesize that a single season at the professional level can negatively affect bone health status. The aim of this study was to assess how professional cycling affects bone health markers after one season. Densitometry was used to measure the bone mineral density (BMD), bone mineral content (BMC), bone area (BA), fat mass (FM), fat-free mass (FFM), T-score and Z-score in professional cyclists after one season. After one season at the professional level, cyclists' BMD decreased signi cantly in the legs, trunk, ribs and pelvis (p 0.05). BMC decreased in the arms and spine (p 0.05). BA decreased signi cantly in the arms and spine (p 0.05). In addition, a signi cant decrease in Z-score (p 0.05) and a decreasing trend in T-score and total BMD (p= 0.06) were observed. One season of professional cycling is enough to negatively affect bone

trunk, ribs and pelvis (p 0.05). BMC decreased in the arms and spine (p 0.05). BA decreased signi cantly in the arms and spine (p 0.05). In addition, a signi cant decrease in Z-score (p 0.05) and a decreasing trend in T-score and total BMD (p= 0.06) were observed. One season of professional cycling is enough to negatively affect bone health status. Keywords:endurance; bone mineral density; T-score; osteoporosis and osteopenia 1. Introduction In recent years, there has been a growing concern within sports science regarding bone health, especially in non-impact sports [1–7]. In particular, studies that have examined cyclists have demonstrated low values in bone health markers, which may consequently increase the risk of injury or early onset of bone disease (osteoporosis) [1,2]. This problem is multifactorial for cyclists. One of the factors is the lack of force impact that would stimulate bone remodeling by nature of the sport [8]. Another factor is energy availability (EA), speci cally the amount of dietary energy available after exercise training for all metabolic processes expressed in relation to fat-free mass (FFM) [9]. For example, athletes who train and compete in endurance races (i.e., long distance) are more likely to have energy de ciencies [9]. This is due to the fact that cyclists use carbohydrate- or energy-restrictive diets to reduce body mass and fat mass with the aim of improving their power/weight ratio, as this is one of the best indicators of performance, especially in competitions with a lot of uphill terrain [10]. Since a lighter cyclist expends less energy than a heavier rider to maintain the same speed on uphill terrain, their fatigue on long climbs will be delayed. These energy imbalances are related to reproductive function and bone health in female and male athletes, also known as the “Relative Energy De ciency in Sport” (RED-S) [11]. Energy de cit-related suppression of hormones, such as testosterone, triiodothyronine (T3) and leptin, suggests the dysregulation of the reproductive system and energy metabolism in male athletes [12,13]. Increased calcium loss through sweat in elite cyclists (up to 150 mg/h) could be another factor that negatively affects

male athletes, also known as the “Relative Energy De ciency in Sport” (RED-S) [11]. Energy de cit-related suppression of hormones, such as testosterone, triiodothyronine (T3) and leptin, suggests the dysregulation of the reproductive system and energy metabolism in male athletes [12,13]. Increased calcium loss through sweat in elite cyclists (up to 150 mg/h) could be another factor that negatively affects bone mineral density (BMD) [14]. As a consequence, Nutrients2023,15, 3632.

Nutrients2023,15, 3632 2 of 15 there is an increase in parathyroid hormone concentrations that would promote bone demineralization to increase serum calcium levels [15]. If this mechanism is chronically activated, it may be a contributing factor to the low BMD of elite cyclists [16], although calcium loss through sweat is currently being questioned [17]. Bone health problems in cycling develop over a prolonged period with several in- uencing factors, where poor nutrition and lack of loading due to the mode of exercise are key factors [11,18,19]. It is known that low long-term energy availability is related to poor bone health in both male and female athletes [11,18–20], and road cycling does not produce signi cant osteogenic bene ts compared to weight-bearing sports [21]. Cycling improves the cardiovascular system with decreased cardiovascular risk factors as well as reduced cancer risk [22]. However, as a non-weight-bearing sport, cycling is often associated with lower levels of bone mass [23], with two thirds of adult professional and masters road cyclists classi ed as osteopenic [24]. This situation can therefore lead to the development of osteoporosis, which typically affects older populations and is characterized by a deterioration of the microarchitecture of bone tissue and BMD, leading to increased bone fragility and susceptibility to fractures [25]. In addition, it has been shown that the level of practice and/or years of training are factors that could increase the risk of low bone mass [21]. There are many studies that have evaluated the effect of years of training and com- petition of high-level road cyclists (well-trained, amateur and professional cyclists) on markers of bone health [1,2,26]. Recently Mart½nez-Noguera et al. [2] found lower levels of BMD, bone mineral content (BMC) and bone area (BA) in professional cyclists compared to amateurs. A few years before, Klomsten et al. [1] observed that Norwegian national elite road cyclists had lower BMD compared to runners, and a large proportion were classi ed as having low BMD (Z-score 1), despite having performed heavy endurance training. Previously, Piotrowska et al. [26] found no signi cant change in BMD in any age or sex group

to amateurs. A few years before, Klomsten et al. [1] observed that Norwegian national elite road cyclists had lower BMD compared to runners, and a large proportion were classi ed as having low BMD (Z-score 1), despite having performed heavy endurance training. Previously, Piotrowska et al. [26] found no signi cant change in BMD in any age or sex group in amateur cyclists during one season. To date, we have not found any studies on professional road cyclists that assessed changes in bone health markers longitudinally. Therefore, the main objective of this study was to evaluate changes in bone health markers in professional road cyclists over two seasons. We hypothesized that there would be a negative effect on BMD and BMC in professional cyclists after two competitive seasons. 2. Methodology 2.1. Subjects of Study Eighteen male professional cyclists completed this study (Table). The professional cyclists (ethnicity: 14 Caucasian and 4 Hispanic) competed in Union Cycliste Internationale (UCI) PRO TOUR competitions and participated in major UCI stage races (Vuelta a España, Giro d'Italia and Tour de France). The PRO cyclists were recruited on the basis of the following criteria: (i) aged between 20 and 40 years, (ii) enrolled in a registered professional team and (iii) have raced in at least one of the main 3-week-stage races in recent years. Ad- ditionally, exclusion criteria included riders who could have had or had rickets, metabolic diseases suffered in infancy and thyroid diseases. Table 1.Baseline general characteristics of the professional cyclists. Characteristics Age (years) 27.3 (3.40) Body mass (kg) 72.7 (5.98) Height (cm) 180.0 (5.89) FM (kg) 5.01 (1.74) FFM (kg) 64.7 (4.88) Values are expressed as mean (SD). FM = fat mass; FFM = fat-free mass.

Nutrients2023,15, 3632 3 of 15 The subjects signed an informed consent form prior to enrollment. The study was performed under the guidelines of the Declaration of Helsinki Declaration for Human Research [27] and was approved by the Ethics Committee (CE091802). 2.2. Study Protocol This study has a longitudinal experimental design that required each cyclist to visit the laboratory in the 2018 and 2019 pre-season. Subjects were measured from 8:30 to 11:00 a.m. on an empty stomach (no food and liquid intake). Prior to data collection, subjects were advised of the nature and possible risks of the project, and informed written consent was obtained. 2.3. Dual-Energy X-ray Absorptiometry (DXA) Body composition was assessed via whole-body DXA (XR-46; Norland Corp., Fort Atkinson, WI, USA). BMD (g/cm 2 ), bone mineral content (BMC) (g), bone area (BA) (cm 2 ), fat mass (FM) and fat-free mass (FFM) (g) were evaluated during morning fasting. In the preceding 5 years, no calibration errors were found, and there were no rmware or software updates. The measuring device had been checked by the manufacturer. All patients wore underwear without metal accessories during the assessments. The explorations and analyses were carried out by an experimented and certi ed technician. The repeatability, expressed as the coef cient of variation of BMD measurements, was 0.86% for the whole body. The anatomical segments of arms, legs, trunk, ribs, pelvis and spine were analyzed using the whole-body scanner. 2.4. Statistical Analyses Statistical analysis was carried out with SPSS 21.0 software (International Business Machines, Chicago, IL, USA). Data are presented as mean standard deviation (SD). The Levene and Shapiro–Wilk tests were run to test for homogeneity and normality of the data, respectively. A paired-samplest-test was applied to compare BMD, BMC, BA, FT, FFT, T-score and Z-score between 2018 and 2019. Moreover, Wilcoxon signed-rank test was used when the data did not have a normal distribution. The level of signi cance was set at p 0.05. Furthermore, standardized mean differences were calculated utilizing Cohen's effect size (ES) with a 95% con dence interval (CI) for all comparisons. Threshold values for the ES statistics were

T-score and Z-score between 2018 and 2019. Moreover, Wilcoxon signed-rank test was used when the data did not have a normal distribution. The level of signi cance was set at p 0.05. Furthermore, standardized mean differences were calculated utilizing Cohen's effect size (ES) with a 95% con dence interval (CI) for all comparisons. Threshold values for the ES statistics were as follows: >0.2 small, >0.5 moderate and >0.8 large [28]. 3. Results Table professional cycling in 2018 and 2019. After one year of training and competition at the professional level, a signi cant decrease in BMD was observed in the legs, trunk, ribs and pelvis (p 0.05), and a decreasing trend was observed in total BMD in professional cyclists (p= 0.061; Table). In addition, a signi cant increase in BMC (p 0.05; Figure) and BA ( p 0.05; Figure) was found in the arms and spine after one season (Table). However, no signi cant changes in FM and FFM were observed in any of the anatomical areas analyzed (Table).

Nutrients2023,15, 3632 4 of 15 Table 2. Comparison of bone mineral density (BMD), bone mineral content (BMC), bone area, fat mass and fat-free mass values in professional cyclists between 2018 and 2019 pre-seasons. Values are mean (SD). 2018 2019 Time p-Value ES BMD Arms 1.11 (0.08) 1.10 (0.07) 0.102 0.407 BMD Legs 1.31 (0.10) 1.30 (0.11) 0.017 * 0.504 BMD Trunk 0.868 (0.07) 0.851 (0.07) 0.012 * 0.489 BMD Ribs 0.678 (0.04) 0.663 (0.04) 0.003 * 0.814 BMD Pelvis 1.05 (0.11) 1.02 (0.10) 0.001 * 0.811 BMD Spine 1.01 (0.10) 1.03 (0.11) 0.081 0.278 BMD Total 1.19 (0.08) 1.18 (0.08) 0.061 0.410 BMC Arms 434 (51.4) 452 (66.7) 0.033 * 0.320 BMC Legs 1213 (106) 1195 (107) 0.663 0.235 BMC Trunk 722 (125) 711 (130) 0.260 0.275 BMC Ribs 262 (49.5) 265 (62.9) 0.499 0.092 BMC Pelvis 248 (52.2) 244 (53.4) 0.427 0.192 BMC Spine 212 (36.5) 201 (38.5) 0.003 * 0.648 BMC Total 2879 (315) 2869 (322) 0.187 0.324 BA Arms 390 (34.0) 400 (30.9) 0.023 * 0.587 BA Legs 923 (44.2) 906 (134) 0.257 0.139 BA Trunk 827 (87.3) 832 (123.0) 0.459 0.063 BA Ribs 385 (53.5) 399 (87.5) 0.528 0.242 BA Pelvis 235 (30.1) 239 (40.7) 0.794 0.176 BA Spine 208 (20.2) 194 (24.1) 0.003 * 0.828 BA Total 2391 (147) 2436 (190) 0.138 0.396 FM Arm left 221 (76.0) 232 (94.7) 0.337 0.233 FM Arm right 241 (80.9) 249 (99.8) 0.446 0.184 FM Trunk 2151(741) 2008 (657) 0.459 0.291 FM Leg left 1025 (445) 997 (422) 0.865 0.120 FM Leg right 1041 (445) 1021 (442) 0.865 0.084 Fat Mass Total 5014 (1737) 4835 (1715) 0.640 0.177 FFM Arm left 3645 (417) 3719 (380) 0.097 0.414 FFM Arm right 3976 (498) 4009 (392) 0.535 0.149 FFM Trunk 27,394 (2355) 27,290 (2267) 0.638 0.113 FFM Leg left 12,463 (937) 12,527 (895) 0.470 0.174 FFM Leg right 12,696 (934) 12,811 (865) 0.159 0.348 Fat-Free Mass Total 64,722 (4883) 64,880 (4636) 0.629 0.116 T-score 0.436 (0.965) 0.679 (1.012) 0.061 0.462 Z-score 0.057 (0.958) 0.343 (1.000) 0.021 * 0.556 * =p-values 0.05 and trends in the range of 0.05–0.07. BA =

27,394 (2355) 27,290 (2267) 0.638 0.113 FFM Leg left 12,463 (937) 12,527 (895) 0.470 0.174 FFM Leg right 12,696 (934) 12,811 (865) 0.159 0.348 Fat-Free Mass Total 64,722 (4883) 64,880 (4636) 0.629 0.116 T-score 0.436 (0.965) 0.679 (1.012) 0.061 0.462 Z-score 0.057 (0.958) 0.343 (1.000) 0.021 * 0.556 * =p-values 0.05 and trends in the range of 0.05–0.07. BA = bone area; BMC = bone mineral content; BMD = bone mineral density; FFM = fat-free mass; FM = fat mass; T-score = is the number of SD below the mean BMD in young adults, osteoporosis is de ned by a BMD T-score of less than 2.5SD, and osteopenia by a T-score between 1 and 2.5SD.; Z-score = is the number of SDs above or below the mean BMD in the population of the same age as the patient/subject, a Z-score of 2.0SD or below was described as “low BMD for chronological age”, and above 2.0 was described as “normal BMD for chronological age”.

Nutrients2023,15, 3632 5 of 15Nutrients 2023, 15, x FOR PEER REVIEW 4 of 15 Figure 1. Changes in BMD after one season in professional cyclists in arms, legs, trunk, ribs, pelvis, spine and total. BMD = bone mineral density. * ≤ 0.05; # = in the range of 0.051–0.07. Figure 1. Changes in BMD after one season in professional cyclists in arms, legs, trunk, ribs, pelvis, spine and total. BMD = bone mineral density. * 0.05; # = in the range of 0.051–0.07.

Nutrients2023,15, 3632 6 of 15Nutrients 2023, 15, x FOR PEER REVIEW 6 of 15 Moreover, professional cyclists showed a decrease in Z‐score (−502%; p = 0.021; ES = 0.556) and a downward trend in T‐score (−55.7%; p = 0.061; ES = 0.462) after one season of training and competitions (from 2018 to 2019; Table 2 and Figure 6). It should be noted that 5 of the 29 cyclists had osteopenia in 2018, and this figure increased to 6 in 2019. Figure 2. Changes in BMC after one season in professional cyclists in arms, legs, trunk, ribs, pelvis, spine and total. BMC = bone mineral content. * ≤ 0.05. Figure 2. Changes in BMC after one season in professional cyclists in arms, legs, trunk, ribs, pelvis, spine and total. BMC = bone mineral content. * 0.05.

Nutrients2023,15, 3632 7 of 15Nutrients 2023, 15, x FOR PEER REVIEW 7 of 15 Figure 3. Changes in BA after one season in professional cyclists in arms, legs, trunk, ribs, pelvis and total. * ≤ 0.05. Figure 3. Changes in BA after one season in professional cyclists in arms, legs, trunk, ribs, pelvis and total. * 0.05.

The study evaluates the impact of a professional cycling season on bone health markers.