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Hormonal balance and nutritional intake in elite tactical athletes
Journal Pre-proofs Hormonal balance and nutritional intake in elite tactical athletes Andrew E. Jensen, Laura J. Arrington, Lorraine P. Turcotte, Karen R. Kelly PII: DOI: Reference:
S0039-128X(19)30194-1 https://doi.org/10.1016/j.steroids.2019.108504 STE 108504
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Steroids
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22 May 2019 14 August 2019 24 September 2019
Please cite this article as: Jensen, A.E., Arrington, L.J., Turcotte, L.P., Kelly, K.R., Hormonal balance and nutritional intake in elite tactical athletes, Steroids (2019), doi: https://doi.org/10.1016/j.steroids.2019.108504
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Pages: 28 Words: 3987 Figures: 3 Tables: 6 References: 37 Contact: Karen Kelly Email: [email protected] Guarantor: Karen Kelly Hormonal balance and nutritional intake in elite tactical athletes Andrew E. Jensen, PhD1,2,3 Laura J. Arrington, MS1,2 Lorraine P. Turcotte, PhD3 Karen R. Kelly, PhD1,3 1Naval
Health Research Center Warfighter Performance Department 140 Sylvester Road San Diego, CA 92106 2Leidos
Inc. 10260 Campus Point Drive San Diego, CA 92121 3University
of Southern California Biological Sciences, Human and Evolutionary Biology Dornsife College of Letters, Arts and Sciences 3616 Trousdale Parkway, AHF 247 Los Angeles, CA 90089
I am a military service member (or employee of the U.S. Government). This work was prepared as part of my official duties. Title 17, USC, §105 provides the “Copyright protection under this title is not available for any work of the United States Government.” Title 17, USC, §101 defines a U.S. Government work as work prepared by a military service member or employee of the U.S. Government as part of that person’s official duties. This work was supported by Naval Special Warfare under work unit N1239.The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, nor the U.S. Government. The study protocol was approved by the Naval Health Research Center Institutional Review Board in compliance with all applicable Federal regulations governing the protection of human
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subjects. Research data were derived from an approved Naval Health Research Center, Institutional Review Board protocol number NHRC.2012.0011.
HIGHLIGHTS ● High prevalence of low testosterone was sampled in the elite tactical athletes. ● Weak positive correlation observed between testosterone and cortisol. ● Long-term elite military training affects the HPA, HPT, and HPG axes.Nutritional intake may influence hormonal imbalances in elite tactical athletes. KEYWORDS Military, androgen, stress, nutrition, thyroid, elite athletes
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ABSTRACT Chronic exposure to multifactorial stress, such as that endured by elite military operators, may lead to overtraining syndrome and negatively impact hormonal regulation. In acute settings (<6 mos), military training has been shown to lead to hormonal dysfunction; however, less is known about the consequences of long-term military training. Thus, the purpose of this study was to determine the chronic effects of military operations and training on the hormone profile of elite military operators. A cross-sectional, random sample of aActive duty elite US military operators (n = 65, age = 29.8 ± 1.0 yrs, height = 178.4 ± 0.7 cm, weight = 85.1 ± 2.0 kg) concomitantly engaged in rigorous physical training were recruited to participate in the study. Following an overnight fast, Wwaking plasma concentrations of luteinizing hormone, total testosterone (TT), free testosterone, sex-hormone binding globulin, cortisol, thyroid stimulating hormone, triiodothyronine, and thyroxine were obtained. Data were analyzed for correlations and compared against normative reference values. There was a significant positive correlation between TT and cortisol (R² = 0.07; P = 0.038). In addition, 43% of the participants (n = 28) had TT below age-based normative reference ranges. These results indicate that long-term military operations and training may place a large burden on the operators and depress or alter the hypothalamic pituitary, adrenal, gonadal, and thyroid axes. Further research need be conducted to determine what, if any, consequences these differences may cause.
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INTRODUCTION During times of enhanced multifactorial stress, such as that induced by military operations and training, hormonal balance may be impacted. Several factors have been shown to impact hormonal balance under stress conditions including training load and nutritional deficiencies (1-3). However, most studies have examined the effects of acute (< 8 weeks) military training operations on stress-related hormonal factors and they have shown that once the intense training stimulus is removed hormones return to baseline measures (3-5). There is, however, a dearth of information regarding the chronic and long-term hormonal and physiological consequences of intense physical and operational training in elite military communities. Chronic exposure to multifactorial stress, including training load and nutritional deficits, is associated with hormonal imbalances and may ultimately lead to overtraining syndrome (3, 6). Overtraining syndrome is generally characterized by reduced physical performance, increased fatigability, and subjective symptoms of stress (2). Some of the hormonal alterations shown to be responsible for these consequences include changes in the hypothalamic-pituitary-gonadal axis (HPGA) and the hypothalamic-pituitary-adrenal axis (HPAA) including: low testosterone, high cortisol, and high sex hormone-binding globulin (SHBG) (2, 6, 7). Testosterone deficiency with or without elevated cortisol levels is a well-accepted marker of overtraining (2, 7, 8). High cortisol levels have been correlated with low testosterone levels in over-trained athletes (9) and has been shown to inhibit testosterone production in both civilian and military men (10-12). In addition, there is a negative correlation during high intensity exercise between SHBG and
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testosterone, which may influence testosterone turnover and ultimately lead to other negative hormonal changes when high intensity exercise is performed daily (13). Improper nutritional intake has also been implicated in the development of overtraining syndrome and hormonal imbalance in those with high stress loads (1, 3, 14). In healthy resistance trained males there is a positive correlation between fat intake and testosterone levels and a negative correlation between protein intake and testosterone levels (15). This is supported by findings which indicate that a typical Western diet that is high in fat intake leads to an increase in circulating SHBG, which limits the amount of biologically active testosterone circulating in the body (16). Reductions in biologically active testosterone are correlated to declines in physical performance (17). Additionally, over time, caloric deficits in conjunction with reductions in testosterone may impact the hypothalamic-pituitary-thyroid axis (HPTA) further affecting health and physical performance (1). Therefore, prolonged exposure to a high training load in combination with an inadequate nutritional intake could challenge the ability of the system to maintain a healthy hormonal balance and this may lead to overtraining syndrome. To ensure military readiness and operational effectiveness it would be prudent that preventative or mitigating measures be taken to maintain or enhance physical performance and reduce susceptibility to overtraining syndrome. Thus, the purpose of this study was to objectively determine the current prevalence of overtraining syndrome symptoms signs (i.e. hormonal balance) in elite military warfighters and to evaluate any nutritional factors that may influence overtraininghormonal balance. Based on the lifestyle and demands of the work being performed, Wwe hypothesized that there would be a high prevalence of hormonal imbalance, namely: elevated cortisol and depressed testosterone
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concentrations. In addition, we postulated that factors associated with caloric balance and macronutrient intake would influence biomarkers reflective of overtraining.
METHODS Participants. Participants were recruited from naval bases in the San Diego, CA area. All participants (n = 65) were healthy, active duty, male, U.S. naval operators between the ages of 21-51 years old (Table 1). All participants were actively engaged in rigorous physical fitness training regimens, which typically consisted of ≥ 6 hr/day of physical activity including: 1-3 hr/day of aerobic activity (> 50% VO2 peak), ≥ 1.5 hr/day resistance training (> 75% 1-RM) in addition to ≥ 3 hr/day of tactical training (18, 19). Subject enrollment was restricted to those whom had just completed an administration week (a week in which typical work involves desk duties and paperwork); therefore, while physical fitness training was very high, the influence of highly intensive job training and/or sleep deprivation due to duties was minimized. The participants were instructed to maintain their regularly scheduled training exercises as well as their dietary intake, including caffeine, nicotine, and alcohol consumption during the duration of this study. All subjects provided written and verbal consent to take part in the research study. This study was approved by the Institutional Review Board of the Naval Health Research Center and adhered to the Department of the Navy human research protection policies (Protocol No. NHRC.2012.0011); all participants gave their free and informed written consent. Data Collection Timeline. Data collections occurred over the course of 7 calendar days (Monday – Sunday). Anthropometric, health history questionnaires and fasted blood draws occurred at the on the first day of each subject’s recording week (Monday), between 0700 – 0900
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hrs. Following the blood draw, a randomized sample of subjects (n = 23) were provided a food log and individual instruction on how to complete dietary recall. Demographic and Anthropometric Assessment. During the first visit to the lab, subjects completed a basic health history questionnaire and anthropometric data were recorded (Table 1). Height and weight for each subject were recorded to the nearest 0.1 cm and 0.05 kg, respectively, using a digital scale with height rod (ProMed 6129, Detecto, Webb City, MO). Sampling and Blood Analyses. At the beginning of each subject’s recording week, whole blood (8 mL) was collected in tubes coated with the anti-coagulant Ethylenediaminetetraacetic acid (EDTA). The samples were centrifuged at 1000 × g for 15 minutes; plasma was then aliquoted into individually labeled microcentrifuge tubes, frozen and stored at -80°C for future analysis. All plasma samples were batch analyzed in duplicate for Total Testosterone (TT), Free Testosterone (FT), Cortisol, Triiodothryonine (T3), Thyroxine (T4), Thyroid Stimulating Hormone (TSH), and Luteinizing Hormone (LH) (TE187S, FT178S, CO103S, T3S5141, T4224T, TS227T, and LH231F, respectively; Calbiotech, San Diego, CA); as well as, Sex Hormone-Binding Globulin (SHBG; RAB0734; Sigma-Aldrich, Saint Louis, MO) and 17βEstradiol (E2; ADI-900-008; Enzo Life Sciences Inc.; Farmingdale, NY) via enzyme-linked immunosorbent assay (ELISA). Intra-assay (and inter-assay) variances were 2.13(6.41), 3.80(7.43), 3.14(4.21), 10.0(11.22), 3.83(5.66), 4.74(7.38), 5.53(8.91), 2.60(5.44), and 6.89(10.74)% for TT, FT, Cortisol, T3, T4, TSH, LH, SHBG and E2, respectively. Assay sensitivities were 0.35 nmol·L-1, 0.87 pmol·L-1, 55.2 nmol·L-1, 50.0 ng·dL-1, 2.0 µg·dL-1, 0.5 mIU·L-1, 3.1 IU·L-1, 0.001 nmol·L-1, and 28.5 pg·mL-1 for TT, FT, Cortisol, T3, T4, TSH, LH, SHBG and E2, respectively.
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Nutritional Analysis. A subset of subjects (n = 23) were instructed to complete a dietary recall for seven days following blood collection. The subjects recorded all food, nutrient, and liquid intake over the course of the week-long recording period. Data from the food logs were entered into a nutritional software program (Food Processor, EHSA, Salem, OR) which assessed the macro- and micro-nutrient content of the subjects’ diet. Metabolic Calculations. Basal metabolic rate was estimated using the Harris-Benedict equation (BMR [kcals] = 88.362 + (13.397 x weight in kg) + (4.799 x height in cm) - (5.677 x age in years)) (20). The Harris-Benedict BMR values were used to calculate the energy expenditure associated with heavy physical activity (PA) for each subject (PA = BMR x 0.6). Due to the nature of the subjects’ intense training, heavy activity was chosen as the factor for PA (PA factor: 0.6). The thermic effect of food (TEF) was calculated using the calculated BMR and PA for each respective subject (TEF = (BMR + PA) x 0.1). The total energy expenditure (TEE) was calculated as the summation of each subject’s BMR, PA, and TEF. Values are reported as daily caloric expenditures (kcals · day-1). Statistical Analyses. Statistical analyses were performed using SPSS software (IBM; SPSS v.23; Chicago, IL). For parametric data sets, the square of Pearson’s Product Moment coefficient was used to determine the significance of correlation between lifestyle factors (e.g. time in service and nutritional intake) and biochemical measures (TT, FT, Cortisol, T3, T4, TSH, LH, SHBG, and E2). For nonparametric data sets, Spearman’s rho was used to determine the significance of correlation. Furthermore, those with lower than normal testosterone levels (LT; < 10.4 nmol · L-1) and those with normal testosterone levels (non-LT; > 10.4 nmol · L-1) were grouped and comparisons between the groups were completed using independent sample t-tests. To quantify the magnitude of the differences between LT and non-LT groups, the size of each
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effect, expressed as a standardized mean difference (Hedge’s g), were calculated for each comparison, using the non-LT group as the contrast group. Following traditional conventions, interpretations of effects are as follows: 0.20 as small, 0.50 as medium, and ≥ 0.80 as large. Statistical significance was accepted when P < 0.05. All data are expressed as mean ± standard error of the mean (SE).
RESULTS Hormone Concentrations. The mean TT, FT, cortisol, T3, T4, TSH, LH, and SHBG plasma concentrations are reported in Table 2 and Figures 1A-D and 2A-C. Close to half of the operators (43%, n= 28) participating in this research effort had TT levels below the clinically defined threshold for low-testosterone syndrome (LTS), as defined by the Endocrine Society, as total testosterone < 10.4 nmol · L-1 (21). E2 concentrations were below the minimum detectable value of the assay kit (< 29.5 pg · mL-1) in all subjects. The mean molar ratio of TT to cortisol was 0.035 ± 0.002, which is at the threshold for overtraining/overreaching status (22). When the sample was dichotomized based on total testosterone levels (i.e. LT and nonLT) there were significant differences observed for multiple parameters. As expected, total testosterone levels were significantly different between the LT and non-LT groups (8.2 ± 0.3 vs. 17.6 ± 1.3 nmol · L-1, LT vs non-LT respectively; P < 0.001; g = -1.41; Figure 1B). Free testosterone was also significantly different between LT and non-LT groups (24.3 ± 1.9 vs. 31.1 ± 1.4 pmol · L-1, LT vs non-LT respectively; P = 0.004; g = -0.72; Figure 1C). Cortisol was significantly lower in the LT group (367.4 ± 39.1) compared to the non-LT group (497.2 ± 33.3 nmol · L-1; P = 0.014; g = -0.63; Figure 1D). Similarly, T3 was different between the LT and non-LT groups (121.1 ± 5.4 vs. 163.2 ± 14.5 ng · dL-1, LT vs non-LT respectively; P = 0.010; g
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= -0.60; Figure 2B). The ratio of total testosterone to cortisol was significantly lower in the LT group (0.028 ± 0.002) compared to the non-LT group (0.040 ± 0.004; P = 0.011; g = -0.65). There were no other significant hormonal differences observed between the LT and non-LT groups. Metabolic and Nutritional Parameters. Metabolic and nutritional data are provided in Tables 3 and 4. Total energy expenditure averaged 3382.0 ± 25.4 kcals · day-1 with basal metabolic rate and physical activity contributing 56.8% and 34.1%, respectively. Mean caloric intake was calculated using the data provided by the food logs (n = 23) and averaged 2587.8 ± 144.2 kcals · day-1; which corresponds to a net caloric balance of -813.1 ± 144.2 kcals · day-1. Protein, carbohydrate, and fat intake represented 21.5 ± 1.2%, 40.1 ± 1.9%, and 36.8 ± 1.3% of the total daily energy intake, respectively. To assess the impact of low testosterone on metabolic and nutritional factors, the subject pool was divided into one of two groups: low-testosterone (LT, n = 12) or non-LT (n = 11). Energy expenditure and macronutrient intake parameters were not different between groups except for a 28.8% higher PRO/FAT macronutrient ratio in the LT group when compared to the non-LT group (P = 0.041; g = 0.87; Table 5). Correlative analysis showed that total testosterone concentration was positively correlated with cortisol concentration (Figure 3; R² = 0.07; P = 0.038) and free testosterone (R² = 0.31; P < 0.001). Positive correlations were also observed between SHBG concentration and energy balance (Figure 4; R² = 0.18; P = 0.044; n = 23) as well as between SHBG concentration and total fat intake (kcals · day-1; Table 6; R² = 0.19; P = 0.038; n = 23) and saturated fat intake (grams · day-1; Table 6; R2 = 0.20; P = 0.032; n = 23). Relative daily fat intake (% of total daily EI) was positively correlated with cortisol concentration (Table 6; R² = 0.19; P = 0.038; n = 23). To assess the impact of time in service on overtraining/overreaching, we performed correlative
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analysis between the molar ratio of TT to cortisol and time in service and found no correlation between these two factors (R2 = 0.0039; P > 0.05; n = 23). No other correlations were found.
DISCUSSION The main finding of this study was the high prevalence of hormonal abnormalities in elite tactical athletes; namely, that 43% of the operators presented with lower than normal levels of testosterone, as defined by the Endocrine Society’s guidelines (21). Second, in contrast to previous work examining athletes, testosterone was positively correlated with cortisol in this population of highly trained healthy subjects (9, 23). The participants also displayed hormonal variations that are often present during overtraining syndrome including elevated SHBG (22). In addition, our data support the notion that nutritional intake may be an important determining factor in the development of hormonal imbalances (15, 16). Testosterone levels have been shown to decrease over time during short-term military training that includes high levels of physical activity and that is associated with inadequate nutritional intake (3, 5, 12, 24). Participation in three weeks of Army Officer Candidate School resulted in a significant decrease in plasma testosterone; however, the mean testosterone concentrations remained above the clinical definition of LTS (12). Conversely, subjects completing the Army Ranger training course, an 8-week long intense selection course for Army special operations, were found to have a significant decrease in circulating testosterone to the point that the average for all subjects was below the threshold for LTS (1, 3, 21). The participants in our study were a cross-sectional sample of elite naval operators, with daily training regimens that are similar to those of the Army Rangers; however, the subjects in our study had already completed on average 7.7 ± 0.9 years of elite military training, which is much
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longer than the 8-week long selection course completed in the Army Ranger studies (3, 24). While it would be tempting to speculate that training duration might be a factor in the development of low testosterone, plasma testosterone concentrations were not correlated with age or time as an operator in our study. This suggests that while high-intensity military training, even as short as three weeks (12), can negatively impact circulating testosterone levels, military training programs of longer (i.e. Army Ranger School) durations do not necessarily result in a sustained reduction in testosterone levels, as observed by Henning et al. when testosterone levels rebounded to pre-training levels within 2-6 weeks of the training stimulus removal (24). In contrast with our results, the previous studies examining Army training demonstrated that the decrease in basal testosterone concentration was associated with a concomitant rise in circulating cortisol concentration (1, 3, 12). These findings are in line with others which found that glucocorticoids (i.e. cortisol) depress testosterone production (9, 25); conversely, our results indicate that there was a positive correlation between cortisol and testosterone concentrations in our subjects. Our data suggest that in subjects undergoing daily physical training over a prolonged duration, cellular adaptations may occur that mitigate the deleterious effects of elevated cortisol on testosterone production. In fact, much like others examining long distance runners or endurance athletes (26)It is also important to note that despite having low levels of testosterone, the subjects in our study were able to train and perform at high exercise intensity levels suggesting either an adaptation to the reduced testosterone levels or a higher uptake of testosterone by androgen receptors in some of the individuals tested. Sometimes used as an indicator of overtraining, the testosterone-to-cortisol ratio is a measure of the anabolic and catabolic status of the individual (6). Testosterone acts as an indicator of anabolism, whereas, cortisol acts as an indicator of catabolism. In those that are
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overtraining, it is expected that cortisol levels will be elevated, whereas, testosterone levels will be reduced; this holds true for most individuals. In general, there is a negative correlation between testosterone and cortisol; during states of anabolism testosterone is high and cortisol is low and during catabolism testosterone is low and cortisol is high. In our participants, testosterone and cortisol were positively correlated, suggesting that an adaptation occurred that allowed the participants to maintain testosterone during times of catabolism to mitigate any consequences. Overtraining is found in new Army Officer Candidates (12); but, perhaps given enough time these subjects would have physiologically adapted like our participants to have a positive correlation between the testosterone and cortisol. During times of negative caloric balance, such as that experienced in intense military training, there are alterations in the hypothalamic-pituitary-thyroid axis (HPTA) and some changes may be mediated by testosterone. In male rats, sustained testosterone reductions are implicated in the fasting induced suppression of TSH; however, exogenous testosterone administration to male rats with low testosterone was shown to increase TSH levels (276). Further studies conducted in human military members, during military training, demonstrated that reductions in testosterone are accompanied by a decrease in TSH, T4, and T3 (3, 287); in these studies, the changes in thyroid hormones were attributed to increased physical strain and a caloric deficit. Therefore, it is well established that a caloric deficit alters the HPTA potentially in an effort to reduce metabolic rates and preserve vital functions during perceived starvation. However, as indicated by the data of this study, TSH, T3, and T4 levels remained in the “normal” range for healthy adults and was not different between subjects with low testosterone and those with testosterone levels in the normal range. These thyroid concentrations, indicate that either caloric balance is being maintained; or that despite a negative caloric balance, thyroid
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functioning has adapted to maintain levels within a normal range for thyroid hormones. Based upon the dietary recall data (n = 23), our subjects trained at a caloric deficit of 813.1 ± 144.2 kcals · day-1; however, their mean TSH was 4.4 ± 1.5 mIU · L-1, which is within the normal range. These findings suggest that despite low-testosterone levels and a caloric deficit thyroid function is maintained. Another possibility, while unlikely due to normal temperatures (San Diego, CA), would be that the subjects are maintaining thyroid hormones despite a caloric deficit to maintain thermoregulation during cold exposure (298). It is well known that caloric deficits, particularly those sustained over time, lead to alterations in sex-hormone concentrations, such as depressed TT and increased SHBG levels (30). T However, in this brief snapshot of time, these results do not directly indicate that there is a link between caloric balance and gonad, thyroid, and adrenal hormone concentrations for those engaged in a rigorous military physical training program. Indeed, there were no correlations between caloric balance and hormone concentrations; howevernonetheless, macronutrient intake was correlated to hormone concentrations. Herein, we add to the body of knowledge on the impact of nutrient intake and hormonal balance by demonstrating that the relative distribution of macronutrient intake also plays an important role in determining the hypothalamic-pituitarygonadal axis (HPGA) and hypothalamic-pituitary-adrenal axis (HPAA) hormone status of highly trained individuals. Previous research has shown that testosterone levels are negatively correlated with protein intake and positively correlated with fat intake in healthy trained male subjects (15). Other correlative and experimental studies have shown that a diet with a high PRO/CHO macronutrient ratio depresses testosterone levels (15, 3029, 310). Our results show that in our population of highly trained individuals, the relative intake of protein and fat may play a more important role than the PRO/CHO ratio, as indicated by previous reports in healthy physically
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active male subjects (3029, 310). Interestingly, unlike other studies (15, 321, 332), our results indicate that dietary fat composition (i.e. SFA, MUFA, PUFA, PUFA/SFA ratio) is not influential on testosterone levels. It is possible that the differences observed between studies are due to variations in physical training workload of the subject populations. The subjects of the current study were physically active for much longer durations and at higher exercise intensities than the recreational athletes examined in the aforementioned studies. Our data also suggest that macronutrient intake plays a role in other biomarkers implicated in the regulation of testosterone production, namely cortisol and SHBG. The present results indicate that there is a positive correlation between fat intake (as a percentage of average daily total energy intake) and cortisol which is in stark contrast to findings by Martens et al. (2010) who found that cortisol decreases in response to fat intake (343). As opposed to previous findings, SHBG was also found to be positively correlated with energy balance, fat intake, and SFA intake (354). In combination with decreasing testosterone, this increase in SHBG over time is suggestive of the presence of overtraining syndrome (2, 22, 365, 376). Our HPGA and HPAA hormone data also indicate that this group of subjects presented with several of the physiological characteristics associated with physical overtraining/overreaching (22); however, our data also show that the non-LT subjects exhibited adaptations that would provide enhanced resiliency to the normal stress response. This is made evident due to the positive correlation between cortisol and testosterone in the non-LT group; these results are in contrast to previous findings which indicate that high levels of circulating cortisol negatively correlate to circulating levels of testosterone (10, 12) and that cortisol administration (endogenous/exogenous) directly reduces testosterone production (without affecting follicle stimulating hormone and luteinizing hormone) (11). To add to this
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unanticipated finding, comparisons between the oldest subjects (≥ 35 yrs) and the youngest subjects (< 35 yrs) failed to demonstrate any differences in any of the hormones measured. In fact, the oldest subject (51 yrs of age; > 30 yrs of service; 12 deployments) had total testosterone (12.5 nmol · L-1) and all other measured hormones fell within the normal range for an adult male. This begs the question – what is causing hormonal abnormalities, particularly in the HPGA, to occur in a large percentage of elite tactical athletes, but not others? The answer is likely multifactorial and likely includes both nutrition and rest, as well other factors not assessed in the current study. Thus, further investigations into the mechanisms responsible for hormonal imbalances and determination if hormonal imbalances are preexisting (prior to service) or occur as a result of service is warranted.
LIMITATIONS This study is not without limitations. The primary limitation is that this study is crosssectional in design and only captures a single time point for each operator. While the crosssectional design does provide valuable information regarding the state of operators across ages and time in service, it fails to indicate whether or not individuals had preexisting LT prior to service. Therefore, it would be prudent to investigate the hormonal balance in operators from the beginning of their service to the end of service and beyond to determine what role, if any, elite military training and operations have on hormonal balance. Other limitations include: undiagnosed preexisting medical conditions, genetics, unknown family stress (including fatherhood), sleep health, and financial situation, among other factors.
CONCLUSION
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In summary, this study found that of 65 elite tactical athletes (operators) assessed, 43% displayed testosterone levels below the threshold for LTS (21). These athletes also displayed abnormally high levels of SHBG and some displayed high resting levels of cortisol, both hallmarks of overtraining syndrome. Interestingly enough, there was a weak positive correlation between testosterone and cortisol, indicating that those who may be experiencing the most stress are also the most adept at maintaining hormonal balance. The present findings indicate that elite tactical athletes are highly stressed; however, some may have developed or been born with coping mechanisms to maintain satisfactory performance and hormonal balance.
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Figure Legends – Figure 1A – D. Concentrations of sex and stress hormones stratified by testosterone grouping in United States Naval Operators. Participants were split into two groups, those with low-testosterone (LT: total testosterone <10.4 nmol · L-1) and those with normal testosterone (Non-LT: total testosterone ≥10.4 nmol · L-1). Baseline concentrations of Luteinizing Hormone (A), Total Testosterone (B), Free Testosterone (C), and Cortisol (D) for each participant were measured and stratified by group (LT vs. Non-LT). Each grey circle represents one participant’s values and the black bar is the mean concentration for each group. The hash marked box in-line with the y-axis denotes the normal range for each hormone assessed, as determined by the Endocrine Society (37); the reference range for Free Testosterone is outside the range of values depicted within Figure 1C. † denotes significant difference from LT group (P < 0.05). N = 65; LT: n = 28; Non-LT: n = 37. Figure 2A – C. Concentrations of thyroid hormones stratified by testosterone grouping in United States Naval Operators. Participants were split into two groups, those with lowtestosterone (LT: total testosterone <10.4 nmol · L-1) and those with normal testosterone (NonLT: total testosterone ≥10.4 nmol · L-1). Baseline concentrations of Thyroid Stimulating Hormone (A), Triiodothyronine (B), and Thyroxine (C) for each participant were measured and stratified by group (LT vs. Non-LT). Each grey circle represents one participant’s values and the black bar is the mean concentration for each group. The hash marked box in-line with the y-axis denotes the normal range for each hormone assessed, as determined by the Endocrine Society (37). † denotes significant difference from LT group (P < 0.05). N = 65; LT: n = 28; Non-LT: n = 37. Figure 3. Correlation between Cortisol Concentration and Total Testosterone Concentration. Each black diamond represents one individual’s Cortisol and Total testosterone values. The dashed line represents the clinically defined threshold for LT, total testosterone <10.4 nmol · L-1 (21). R² = 0.07; P < 0.05; n = 65.
Hormonal balance in elite tactical athletes 19
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Hormonal balance in elite tactical athletes 20
16. Adlercreutz H. Western diet and Western diseases: some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Invest Suppl. 1990;201:3-23. PubMed PMID: 2173856. 17. Flynn MG, Pizza FX, Boone JB, Andres FF, Michaud TA, Rodriguez-Zayas JR. Indices of training stress during competitive running and swimming seasons. Int J Sports Med. 1994;15(1):21-6. doi: 10.1055/s-2007-1021014. PubMed PMID: 8163321. 18. Prusaczyk WK, Goforth Jr HW, Nelson MS. Physical Training Activities of East Coast US Navy SEALs. DTIC Document; 1994. 19. Prusaczyk WK, Stuster JW, Goforth Jr HW, Smith TS, Meyer LT. Physical Demands of US Navy Sea-Air-Land (SEAL) Operations. DTIC Document; 1995. 20. Roza AM, Shizgal HM. The Harris Benedict equation reevaluated: resting energy requirements and the body cell mass. Am J Clin Nutr. 1984;40(1):168-82. PubMed PMID: 6741850. 21. Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, et al. Testosterone therapy in men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2010;95(6):2536-59. doi: 10.1210/jc.2009-2354. PubMed PMID: 20525905. 22. Tanskanen MM, Kyröläinen H, Uusitalo AL, Huovinen J, Nissilä J, Kinnunen H, et al. Serum sex hormone-binding globulin and cortisol concentrations are associated with overreaching during strenuous military training. J Strength Cond Res. 2011;25(3):787-97. doi: 10.1519/JSC.0b013e3181c1fa5d. PubMed PMID: 20543745. 23. Anderson T, Lane AR, Hackney AC. Cortisol and testosterone dynamics following exhaustive endurance exercise. Eur J Appl Physiol. 2016;116(8):1503-9. Epub 2016/06/04. doi: 10.1007/s00421-016-3406-y. PubMed PMID: 27262888. 24. Henning PC, Scofield DE, Spiering BA, Staab JS, Matheny RW, Smith MA, et al. Recovery of endocrine and inflammatory mediators following an extended energy deficit. J Clin Endocrinol Metab. 2014;99(3):956-64. doi: 10.1210/jc.2013-3046. PubMed PMID: 24423293. 25. Bambino TH, Hsueh AJ. Direct inhibitory effect of glucocorticoids upon testicular luteinizing hormone receptor and steroidogenesis in vivo and in vitro. Endocrinology. 1981;108(6):2142-8. doi: 10.1210/endo-108-6-2142. PubMed PMID: 6262050. 26. Hooper DR, Kraemer WJ, Saenz C, Schill KE, Focht BC, Volek JS, et al. The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition. Eur J Appl Physiol. 2017;117(7):1349-57. Epub 2017/05/05. doi: 10.1007/s00421017-3623-z. PubMed PMID: 28470410. 276. Cohen JH, Alex S, DeVito WJ, Braverman LE, Emerson CH. Fasting-associated changes in serum thyrotropin in the rat are influenced by gender. Endocrinology. 1989;124(6):3025-9. doi: 10.1210/endo-124-6-3025. PubMed PMID: 2721456. 287. Opstad PK, Falch D, Oktedalen O, Fonnum F, Wergeland R. The thyroid function in young men during prolonged exercise and the effect of energy and sleep deprivation. Clin Endocrinol (Oxf). 1984;20(6):657-69. PubMed PMID: 6432374. 298. Stroud MA, Ritz P, Coward WA, Sawyer MB, Constantin-Teodosiu D, Greenhaff PL, et al. Energy expenditure using isotope-labelled water (2H218O), exercise performance, skeletal muscle enzyme activities and plasma biochemical parameters in humans during 95 days of endurance exercise with inadequate energy intake. Eur J Appl Physiol Occup Physiol. 1997;76(3):243-52. PubMed PMID: 9286604.
Hormonal balance in elite tactical athletes 21
3029. Anderson KE, Rosner W, Khan MS, New MI, Pang SY, Wissel PS, et al. Diet-hormone interactions: protein/carbohydrate ratio alters reciprocally the plasma levels of testosterone and cortisol and their respective binding globulins in man. Life Sci. 1987;40(18):1761-8. PubMed PMID: 3573976. 310. Kappas A, Anderson KE, Conney AH, Pantuck EJ, Fishman J, Bradlow HL. Nutritionendocrine interactions: induction of reciprocal changes in the delta 4-5 alpha-reduction of #
Role
Definition Dr Karen Kelly – lead 1 Conceptualization Dr Andrew Jensen – supporting Dr Andrew Jensen – equal 2 Data curation Ms Laura Arrington – equal 3 Formal analysis Dr Andrew Jensen – lead 4 Funding acquisition Dr Karen Kelly – lead Dr Karen Kelly – equal Dr Andrew Jensen – equal 5 Investigation Ms Laura Arrington – equal Dr Andrew Jensen – equal 6 Methodology Dr Karen Kelly – equal testosterone and the cytochrome P-450-dependent oxidation of estradiol by dietary macronutrients in man. Proc Natl Acad Sci U S A. 1983;80(24):7646-9. PubMed PMID: 6584878; PubMed Central PMCID: PMCPMC534397. 321. Sebokova E, Garg ML, Wierzbicki A, Thomson AB, Clandinin MT. Alteration of the lipid composition of rat testicular plasma membranes by dietary (n-3) fatty acids changes the responsiveness of Leydig cells and testosterone synthesis. J Nutr. 1990;120(6):610-8. PubMed PMID: 2352035. 332. Sebokova E, Wierzbicki A, Clandinin MT. Modulation of rat testes lipid composition by hormones: effect of PRL and hCG. Am J Physiol. 1988;255(4 Pt 1):E442-8. PubMed PMID: 2845800. 343. Martens MJ, Rutters F, Lemmens SG, Born JM, Westerterp-Plantenga MS. Effects of single macronutrients on serum cortisol concentrations in normal weight men. Physiol Behav. 2010;101(5):563-7. Epub 2010/09/16. doi: 10.1016/j.physbeh.2010.09.007. PubMed PMID: 20849868. 354. Longcope C, Feldman HA, McKinlay JB, Araujo AB. Diet and sex hormone-binding globulin. J Clin Endocrinol Metab. 2000;85(1):293-6. doi: 10.1210/jcem.85.1.6291. PubMed PMID: 10634401. 365. Busso T, Häkkinen K, Pakarinen A, Kauhanen H, Komi PV, Lacour JR. Hormonal adaptations and modelled responses in elite weightlifters during 6 weeks of training. Eur J Appl Physiol Occup Physiol. 1992;64(4):381-6. PubMed PMID: 1592066. 376. Häkkinen K, Pakarinen A, Alen M, Kauhanen H, Komi PV. Neuromuscular and hormonal adaptations in athletes to strength training in two years. J Appl Physiol (1985). 1988;65(6):2406-12. PubMed PMID: 3215840. 387. Endocrine self-assessment program 2016. Washington, D.C., DC: Endocrine Society; 2016.
Hormonal balance in elite tactical athletes 22
Dr Karen Kelly – lead Project administration Dr Andrew Jensen – supporting Ms Laura Arrington – supporting Dr Lorraine Turcotte – equal 8 Resources Dr Karen Kelly – equal Dr Andrew Jensen – lead 9 Software Ms Laura Arrington – supporting Dr Lorraine Turcotte – equal 10 Supervision Dr Karen Kelly – equal Dr Andrew Jensen – equal 11 Validation Dr Lorraine Turcotte – equal Dr Karen Kelly – equal Dr Andrew Jensen – lead 12 Visualization Ms Laura Arrington – supporting Writing – original Dr Andrew Jensen – lead 13 Dr Lorraine Turcotte – supporting draft Dr Andrew Jensen – lead Writing – review & Dr Lorraine Turcotte – supporting 14 editing Dr Karen Kelly - supporting Contributor Roles Taxonomy (CRediT) 7
Hormonal balance and nutritional intake in elite tactical athletes Andrew E. Jensen, PhD; Laura J. Arrington, MS; Lorraine P. Turcotte, PhD; Karen R. Kelly, PhD.
Figure 1A.
Figure 1B.
10
45
9
40
8
Total Testosterone (nmol · L-1)
Luteinizing Hormone (IU · L-1)
Hormonal balance in elite tactical athletes 23
7 6 5 4 3 2
LT
30 25 20 15 10
0
Non-LT
Figure 1C.
1400
†
Non-LT
†
1200 Cortisol (nmol · L-1)
60 50 40 30
1000 800 600
20
400
10
200
0
LT
Figure 1D.
70
Free Testosterone (pmol · L-1)
35
5
1 0
†
LT
Non-LT
0
LT
Non-LT
Hormonal balance in elite tactical athletes 24
Figure 2B.
30
600
25
500 Triiodothyronine (ng · dL-1)
Thyroid Stimulating Hormone (mIU · L-1)
Figure 2A.
20
15
10
5
0
LT
Non-LT
LT
Non-LT
16 14 12 Thyroxine (µg · dL-1)
400
300
200
100
Figure 2C.
10 8 6 4 2 0
†
0
LT
NonLT
Hormonal balance in elite tactical athletes 25
Table 1. Physical Characteristics of United States Naval Operators Baseline
(Range)
Age, yrs
29.9 ± 0.9
(21 – 51)
Height, cm
178.4 ± 0.7
(162.6 – 188.0)
Weight, kg
85.1 ± 0.9
(72.0 – 110.9)
BMI, kg · m-2
26.7 ± 0.3
(23.7 – 37.2)
Time as Operator, yrs
7.7 ± 0.9
(0.2 – 32.6)
Deployments, #
3.0 ± 0.5
(0 – 13)
Values presented as Mean ± SE. n = 65.
Table 2. Concentrations of Sex, Stress and Thyroid Hormones in United States Naval Operators Baseline
(Range)
Normal Range*
Free Testosterone, pmol · L-1
28.2 ± 1.2
(15.1 – 60.1)
310.0 – 1040.0
Total Testosterone, nmol · L-1
13.5 ± 0.9
(5.9 – 40.5)
10.4 – 41.6
SHBG, nmol · L-1
94.2 ± 6.4
(32.2 – 171.5)
10.0 – 60.0
441.3 ± 26.4
(141.4 – 1154.9)
137.9 – 689.7
3.4 ± 0.2
(0.2 – 9.2)
1.0 – 9.0
145.9 ± 9.0
(42.0 – 546.0)
70.0 – 200.0
Thryoxine, µg · dL-1
7.8 ± 0.2
(4.5 – 14.3)
5.5 – 12.5
Thyroid Stimulating Hormone, mIU · L-1
3.5 ± 0.7
(0.2 – 28.4)
0.5 – 5.0
Total Testosterone / Cortisol, molar ratio
0.035 ± 0.002
(0.008 – 0.127)
Cortisol, nmol · L-1 Luteinizing Hormone, IU · L-1 Triiodothryronine, ng · dL-1
Values presented as Mean ± SE. n = 65. *As determined by the Endocrine Society (37).
Table 3. Metabolic Characteristics of United States Naval Operators Baseline
(Range)
BMR, kcals · day-1
1921.6 ± 14.4
(1674.6 – 2191.7)
PA, kcals · day-1
1153.0 ± 8.7
(1004.8 – 1315.0)
Hormonal balance in elite tactical athletes 26
TEF, kcals · day-1
307.5 ± 2.3
(267.9 – 350.7)
TEE, kcals · day-1
3382.0 ± 25.4
(2947.3 – 3857.4)
Values presented as Mean ± SE. BMR: basal metabolic rate. PA: physical activity. TEF: thermic effect of food. TEE: total energy expenditure. All values were calculated via Harris-Benedict Equation as described in the methods. n = 65.
Table 4. Nutritional Characteristics of Energy Intake in United States Naval Operators Baseline
(Range)
EI, kcals · day-1
2587.8 ± 144.2
(1230.3 – 3744.5)
Energy Balance, kcals · day-1
-813.1 ± 144.2
(-2415.8 – +374.6)
548.1 ± 36.7
(271.6 – 931.9)
1048.13 ± 85.4
(489.9 – 2013.1)
Fat, kcals · day-1
945.7 ± 56.6
(427.5 – 1538.4)
Alcohol, kcals · day-1
113.5 ± 38.5
(23.4 – 520.3)
Fiber, g · day-1
26.1 ± 2.8
(8.9 – 60.1)
SFA, g · day-1
32.7 ± 1.9
(14.0 – 46.6)
MUFA, g · day-1
21.0 ± 3.1
(1.4 – 56.4)
PUFA, g · day-1
9.1 ± 1.4
(0.6 – 25.5)
Cholesterol, mg · day-1
550.2 ± 53.6
(162.9 – 958.0)
Vitamin D, mcg · day-1
6.5 ± 2.3
(0.1 – 41.9)
Magnesium, mg · day-1
273.1 ± 39.4
(19.6 – 693.9)
11.6 ± 2.1
(0.7 – 42.1)
Protein, kcals · day-1 Carbohydrates, kcals · day-1
Zinc, mg · day-1
Values presented as Mean ± SE. EI: Energy Intake. Energy Balance: EI – Total Energy Expenditure. SFA: Saturated fatty acids. MUFA: Mono-unsaturated fatty acids. PUFA: poly-unsaturated fatty acids. n = 23.
Table 5. Total Energy Expenditure and Macronutrient Intake Differences between LT and non-LT United States Naval Operators EI, kcals · day-1
LT (n= 12)
non-LT (n= 11)
2558.5 ± 228.7
2619.7 ± 180.9
Hormonal balance in elite tactical athletes 27
TEE, kcals · day-1
3417.4 ± 54.7
3382.8 ± 55.5
23.3 ± 2.0
19.6 ± 1.0
575.5 ± 56.6
518.3 ± 46.8
35.4 ± 1.9
38.4 ± 1.6
895.6 ± 83.8
1000.4 ± 75.6
39.9 ± 3.0
40.4 ± 2.4
1033.9 ± 136.7
1063.7 ± 105.2
PRO/CHO, ratio
0.65 ± 0.10
0.51 ± 0.05
PRO/FAT, ratio
0.67 ± 0.06*
0.52 ± 0.03
CHO/FAT, ratio
1.21 ± 0.15
1.08 ± 0.09
PRO, % EI kcals · day-1 FAT, % EI kcals · day-1 CHO, % EI kcals · day-1
Values presented as Mean ± SE. LT: Low Testosterone. Non-LT: “normal” total testosterone. TT: Total Testosterone. LT: TT <10.4 nmol · L-1 (21). non-LT: TT ≥ 10.4 nmol · L-1. EI: Energy Intake. TEE: Total Energy Expenditure. PRO: Protein. FAT: Fat. CHO: Carbohydrate. Macronutrient ratios were calculated using mean kcal · day-1 data. Macronutrient percent values were calculated as the percentage of average total energy intake per day. *P<0.05 vs. non-LT group. n = 23.
Table 6. Correlation coefficients between daily nutrient intake and sex hormone concentrations in United States Naval Operators FT
TT
Cortisol
SHBG
TT/Cortisol Ratio
Energy balance, kcals
-0.26
0.06
-0.07
0.42*
0.07
PRO, kcals
-0.04
-0.01
0.00
0.28
-0.10
PRO, EI%
0.16
-0.10
-0.02
-0.13
-0.17
CHO, kcals
-0.29
-0.01
-0.08
0.25
0.03
CHO, EI%
-0.23
-0.11
-0.20
0.03
0.08
FAT, kcals
-0.10
0.18
0.28
0.43*
-0.07
FAT, EI%
0.21
0.24
0.44*
0.13
-0.05
Alcohol, kcals
0.02
0.08
-0.15
-0.26
0.22
Fiber, g
-0.48
-0.10
0.03
0.22
-0.22
SFA, g
0.17
0.30
0.29
0.44*
0.12
MUFA, g
-0.19
0.17
0.25
0.32
-0.13
Hormonal balance in elite tactical athletes 28
PUFA, g
-0.20
0.25
0.30
0.40
-0.08
PUFA/SFA Ratio
-0.30
0.11
0.13
0.23
-0.13
PUFA/MUFA Ratio
-0.30
0.12
0.13
0.22
-0.13
Cholesterol, mg
0.36
0.14
0.15
0.32
-0.05
Vitamin D, mcg
-0.13
-0.01
-0.21
0.27
0.17
Magnesium, mg
0.10
0.08
-0.07
0.31
0.03
Zinc, mg
0.28
0.02
-0.20
0.18
0.19
Correlation coefficients are Pearson product-moment correlation. Macronutrient percent values were calculated as the percentage of average total energy intake per day. PRO: protein. CHO: carbohydrate. SFA: saturated fatty acids. MUFA: mono-unsaturated fatty acids. PUFA: poly-unsaturated fatty acids. FT: free testosterone. TT: total testosterone. SHBG: sex hormone-binding globulin. TT/Cortisol Ratio: molar ratio of total testosterone to cortisol. *Statistically significant correlation, P < 0.05. n = 23.
HIGHLIGHTS ● High prevalence of low testosterone was sampled in the elite tactical athletes. ● Weak positive correlation observed between testosterone and cortisol. ● Long-term elite military training affects the HPA, HPT, and HPG axes.
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Please cite this article as: Jensen, A.E., Arrington, L.J., Turcotte, L.P., Kelly, K.R., Hormonal balance and nutritional intake in elite tactical athletes, Steroids (2019), doi: https://doi.org/10.1016/j.steroids.2019.108504
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Hormonal balance in elite tactical athletes 1
Pages: 28 Words: 3987 Figures: 3 Tables: 6 References: 37 Contact: Karen Kelly Email: [email protected] Guarantor: Karen Kelly Hormonal balance and nutritional intake in elite tactical athletes Andrew E. Jensen, PhD1,2,3 Laura J. Arrington, MS1,2 Lorraine P. Turcotte, PhD3 Karen R. Kelly, PhD1,3 1Naval
Health Research Center Warfighter Performance Department 140 Sylvester Road San Diego, CA 92106 2Leidos
Inc. 10260 Campus Point Drive San Diego, CA 92121 3University
of Southern California Biological Sciences, Human and Evolutionary Biology Dornsife College of Letters, Arts and Sciences 3616 Trousdale Parkway, AHF 247 Los Angeles, CA 90089
I am a military service member (or employee of the U.S. Government). This work was prepared as part of my official duties. Title 17, USC, §105 provides the “Copyright protection under this title is not available for any work of the United States Government.” Title 17, USC, §101 defines a U.S. Government work as work prepared by a military service member or employee of the U.S. Government as part of that person’s official duties. This work was supported by Naval Special Warfare under work unit N1239.The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, nor the U.S. Government. The study protocol was approved by the Naval Health Research Center Institutional Review Board in compliance with all applicable Federal regulations governing the protection of human
Hormonal balance in elite tactical athletes 2
subjects. Research data were derived from an approved Naval Health Research Center, Institutional Review Board protocol number NHRC.2012.0011.
HIGHLIGHTS ● High prevalence of low testosterone was sampled in the elite tactical athletes. ● Weak positive correlation observed between testosterone and cortisol. ● Long-term elite military training affects the HPA, HPT, and HPG axes.Nutritional intake may influence hormonal imbalances in elite tactical athletes. KEYWORDS Military, androgen, stress, nutrition, thyroid, elite athletes
Hormonal balance in elite tactical athletes 3
ABSTRACT Chronic exposure to multifactorial stress, such as that endured by elite military operators, may lead to overtraining syndrome and negatively impact hormonal regulation. In acute settings (<6 mos), military training has been shown to lead to hormonal dysfunction; however, less is known about the consequences of long-term military training. Thus, the purpose of this study was to determine the chronic effects of military operations and training on the hormone profile of elite military operators. A cross-sectional, random sample of aActive duty elite US military operators (n = 65, age = 29.8 ± 1.0 yrs, height = 178.4 ± 0.7 cm, weight = 85.1 ± 2.0 kg) concomitantly engaged in rigorous physical training were recruited to participate in the study. Following an overnight fast, Wwaking plasma concentrations of luteinizing hormone, total testosterone (TT), free testosterone, sex-hormone binding globulin, cortisol, thyroid stimulating hormone, triiodothyronine, and thyroxine were obtained. Data were analyzed for correlations and compared against normative reference values. There was a significant positive correlation between TT and cortisol (R² = 0.07; P = 0.038). In addition, 43% of the participants (n = 28) had TT below age-based normative reference ranges. These results indicate that long-term military operations and training may place a large burden on the operators and depress or alter the hypothalamic pituitary, adrenal, gonadal, and thyroid axes. Further research need be conducted to determine what, if any, consequences these differences may cause.
Hormonal balance in elite tactical athletes 4
INTRODUCTION During times of enhanced multifactorial stress, such as that induced by military operations and training, hormonal balance may be impacted. Several factors have been shown to impact hormonal balance under stress conditions including training load and nutritional deficiencies (1-3). However, most studies have examined the effects of acute (< 8 weeks) military training operations on stress-related hormonal factors and they have shown that once the intense training stimulus is removed hormones return to baseline measures (3-5). There is, however, a dearth of information regarding the chronic and long-term hormonal and physiological consequences of intense physical and operational training in elite military communities. Chronic exposure to multifactorial stress, including training load and nutritional deficits, is associated with hormonal imbalances and may ultimately lead to overtraining syndrome (3, 6). Overtraining syndrome is generally characterized by reduced physical performance, increased fatigability, and subjective symptoms of stress (2). Some of the hormonal alterations shown to be responsible for these consequences include changes in the hypothalamic-pituitary-gonadal axis (HPGA) and the hypothalamic-pituitary-adrenal axis (HPAA) including: low testosterone, high cortisol, and high sex hormone-binding globulin (SHBG) (2, 6, 7). Testosterone deficiency with or without elevated cortisol levels is a well-accepted marker of overtraining (2, 7, 8). High cortisol levels have been correlated with low testosterone levels in over-trained athletes (9) and has been shown to inhibit testosterone production in both civilian and military men (10-12). In addition, there is a negative correlation during high intensity exercise between SHBG and
Hormonal balance in elite tactical athletes 5
testosterone, which may influence testosterone turnover and ultimately lead to other negative hormonal changes when high intensity exercise is performed daily (13). Improper nutritional intake has also been implicated in the development of overtraining syndrome and hormonal imbalance in those with high stress loads (1, 3, 14). In healthy resistance trained males there is a positive correlation between fat intake and testosterone levels and a negative correlation between protein intake and testosterone levels (15). This is supported by findings which indicate that a typical Western diet that is high in fat intake leads to an increase in circulating SHBG, which limits the amount of biologically active testosterone circulating in the body (16). Reductions in biologically active testosterone are correlated to declines in physical performance (17). Additionally, over time, caloric deficits in conjunction with reductions in testosterone may impact the hypothalamic-pituitary-thyroid axis (HPTA) further affecting health and physical performance (1). Therefore, prolonged exposure to a high training load in combination with an inadequate nutritional intake could challenge the ability of the system to maintain a healthy hormonal balance and this may lead to overtraining syndrome. To ensure military readiness and operational effectiveness it would be prudent that preventative or mitigating measures be taken to maintain or enhance physical performance and reduce susceptibility to overtraining syndrome. Thus, the purpose of this study was to objectively determine the current prevalence of overtraining syndrome symptoms signs (i.e. hormonal balance) in elite military warfighters and to evaluate any nutritional factors that may influence overtraininghormonal balance. Based on the lifestyle and demands of the work being performed, Wwe hypothesized that there would be a high prevalence of hormonal imbalance, namely: elevated cortisol and depressed testosterone
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concentrations. In addition, we postulated that factors associated with caloric balance and macronutrient intake would influence biomarkers reflective of overtraining.
METHODS Participants. Participants were recruited from naval bases in the San Diego, CA area. All participants (n = 65) were healthy, active duty, male, U.S. naval operators between the ages of 21-51 years old (Table 1). All participants were actively engaged in rigorous physical fitness training regimens, which typically consisted of ≥ 6 hr/day of physical activity including: 1-3 hr/day of aerobic activity (> 50% VO2 peak), ≥ 1.5 hr/day resistance training (> 75% 1-RM) in addition to ≥ 3 hr/day of tactical training (18, 19). Subject enrollment was restricted to those whom had just completed an administration week (a week in which typical work involves desk duties and paperwork); therefore, while physical fitness training was very high, the influence of highly intensive job training and/or sleep deprivation due to duties was minimized. The participants were instructed to maintain their regularly scheduled training exercises as well as their dietary intake, including caffeine, nicotine, and alcohol consumption during the duration of this study. All subjects provided written and verbal consent to take part in the research study. This study was approved by the Institutional Review Board of the Naval Health Research Center and adhered to the Department of the Navy human research protection policies (Protocol No. NHRC.2012.0011); all participants gave their free and informed written consent. Data Collection Timeline. Data collections occurred over the course of 7 calendar days (Monday – Sunday). Anthropometric, health history questionnaires and fasted blood draws occurred at the on the first day of each subject’s recording week (Monday), between 0700 – 0900
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hrs. Following the blood draw, a randomized sample of subjects (n = 23) were provided a food log and individual instruction on how to complete dietary recall. Demographic and Anthropometric Assessment. During the first visit to the lab, subjects completed a basic health history questionnaire and anthropometric data were recorded (Table 1). Height and weight for each subject were recorded to the nearest 0.1 cm and 0.05 kg, respectively, using a digital scale with height rod (ProMed 6129, Detecto, Webb City, MO). Sampling and Blood Analyses. At the beginning of each subject’s recording week, whole blood (8 mL) was collected in tubes coated with the anti-coagulant Ethylenediaminetetraacetic acid (EDTA). The samples were centrifuged at 1000 × g for 15 minutes; plasma was then aliquoted into individually labeled microcentrifuge tubes, frozen and stored at -80°C for future analysis. All plasma samples were batch analyzed in duplicate for Total Testosterone (TT), Free Testosterone (FT), Cortisol, Triiodothryonine (T3), Thyroxine (T4), Thyroid Stimulating Hormone (TSH), and Luteinizing Hormone (LH) (TE187S, FT178S, CO103S, T3S5141, T4224T, TS227T, and LH231F, respectively; Calbiotech, San Diego, CA); as well as, Sex Hormone-Binding Globulin (SHBG; RAB0734; Sigma-Aldrich, Saint Louis, MO) and 17βEstradiol (E2; ADI-900-008; Enzo Life Sciences Inc.; Farmingdale, NY) via enzyme-linked immunosorbent assay (ELISA). Intra-assay (and inter-assay) variances were 2.13(6.41), 3.80(7.43), 3.14(4.21), 10.0(11.22), 3.83(5.66), 4.74(7.38), 5.53(8.91), 2.60(5.44), and 6.89(10.74)% for TT, FT, Cortisol, T3, T4, TSH, LH, SHBG and E2, respectively. Assay sensitivities were 0.35 nmol·L-1, 0.87 pmol·L-1, 55.2 nmol·L-1, 50.0 ng·dL-1, 2.0 µg·dL-1, 0.5 mIU·L-1, 3.1 IU·L-1, 0.001 nmol·L-1, and 28.5 pg·mL-1 for TT, FT, Cortisol, T3, T4, TSH, LH, SHBG and E2, respectively.
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Nutritional Analysis. A subset of subjects (n = 23) were instructed to complete a dietary recall for seven days following blood collection. The subjects recorded all food, nutrient, and liquid intake over the course of the week-long recording period. Data from the food logs were entered into a nutritional software program (Food Processor, EHSA, Salem, OR) which assessed the macro- and micro-nutrient content of the subjects’ diet. Metabolic Calculations. Basal metabolic rate was estimated using the Harris-Benedict equation (BMR [kcals] = 88.362 + (13.397 x weight in kg) + (4.799 x height in cm) - (5.677 x age in years)) (20). The Harris-Benedict BMR values were used to calculate the energy expenditure associated with heavy physical activity (PA) for each subject (PA = BMR x 0.6). Due to the nature of the subjects’ intense training, heavy activity was chosen as the factor for PA (PA factor: 0.6). The thermic effect of food (TEF) was calculated using the calculated BMR and PA for each respective subject (TEF = (BMR + PA) x 0.1). The total energy expenditure (TEE) was calculated as the summation of each subject’s BMR, PA, and TEF. Values are reported as daily caloric expenditures (kcals · day-1). Statistical Analyses. Statistical analyses were performed using SPSS software (IBM; SPSS v.23; Chicago, IL). For parametric data sets, the square of Pearson’s Product Moment coefficient was used to determine the significance of correlation between lifestyle factors (e.g. time in service and nutritional intake) and biochemical measures (TT, FT, Cortisol, T3, T4, TSH, LH, SHBG, and E2). For nonparametric data sets, Spearman’s rho was used to determine the significance of correlation. Furthermore, those with lower than normal testosterone levels (LT; < 10.4 nmol · L-1) and those with normal testosterone levels (non-LT; > 10.4 nmol · L-1) were grouped and comparisons between the groups were completed using independent sample t-tests. To quantify the magnitude of the differences between LT and non-LT groups, the size of each
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effect, expressed as a standardized mean difference (Hedge’s g), were calculated for each comparison, using the non-LT group as the contrast group. Following traditional conventions, interpretations of effects are as follows: 0.20 as small, 0.50 as medium, and ≥ 0.80 as large. Statistical significance was accepted when P < 0.05. All data are expressed as mean ± standard error of the mean (SE).
RESULTS Hormone Concentrations. The mean TT, FT, cortisol, T3, T4, TSH, LH, and SHBG plasma concentrations are reported in Table 2 and Figures 1A-D and 2A-C. Close to half of the operators (43%, n= 28) participating in this research effort had TT levels below the clinically defined threshold for low-testosterone syndrome (LTS), as defined by the Endocrine Society, as total testosterone < 10.4 nmol · L-1 (21). E2 concentrations were below the minimum detectable value of the assay kit (< 29.5 pg · mL-1) in all subjects. The mean molar ratio of TT to cortisol was 0.035 ± 0.002, which is at the threshold for overtraining/overreaching status (22). When the sample was dichotomized based on total testosterone levels (i.e. LT and nonLT) there were significant differences observed for multiple parameters. As expected, total testosterone levels were significantly different between the LT and non-LT groups (8.2 ± 0.3 vs. 17.6 ± 1.3 nmol · L-1, LT vs non-LT respectively; P < 0.001; g = -1.41; Figure 1B). Free testosterone was also significantly different between LT and non-LT groups (24.3 ± 1.9 vs. 31.1 ± 1.4 pmol · L-1, LT vs non-LT respectively; P = 0.004; g = -0.72; Figure 1C). Cortisol was significantly lower in the LT group (367.4 ± 39.1) compared to the non-LT group (497.2 ± 33.3 nmol · L-1; P = 0.014; g = -0.63; Figure 1D). Similarly, T3 was different between the LT and non-LT groups (121.1 ± 5.4 vs. 163.2 ± 14.5 ng · dL-1, LT vs non-LT respectively; P = 0.010; g
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= -0.60; Figure 2B). The ratio of total testosterone to cortisol was significantly lower in the LT group (0.028 ± 0.002) compared to the non-LT group (0.040 ± 0.004; P = 0.011; g = -0.65). There were no other significant hormonal differences observed between the LT and non-LT groups. Metabolic and Nutritional Parameters. Metabolic and nutritional data are provided in Tables 3 and 4. Total energy expenditure averaged 3382.0 ± 25.4 kcals · day-1 with basal metabolic rate and physical activity contributing 56.8% and 34.1%, respectively. Mean caloric intake was calculated using the data provided by the food logs (n = 23) and averaged 2587.8 ± 144.2 kcals · day-1; which corresponds to a net caloric balance of -813.1 ± 144.2 kcals · day-1. Protein, carbohydrate, and fat intake represented 21.5 ± 1.2%, 40.1 ± 1.9%, and 36.8 ± 1.3% of the total daily energy intake, respectively. To assess the impact of low testosterone on metabolic and nutritional factors, the subject pool was divided into one of two groups: low-testosterone (LT, n = 12) or non-LT (n = 11). Energy expenditure and macronutrient intake parameters were not different between groups except for a 28.8% higher PRO/FAT macronutrient ratio in the LT group when compared to the non-LT group (P = 0.041; g = 0.87; Table 5). Correlative analysis showed that total testosterone concentration was positively correlated with cortisol concentration (Figure 3; R² = 0.07; P = 0.038) and free testosterone (R² = 0.31; P < 0.001). Positive correlations were also observed between SHBG concentration and energy balance (Figure 4; R² = 0.18; P = 0.044; n = 23) as well as between SHBG concentration and total fat intake (kcals · day-1; Table 6; R² = 0.19; P = 0.038; n = 23) and saturated fat intake (grams · day-1; Table 6; R2 = 0.20; P = 0.032; n = 23). Relative daily fat intake (% of total daily EI) was positively correlated with cortisol concentration (Table 6; R² = 0.19; P = 0.038; n = 23). To assess the impact of time in service on overtraining/overreaching, we performed correlative
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analysis between the molar ratio of TT to cortisol and time in service and found no correlation between these two factors (R2 = 0.0039; P > 0.05; n = 23). No other correlations were found.
DISCUSSION The main finding of this study was the high prevalence of hormonal abnormalities in elite tactical athletes; namely, that 43% of the operators presented with lower than normal levels of testosterone, as defined by the Endocrine Society’s guidelines (21). Second, in contrast to previous work examining athletes, testosterone was positively correlated with cortisol in this population of highly trained healthy subjects (9, 23). The participants also displayed hormonal variations that are often present during overtraining syndrome including elevated SHBG (22). In addition, our data support the notion that nutritional intake may be an important determining factor in the development of hormonal imbalances (15, 16). Testosterone levels have been shown to decrease over time during short-term military training that includes high levels of physical activity and that is associated with inadequate nutritional intake (3, 5, 12, 24). Participation in three weeks of Army Officer Candidate School resulted in a significant decrease in plasma testosterone; however, the mean testosterone concentrations remained above the clinical definition of LTS (12). Conversely, subjects completing the Army Ranger training course, an 8-week long intense selection course for Army special operations, were found to have a significant decrease in circulating testosterone to the point that the average for all subjects was below the threshold for LTS (1, 3, 21). The participants in our study were a cross-sectional sample of elite naval operators, with daily training regimens that are similar to those of the Army Rangers; however, the subjects in our study had already completed on average 7.7 ± 0.9 years of elite military training, which is much
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longer than the 8-week long selection course completed in the Army Ranger studies (3, 24). While it would be tempting to speculate that training duration might be a factor in the development of low testosterone, plasma testosterone concentrations were not correlated with age or time as an operator in our study. This suggests that while high-intensity military training, even as short as three weeks (12), can negatively impact circulating testosterone levels, military training programs of longer (i.e. Army Ranger School) durations do not necessarily result in a sustained reduction in testosterone levels, as observed by Henning et al. when testosterone levels rebounded to pre-training levels within 2-6 weeks of the training stimulus removal (24). In contrast with our results, the previous studies examining Army training demonstrated that the decrease in basal testosterone concentration was associated with a concomitant rise in circulating cortisol concentration (1, 3, 12). These findings are in line with others which found that glucocorticoids (i.e. cortisol) depress testosterone production (9, 25); conversely, our results indicate that there was a positive correlation between cortisol and testosterone concentrations in our subjects. Our data suggest that in subjects undergoing daily physical training over a prolonged duration, cellular adaptations may occur that mitigate the deleterious effects of elevated cortisol on testosterone production. In fact, much like others examining long distance runners or endurance athletes (26)It is also important to note that despite having low levels of testosterone, the subjects in our study were able to train and perform at high exercise intensity levels suggesting either an adaptation to the reduced testosterone levels or a higher uptake of testosterone by androgen receptors in some of the individuals tested. Sometimes used as an indicator of overtraining, the testosterone-to-cortisol ratio is a measure of the anabolic and catabolic status of the individual (6). Testosterone acts as an indicator of anabolism, whereas, cortisol acts as an indicator of catabolism. In those that are
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overtraining, it is expected that cortisol levels will be elevated, whereas, testosterone levels will be reduced; this holds true for most individuals. In general, there is a negative correlation between testosterone and cortisol; during states of anabolism testosterone is high and cortisol is low and during catabolism testosterone is low and cortisol is high. In our participants, testosterone and cortisol were positively correlated, suggesting that an adaptation occurred that allowed the participants to maintain testosterone during times of catabolism to mitigate any consequences. Overtraining is found in new Army Officer Candidates (12); but, perhaps given enough time these subjects would have physiologically adapted like our participants to have a positive correlation between the testosterone and cortisol. During times of negative caloric balance, such as that experienced in intense military training, there are alterations in the hypothalamic-pituitary-thyroid axis (HPTA) and some changes may be mediated by testosterone. In male rats, sustained testosterone reductions are implicated in the fasting induced suppression of TSH; however, exogenous testosterone administration to male rats with low testosterone was shown to increase TSH levels (276). Further studies conducted in human military members, during military training, demonstrated that reductions in testosterone are accompanied by a decrease in TSH, T4, and T3 (3, 287); in these studies, the changes in thyroid hormones were attributed to increased physical strain and a caloric deficit. Therefore, it is well established that a caloric deficit alters the HPTA potentially in an effort to reduce metabolic rates and preserve vital functions during perceived starvation. However, as indicated by the data of this study, TSH, T3, and T4 levels remained in the “normal” range for healthy adults and was not different between subjects with low testosterone and those with testosterone levels in the normal range. These thyroid concentrations, indicate that either caloric balance is being maintained; or that despite a negative caloric balance, thyroid
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functioning has adapted to maintain levels within a normal range for thyroid hormones. Based upon the dietary recall data (n = 23), our subjects trained at a caloric deficit of 813.1 ± 144.2 kcals · day-1; however, their mean TSH was 4.4 ± 1.5 mIU · L-1, which is within the normal range. These findings suggest that despite low-testosterone levels and a caloric deficit thyroid function is maintained. Another possibility, while unlikely due to normal temperatures (San Diego, CA), would be that the subjects are maintaining thyroid hormones despite a caloric deficit to maintain thermoregulation during cold exposure (298). It is well known that caloric deficits, particularly those sustained over time, lead to alterations in sex-hormone concentrations, such as depressed TT and increased SHBG levels (30). T However, in this brief snapshot of time, these results do not directly indicate that there is a link between caloric balance and gonad, thyroid, and adrenal hormone concentrations for those engaged in a rigorous military physical training program. Indeed, there were no correlations between caloric balance and hormone concentrations; howevernonetheless, macronutrient intake was correlated to hormone concentrations. Herein, we add to the body of knowledge on the impact of nutrient intake and hormonal balance by demonstrating that the relative distribution of macronutrient intake also plays an important role in determining the hypothalamic-pituitarygonadal axis (HPGA) and hypothalamic-pituitary-adrenal axis (HPAA) hormone status of highly trained individuals. Previous research has shown that testosterone levels are negatively correlated with protein intake and positively correlated with fat intake in healthy trained male subjects (15). Other correlative and experimental studies have shown that a diet with a high PRO/CHO macronutrient ratio depresses testosterone levels (15, 3029, 310). Our results show that in our population of highly trained individuals, the relative intake of protein and fat may play a more important role than the PRO/CHO ratio, as indicated by previous reports in healthy physically
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active male subjects (3029, 310). Interestingly, unlike other studies (15, 321, 332), our results indicate that dietary fat composition (i.e. SFA, MUFA, PUFA, PUFA/SFA ratio) is not influential on testosterone levels. It is possible that the differences observed between studies are due to variations in physical training workload of the subject populations. The subjects of the current study were physically active for much longer durations and at higher exercise intensities than the recreational athletes examined in the aforementioned studies. Our data also suggest that macronutrient intake plays a role in other biomarkers implicated in the regulation of testosterone production, namely cortisol and SHBG. The present results indicate that there is a positive correlation between fat intake (as a percentage of average daily total energy intake) and cortisol which is in stark contrast to findings by Martens et al. (2010) who found that cortisol decreases in response to fat intake (343). As opposed to previous findings, SHBG was also found to be positively correlated with energy balance, fat intake, and SFA intake (354). In combination with decreasing testosterone, this increase in SHBG over time is suggestive of the presence of overtraining syndrome (2, 22, 365, 376). Our HPGA and HPAA hormone data also indicate that this group of subjects presented with several of the physiological characteristics associated with physical overtraining/overreaching (22); however, our data also show that the non-LT subjects exhibited adaptations that would provide enhanced resiliency to the normal stress response. This is made evident due to the positive correlation between cortisol and testosterone in the non-LT group; these results are in contrast to previous findings which indicate that high levels of circulating cortisol negatively correlate to circulating levels of testosterone (10, 12) and that cortisol administration (endogenous/exogenous) directly reduces testosterone production (without affecting follicle stimulating hormone and luteinizing hormone) (11). To add to this
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unanticipated finding, comparisons between the oldest subjects (≥ 35 yrs) and the youngest subjects (< 35 yrs) failed to demonstrate any differences in any of the hormones measured. In fact, the oldest subject (51 yrs of age; > 30 yrs of service; 12 deployments) had total testosterone (12.5 nmol · L-1) and all other measured hormones fell within the normal range for an adult male. This begs the question – what is causing hormonal abnormalities, particularly in the HPGA, to occur in a large percentage of elite tactical athletes, but not others? The answer is likely multifactorial and likely includes both nutrition and rest, as well other factors not assessed in the current study. Thus, further investigations into the mechanisms responsible for hormonal imbalances and determination if hormonal imbalances are preexisting (prior to service) or occur as a result of service is warranted.
LIMITATIONS This study is not without limitations. The primary limitation is that this study is crosssectional in design and only captures a single time point for each operator. While the crosssectional design does provide valuable information regarding the state of operators across ages and time in service, it fails to indicate whether or not individuals had preexisting LT prior to service. Therefore, it would be prudent to investigate the hormonal balance in operators from the beginning of their service to the end of service and beyond to determine what role, if any, elite military training and operations have on hormonal balance. Other limitations include: undiagnosed preexisting medical conditions, genetics, unknown family stress (including fatherhood), sleep health, and financial situation, among other factors.
CONCLUSION
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In summary, this study found that of 65 elite tactical athletes (operators) assessed, 43% displayed testosterone levels below the threshold for LTS (21). These athletes also displayed abnormally high levels of SHBG and some displayed high resting levels of cortisol, both hallmarks of overtraining syndrome. Interestingly enough, there was a weak positive correlation between testosterone and cortisol, indicating that those who may be experiencing the most stress are also the most adept at maintaining hormonal balance. The present findings indicate that elite tactical athletes are highly stressed; however, some may have developed or been born with coping mechanisms to maintain satisfactory performance and hormonal balance.
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Figure Legends – Figure 1A – D. Concentrations of sex and stress hormones stratified by testosterone grouping in United States Naval Operators. Participants were split into two groups, those with low-testosterone (LT: total testosterone <10.4 nmol · L-1) and those with normal testosterone (Non-LT: total testosterone ≥10.4 nmol · L-1). Baseline concentrations of Luteinizing Hormone (A), Total Testosterone (B), Free Testosterone (C), and Cortisol (D) for each participant were measured and stratified by group (LT vs. Non-LT). Each grey circle represents one participant’s values and the black bar is the mean concentration for each group. The hash marked box in-line with the y-axis denotes the normal range for each hormone assessed, as determined by the Endocrine Society (37); the reference range for Free Testosterone is outside the range of values depicted within Figure 1C. † denotes significant difference from LT group (P < 0.05). N = 65; LT: n = 28; Non-LT: n = 37. Figure 2A – C. Concentrations of thyroid hormones stratified by testosterone grouping in United States Naval Operators. Participants were split into two groups, those with lowtestosterone (LT: total testosterone <10.4 nmol · L-1) and those with normal testosterone (NonLT: total testosterone ≥10.4 nmol · L-1). Baseline concentrations of Thyroid Stimulating Hormone (A), Triiodothyronine (B), and Thyroxine (C) for each participant were measured and stratified by group (LT vs. Non-LT). Each grey circle represents one participant’s values and the black bar is the mean concentration for each group. The hash marked box in-line with the y-axis denotes the normal range for each hormone assessed, as determined by the Endocrine Society (37). † denotes significant difference from LT group (P < 0.05). N = 65; LT: n = 28; Non-LT: n = 37. Figure 3. Correlation between Cortisol Concentration and Total Testosterone Concentration. Each black diamond represents one individual’s Cortisol and Total testosterone values. The dashed line represents the clinically defined threshold for LT, total testosterone <10.4 nmol · L-1 (21). R² = 0.07; P < 0.05; n = 65.
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16. Adlercreutz H. Western diet and Western diseases: some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Invest Suppl. 1990;201:3-23. PubMed PMID: 2173856. 17. Flynn MG, Pizza FX, Boone JB, Andres FF, Michaud TA, Rodriguez-Zayas JR. Indices of training stress during competitive running and swimming seasons. Int J Sports Med. 1994;15(1):21-6. doi: 10.1055/s-2007-1021014. PubMed PMID: 8163321. 18. Prusaczyk WK, Goforth Jr HW, Nelson MS. Physical Training Activities of East Coast US Navy SEALs. DTIC Document; 1994. 19. Prusaczyk WK, Stuster JW, Goforth Jr HW, Smith TS, Meyer LT. Physical Demands of US Navy Sea-Air-Land (SEAL) Operations. DTIC Document; 1995. 20. Roza AM, Shizgal HM. The Harris Benedict equation reevaluated: resting energy requirements and the body cell mass. Am J Clin Nutr. 1984;40(1):168-82. PubMed PMID: 6741850. 21. Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, et al. Testosterone therapy in men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2010;95(6):2536-59. doi: 10.1210/jc.2009-2354. PubMed PMID: 20525905. 22. Tanskanen MM, Kyröläinen H, Uusitalo AL, Huovinen J, Nissilä J, Kinnunen H, et al. Serum sex hormone-binding globulin and cortisol concentrations are associated with overreaching during strenuous military training. J Strength Cond Res. 2011;25(3):787-97. doi: 10.1519/JSC.0b013e3181c1fa5d. PubMed PMID: 20543745. 23. Anderson T, Lane AR, Hackney AC. Cortisol and testosterone dynamics following exhaustive endurance exercise. Eur J Appl Physiol. 2016;116(8):1503-9. Epub 2016/06/04. doi: 10.1007/s00421-016-3406-y. PubMed PMID: 27262888. 24. Henning PC, Scofield DE, Spiering BA, Staab JS, Matheny RW, Smith MA, et al. Recovery of endocrine and inflammatory mediators following an extended energy deficit. J Clin Endocrinol Metab. 2014;99(3):956-64. doi: 10.1210/jc.2013-3046. PubMed PMID: 24423293. 25. Bambino TH, Hsueh AJ. Direct inhibitory effect of glucocorticoids upon testicular luteinizing hormone receptor and steroidogenesis in vivo and in vitro. Endocrinology. 1981;108(6):2142-8. doi: 10.1210/endo-108-6-2142. PubMed PMID: 6262050. 26. Hooper DR, Kraemer WJ, Saenz C, Schill KE, Focht BC, Volek JS, et al. The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition. Eur J Appl Physiol. 2017;117(7):1349-57. Epub 2017/05/05. doi: 10.1007/s00421017-3623-z. PubMed PMID: 28470410. 276. Cohen JH, Alex S, DeVito WJ, Braverman LE, Emerson CH. Fasting-associated changes in serum thyrotropin in the rat are influenced by gender. Endocrinology. 1989;124(6):3025-9. doi: 10.1210/endo-124-6-3025. PubMed PMID: 2721456. 287. Opstad PK, Falch D, Oktedalen O, Fonnum F, Wergeland R. The thyroid function in young men during prolonged exercise and the effect of energy and sleep deprivation. Clin Endocrinol (Oxf). 1984;20(6):657-69. PubMed PMID: 6432374. 298. Stroud MA, Ritz P, Coward WA, Sawyer MB, Constantin-Teodosiu D, Greenhaff PL, et al. Energy expenditure using isotope-labelled water (2H218O), exercise performance, skeletal muscle enzyme activities and plasma biochemical parameters in humans during 95 days of endurance exercise with inadequate energy intake. Eur J Appl Physiol Occup Physiol. 1997;76(3):243-52. PubMed PMID: 9286604.
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3029. Anderson KE, Rosner W, Khan MS, New MI, Pang SY, Wissel PS, et al. Diet-hormone interactions: protein/carbohydrate ratio alters reciprocally the plasma levels of testosterone and cortisol and their respective binding globulins in man. Life Sci. 1987;40(18):1761-8. PubMed PMID: 3573976. 310. Kappas A, Anderson KE, Conney AH, Pantuck EJ, Fishman J, Bradlow HL. Nutritionendocrine interactions: induction of reciprocal changes in the delta 4-5 alpha-reduction of #
Role
Definition Dr Karen Kelly – lead 1 Conceptualization Dr Andrew Jensen – supporting Dr Andrew Jensen – equal 2 Data curation Ms Laura Arrington – equal 3 Formal analysis Dr Andrew Jensen – lead 4 Funding acquisition Dr Karen Kelly – lead Dr Karen Kelly – equal Dr Andrew Jensen – equal 5 Investigation Ms Laura Arrington – equal Dr Andrew Jensen – equal 6 Methodology Dr Karen Kelly – equal testosterone and the cytochrome P-450-dependent oxidation of estradiol by dietary macronutrients in man. Proc Natl Acad Sci U S A. 1983;80(24):7646-9. PubMed PMID: 6584878; PubMed Central PMCID: PMCPMC534397. 321. Sebokova E, Garg ML, Wierzbicki A, Thomson AB, Clandinin MT. Alteration of the lipid composition of rat testicular plasma membranes by dietary (n-3) fatty acids changes the responsiveness of Leydig cells and testosterone synthesis. J Nutr. 1990;120(6):610-8. PubMed PMID: 2352035. 332. Sebokova E, Wierzbicki A, Clandinin MT. Modulation of rat testes lipid composition by hormones: effect of PRL and hCG. Am J Physiol. 1988;255(4 Pt 1):E442-8. PubMed PMID: 2845800. 343. Martens MJ, Rutters F, Lemmens SG, Born JM, Westerterp-Plantenga MS. Effects of single macronutrients on serum cortisol concentrations in normal weight men. Physiol Behav. 2010;101(5):563-7. Epub 2010/09/16. doi: 10.1016/j.physbeh.2010.09.007. PubMed PMID: 20849868. 354. Longcope C, Feldman HA, McKinlay JB, Araujo AB. Diet and sex hormone-binding globulin. J Clin Endocrinol Metab. 2000;85(1):293-6. doi: 10.1210/jcem.85.1.6291. PubMed PMID: 10634401. 365. Busso T, Häkkinen K, Pakarinen A, Kauhanen H, Komi PV, Lacour JR. Hormonal adaptations and modelled responses in elite weightlifters during 6 weeks of training. Eur J Appl Physiol Occup Physiol. 1992;64(4):381-6. PubMed PMID: 1592066. 376. Häkkinen K, Pakarinen A, Alen M, Kauhanen H, Komi PV. Neuromuscular and hormonal adaptations in athletes to strength training in two years. J Appl Physiol (1985). 1988;65(6):2406-12. PubMed PMID: 3215840. 387. Endocrine self-assessment program 2016. Washington, D.C., DC: Endocrine Society; 2016.
Hormonal balance in elite tactical athletes 22
Dr Karen Kelly – lead Project administration Dr Andrew Jensen – supporting Ms Laura Arrington – supporting Dr Lorraine Turcotte – equal 8 Resources Dr Karen Kelly – equal Dr Andrew Jensen – lead 9 Software Ms Laura Arrington – supporting Dr Lorraine Turcotte – equal 10 Supervision Dr Karen Kelly – equal Dr Andrew Jensen – equal 11 Validation Dr Lorraine Turcotte – equal Dr Karen Kelly – equal Dr Andrew Jensen – lead 12 Visualization Ms Laura Arrington – supporting Writing – original Dr Andrew Jensen – lead 13 Dr Lorraine Turcotte – supporting draft Dr Andrew Jensen – lead Writing – review & Dr Lorraine Turcotte – supporting 14 editing Dr Karen Kelly - supporting Contributor Roles Taxonomy (CRediT) 7
Hormonal balance and nutritional intake in elite tactical athletes Andrew E. Jensen, PhD; Laura J. Arrington, MS; Lorraine P. Turcotte, PhD; Karen R. Kelly, PhD.
Figure 1A.
Figure 1B.
10
45
9
40
8
Total Testosterone (nmol · L-1)
Luteinizing Hormone (IU · L-1)
Hormonal balance in elite tactical athletes 23
7 6 5 4 3 2
LT
30 25 20 15 10
0
Non-LT
Figure 1C.
1400
†
Non-LT
†
1200 Cortisol (nmol · L-1)
60 50 40 30
1000 800 600
20
400
10
200
0
LT
Figure 1D.
70
Free Testosterone (pmol · L-1)
35
5
1 0
†
LT
Non-LT
0
LT
Non-LT
Hormonal balance in elite tactical athletes 24
Figure 2B.
30
600
25
500 Triiodothyronine (ng · dL-1)
Thyroid Stimulating Hormone (mIU · L-1)
Figure 2A.
20
15
10
5
0
LT
Non-LT
LT
Non-LT
16 14 12 Thyroxine (µg · dL-1)
400
300
200
100
Figure 2C.
10 8 6 4 2 0
†
0
LT
NonLT
Hormonal balance in elite tactical athletes 25
Table 1. Physical Characteristics of United States Naval Operators Baseline
(Range)
Age, yrs
29.9 ± 0.9
(21 – 51)
Height, cm
178.4 ± 0.7
(162.6 – 188.0)
Weight, kg
85.1 ± 0.9
(72.0 – 110.9)
BMI, kg · m-2
26.7 ± 0.3
(23.7 – 37.2)
Time as Operator, yrs
7.7 ± 0.9
(0.2 – 32.6)
Deployments, #
3.0 ± 0.5
(0 – 13)
Values presented as Mean ± SE. n = 65.
Table 2. Concentrations of Sex, Stress and Thyroid Hormones in United States Naval Operators Baseline
(Range)
Normal Range*
Free Testosterone, pmol · L-1
28.2 ± 1.2
(15.1 – 60.1)
310.0 – 1040.0
Total Testosterone, nmol · L-1
13.5 ± 0.9
(5.9 – 40.5)
10.4 – 41.6
SHBG, nmol · L-1
94.2 ± 6.4
(32.2 – 171.5)
10.0 – 60.0
441.3 ± 26.4
(141.4 – 1154.9)
137.9 – 689.7
3.4 ± 0.2
(0.2 – 9.2)
1.0 – 9.0
145.9 ± 9.0
(42.0 – 546.0)
70.0 – 200.0
Thryoxine, µg · dL-1
7.8 ± 0.2
(4.5 – 14.3)
5.5 – 12.5
Thyroid Stimulating Hormone, mIU · L-1
3.5 ± 0.7
(0.2 – 28.4)
0.5 – 5.0
Total Testosterone / Cortisol, molar ratio
0.035 ± 0.002
(0.008 – 0.127)
Cortisol, nmol · L-1 Luteinizing Hormone, IU · L-1 Triiodothryronine, ng · dL-1
Values presented as Mean ± SE. n = 65. *As determined by the Endocrine Society (37).
Table 3. Metabolic Characteristics of United States Naval Operators Baseline
(Range)
BMR, kcals · day-1
1921.6 ± 14.4
(1674.6 – 2191.7)
PA, kcals · day-1
1153.0 ± 8.7
(1004.8 – 1315.0)
Hormonal balance in elite tactical athletes 26
TEF, kcals · day-1
307.5 ± 2.3
(267.9 – 350.7)
TEE, kcals · day-1
3382.0 ± 25.4
(2947.3 – 3857.4)
Values presented as Mean ± SE. BMR: basal metabolic rate. PA: physical activity. TEF: thermic effect of food. TEE: total energy expenditure. All values were calculated via Harris-Benedict Equation as described in the methods. n = 65.
Table 4. Nutritional Characteristics of Energy Intake in United States Naval Operators Baseline
(Range)
EI, kcals · day-1
2587.8 ± 144.2
(1230.3 – 3744.5)
Energy Balance, kcals · day-1
-813.1 ± 144.2
(-2415.8 – +374.6)
548.1 ± 36.7
(271.6 – 931.9)
1048.13 ± 85.4
(489.9 – 2013.1)
Fat, kcals · day-1
945.7 ± 56.6
(427.5 – 1538.4)
Alcohol, kcals · day-1
113.5 ± 38.5
(23.4 – 520.3)
Fiber, g · day-1
26.1 ± 2.8
(8.9 – 60.1)
SFA, g · day-1
32.7 ± 1.9
(14.0 – 46.6)
MUFA, g · day-1
21.0 ± 3.1
(1.4 – 56.4)
PUFA, g · day-1
9.1 ± 1.4
(0.6 – 25.5)
Cholesterol, mg · day-1
550.2 ± 53.6
(162.9 – 958.0)
Vitamin D, mcg · day-1
6.5 ± 2.3
(0.1 – 41.9)
Magnesium, mg · day-1
273.1 ± 39.4
(19.6 – 693.9)
11.6 ± 2.1
(0.7 – 42.1)
Protein, kcals · day-1 Carbohydrates, kcals · day-1
Zinc, mg · day-1
Values presented as Mean ± SE. EI: Energy Intake. Energy Balance: EI – Total Energy Expenditure. SFA: Saturated fatty acids. MUFA: Mono-unsaturated fatty acids. PUFA: poly-unsaturated fatty acids. n = 23.
Table 5. Total Energy Expenditure and Macronutrient Intake Differences between LT and non-LT United States Naval Operators EI, kcals · day-1
LT (n= 12)
non-LT (n= 11)
2558.5 ± 228.7
2619.7 ± 180.9
Hormonal balance in elite tactical athletes 27
TEE, kcals · day-1
3417.4 ± 54.7
3382.8 ± 55.5
23.3 ± 2.0
19.6 ± 1.0
575.5 ± 56.6
518.3 ± 46.8
35.4 ± 1.9
38.4 ± 1.6
895.6 ± 83.8
1000.4 ± 75.6
39.9 ± 3.0
40.4 ± 2.4
1033.9 ± 136.7
1063.7 ± 105.2
PRO/CHO, ratio
0.65 ± 0.10
0.51 ± 0.05
PRO/FAT, ratio
0.67 ± 0.06*
0.52 ± 0.03
CHO/FAT, ratio
1.21 ± 0.15
1.08 ± 0.09
PRO, % EI kcals · day-1 FAT, % EI kcals · day-1 CHO, % EI kcals · day-1
Values presented as Mean ± SE. LT: Low Testosterone. Non-LT: “normal” total testosterone. TT: Total Testosterone. LT: TT <10.4 nmol · L-1 (21). non-LT: TT ≥ 10.4 nmol · L-1. EI: Energy Intake. TEE: Total Energy Expenditure. PRO: Protein. FAT: Fat. CHO: Carbohydrate. Macronutrient ratios were calculated using mean kcal · day-1 data. Macronutrient percent values were calculated as the percentage of average total energy intake per day. *P<0.05 vs. non-LT group. n = 23.
Table 6. Correlation coefficients between daily nutrient intake and sex hormone concentrations in United States Naval Operators FT
TT
Cortisol
SHBG
TT/Cortisol Ratio
Energy balance, kcals
-0.26
0.06
-0.07
0.42*
0.07
PRO, kcals
-0.04
-0.01
0.00
0.28
-0.10
PRO, EI%
0.16
-0.10
-0.02
-0.13
-0.17
CHO, kcals
-0.29
-0.01
-0.08
0.25
0.03
CHO, EI%
-0.23
-0.11
-0.20
0.03
0.08
FAT, kcals
-0.10
0.18
0.28
0.43*
-0.07
FAT, EI%
0.21
0.24
0.44*
0.13
-0.05
Alcohol, kcals
0.02
0.08
-0.15
-0.26
0.22
Fiber, g
-0.48
-0.10
0.03
0.22
-0.22
SFA, g
0.17
0.30
0.29
0.44*
0.12
MUFA, g
-0.19
0.17
0.25
0.32
-0.13
Hormonal balance in elite tactical athletes 28
PUFA, g
-0.20
0.25
0.30
0.40
-0.08
PUFA/SFA Ratio
-0.30
0.11
0.13
0.23
-0.13
PUFA/MUFA Ratio
-0.30
0.12
0.13
0.22
-0.13
Cholesterol, mg
0.36
0.14
0.15
0.32
-0.05
Vitamin D, mcg
-0.13
-0.01
-0.21
0.27
0.17
Magnesium, mg
0.10
0.08
-0.07
0.31
0.03
Zinc, mg
0.28
0.02
-0.20
0.18
0.19
Correlation coefficients are Pearson product-moment correlation. Macronutrient percent values were calculated as the percentage of average total energy intake per day. PRO: protein. CHO: carbohydrate. SFA: saturated fatty acids. MUFA: mono-unsaturated fatty acids. PUFA: poly-unsaturated fatty acids. FT: free testosterone. TT: total testosterone. SHBG: sex hormone-binding globulin. TT/Cortisol Ratio: molar ratio of total testosterone to cortisol. *Statistically significant correlation, P < 0.05. n = 23.
HIGHLIGHTS ● High prevalence of low testosterone was sampled in the elite tactical athletes. ● Weak positive correlation observed between testosterone and cortisol. ● Long-term elite military training affects the HPA, HPT, and HPG axes.