Internationai Journal of Sports Physiology and Performance, 2014, 9,166-172inttp://dx.doi.org/10.1123/ÍJSPP.2013-0018© 2014 Human Kinetics, Inc.

Improving Strength and Power in Trained AthletesWith 3 Weeks of Occlusion Training

Christian J. Cook, Liam P. Kilduff, and C. Martyn Beaven

Purpose: To examine the effects of moderate-load exercise with and without blood-fiow restriction (BFR) onstrength, power, and repeated-sprint ability, along with acute and chronic salivary hormonal parameters. Meth-ods: Twenty male semiprofessional rugby union athletes were randomized to a lower-body BFR intervention(an occlusion cuff infiated to 180 mmHg worn intermittently on the proximal thighs) or a control interventionthat trained without occlusion in a crossover design. Experimental sessions were performed 3 times a weekfor 3 wk with 5 sets of 5 repetitions of bench press, leg squat, and pull-ups performed at 70% of 1-repetitionmaximum. Results: Greater improvements were observed (occlusion training vs control) in bench press (5.4 ±2.6 vs 3.3 ± 1.4 kg), squat (7.8 ± 2.1 vs 4.3 ± 1.4 kg), maximum sprint time (-0.03 ± 0.03 vs -O.OI ± 0.02 s),and leg power (168 ± 105 vs 68 ± 50 W). Greater exercise-induced salivary testosterone (ES 0.84-0.61) andCortisol responses (ES 0.65-0.20) were observed after the occlusion intervention sessions compared with thenonoccluded controls; however, the acute Cortisol increases were attenuated across the training block. Con-clusions: Occlusion training can potentially improve the rate of strength-training gains and fatigue resistancein trained athletes, possibly allowing greater gains from lower loading that could be of benefit during hightraining loads, in competitive seasons, or in a rehabilitative setting. The clear improvement in bench-pressstrength resulting from lower-body occlusion suggests a systemic effect of BFR training.

Keywords: blood-flow restriction, testosterone, cortisol, training adaptation

In many team sports including rugby, there is an onuson short-term training blocks to enhance aspects of func-tional strength, as trainers and athletes often only haveshort time frames and limited opportunities to enhancemultiple aspects of physical conditioning.' During hightraining phases and in competitive seasons it is necessaryto be mindful of total load on athletes and their require-ment to recover between games. In addition, short-termtraining blocks are necessarily performed concurrentlywith other training practices that contribute to overallperformance. Thus, it is vital that the exercise prescriptionduring such blocks be as effective as possible in elicitingpositive functional gains.

Resistance training with low loads (20% of 1-repeti-tion maximum), in conjunction with an applied occlusionto restrict blood fiow, has been shown to rapidly increasemuscle size and strength in athletic populations.^-^ Aload and intensity as low as that achieved with walking,when combined with blood-flow restriction (BFR), havebeen demonstrated to elicit significant improvements inknee-joint strength and leg-muscle size.'* The enhanced

Cook is with the United Kingdom Sports Council, London,UK. Kilduff is with the Exercise and Medicine ResearchCentre, Swansea University. Swansea, UK. Beaven is withthe Swedish Winter Sports Research Center, Mittuniversitetet,Östersund, Sweden.

hypertrophy and strength gains resulting from BFR train-ing have been associated with acute increases in growthhormone-'''̂ and decreased myostatin mRNA expression.'Furthermore, exercise with BFR elicits increased acutemetabolic stress (lactate and cortisol), activation of themTOR-signaling pathway,*' and increased muscle-fiberrecruitment'" and promotes angiogenesis."

The role of endogenous testosterone in affectingresistance-training outcomes is well established insofaras testosterone levels within the normal physiologicalrange are requisite, or permissive, for the normal adaptiveresponse to resistance exercise.'2-'"* Previous researchinvestigating testosterone responses to BFR training hasdemonstrated no intervention effect when compared withexercising without BFR despite observed increases inother putatively anabolic hormones."^" However, thosestudies used blood, rather than salivary, sampling whichcan infiuence steroid hormone concentrations'^ and didnot involve intermittent occlusion. In contrast, we usedan intermittent occlusion intervention and saliva samplesthat are noninvasive and recognized to reflect free-steroidlevels capable of interacting with hormone receptors.'^

Therefore, the purpose of this investigation wasto compare the functional training effects and salivaryhormonal responses after intermittent BFR training withthose of nonoccluded training across an 8-week preseasonperiod for trained male rugby athletes. We hypothesizedthat, compared with nonoccluded training, BFR training

166

Occlusion and Strength Training 167

would elicit greater strength gains and exaggeratedexercise-induced alterations in salivary testosterone andCortisol, due to the provision of an additional Stressor.

iVIethodsSubjectsTwenty male semiprofessional rugby union athletes(mean ± SD age 21.5 ± 1.4 y, height 1.84 ± 0.05 m, bodymass 95.6 ± 10.4 kg) from tbe same club who played arange of positions were recruited and provided writteninformed consent. All players had a minimum of 2 yearsof resistance-training experience and were currently inthe preseason phase of their training programs.

DesignThe athletes were divided into 2 groups (each n = 10)with a similar spread of age, body mass, height, playingposition, and existing strength and speed performance(Table 1). The study was tailored to form an 8-weekresistance-training block for the athletes to achieve func-tional strength and power gains that they would normallyfocus on during preseason resistance training. The studyprotocol was approved by the ethics committee of thelocal university.

During the time of study all athletes had set dietaryplans that were consistent across the training blocks andwere designed to meet their body-weight and activityneeds. Athletes were encouraged to ensure they got aminimum of 8 hours of sleep, and a self-reported logsuggested they achieved this regularly. Caffeine and otherfluid consumption was similar across both training blocks,while alcohol consumption was low or absent.

MethodologyBefore commencing training all athletes attended 2consecutive days of testing to determine initial strength.

power, speed, and speed endurance. All athletes werefamiliar with the testing protocols from their prior train-ing. They were instructed not to take any anti-inflamma-tory drugs and to refrain from consuming alcohol in the48 hours before each testing day. In addition, the playerswere instructed to consume at least 750 mL of fluid, avoidconsumption of caffeinated products, and replicate theirdietary consumption on the morning of testing days.

Strength. On day 1 of testing, athletes assembled at11:00 AM, having consumed breakfast and a minimumof 750 mL fluid and having been encouraged to haveslept at least 8 hours. A standard 15-minute warm-up wasperformed comprising 5 minutes on a rowing ergometer, 5minutes on a cycling ergometer (both at target heart ratesof 120-130 beats/min measured by heart-rate monitors;Polar S8 lOi, Polar Oy, Kempele, Finland), and 5 minutesof mixed calisthenics.

Athletes then performed leg squats to just belowparallel in a controlled manner under the supervision ofa qualified strength-conditioning coach. Using historicalrecords of individual performance, athletes completedthe following squats based on individual percentage of1-repetition maximum (1-RM): 5 x 50%, 3 x 60%, 2 x80% and then 1 x 90%, 1 x 95%, 1 x 100%. If success-ful at the 1 X 100% lift, the athlete continued to increasethe weight in increments of 2.5 kg until failure. The bestlift was recorded as the athlete's 1-RM. Athletes wereallowed 5 minutes passive recovery between attempts.After a further 5 minutes rest, this routine was repeatedto determine each individual's bench-press 1-RM. Onaverage, athletes performed 3 maximum attempts todetermine their true 1-RM.

Power and Speed. On day 2 of testing, tbe athletesagain assembled at 11:00 AM and performed the samestandard warm-up as on day 1. They then performed 3maximal-effort unloaded countermovement jumps, withthe arms akimbo throughout the movement, on a forceplate sampling at 1000 Hz (Kistler Instrument Corp,Amherst, NY, USA), with the best jump being recorded to

Table 1 Physical Characteristics of the Athletes (Mean ± SD)

Group 1(n = 10) Group 2 (n = 10)Age(y) 21.8±1.2 21.1 ± 1.5

Height (cm) 1.84 ± 0.05 1.84 ± 0,06

Body mass (kg) 94.7 ± 10.3 96.4 ± 11.0

Bench-press strength (kg) 139.0±7.8 141.0±13.6

Leg-squat strength (kg) 171.5 ± 11.9 174.8 ± 13.6

40-m-sprint time (s) 5.08±0.18 5.11 ±0.18

Performance maintenance (%)" 93.1 ± 2.0 92.2 ± 1.8

Countermovement-jump peak power (W) 5216 ±1027 5551 ±932

" Change in sprint speed from the first to last of 5 x 40-m spritits ([Sprint #1/Sprint #5] x 100) with1-min recovery time between sprints.

168 Cook, Kilduff, and Beaven

calculate lower body instantaneous power as previouslydescribed.'* One minute of passive recovery was allowedbetween jump attempts.

After the conclusion of jump testing, athletesundertook three 40-m warm-up sprints at 50%, 65%,and 80% of self-perceived maximum pace. Recoverybetween sprints consisted of walking the distance backto the start. After a further 1 minute of rest, the athletesperformed 5 x 40-m maximal sprints, and speed wasassessed via electronic timing light gates (Brower TimingSystem, Salt Lake City, UT, USA). One minute separatedmaximal sprint efforts. Best sprint time was recorded,and performance maintenance was calculated based onthe change in sprint speed from the first to last sprint:(sprint #l/sprint #5) X 100.

Training BlocksThe 2 groups were randomly assigned to 1 of the 2 train-ing interventions in a counterbalanced crossover fashion.Each training block was 3 weeks long and included 9experimental resistance-training sessions. All trainingsessions began at 9:00 AM

Standard Training. After completing the standardwarm-up described earlier, the athletes performed 3exercises (leg squat, bench press, and weighted pull-up)at 70% of their individually assessed 1-RM. Five sets of5 repetitions were performed with 90 seconds passive restbetween sets and 3 minutes between exercises.

BFR Training. The BFR training was identical to thestandard training just described, except that lower-limb blood flow was restricted with an occlusion cuff(width 10.5 cm) inflated to 180 mmHg. The cuff wasonly inflated during exercise and was deflated duringthe interset and interexercise rest periods (intermittentocclusion). Note that the lower-body occlusion cuff wasworn bilaterally at the most proximal portion of the thighduring all 3 exercises.

Hormone AssessmentSaliva samples were collected before and after the firstexperimental training session of each week. For eachof their 12 samples, participants were asked to expec-torate 2 mL of saliva into a sterile container beforebeginning their training session. Samples were stored at-20°C until assay. Salivary steroid samples were takenin this study as they are minimally invasive, have theadvantage of reflecting free-steroid concentrations, andare reported to be more physiologically relevant thantotal blood levels.'^ To minimize the possibility of anyblood contamination of saliva, which would result in anoverestimation of hormone concentrations, the playerswere advised to avoid brushing their teeth, drinkinghot fluids, or eating hard foods (eg, apples) in the 2hours before providing their sample. Saliva sampleswere analyzed in duplicate for testosterone and cortisolusing commercial enzyme-immunoassay kits as per

manufacturer's instructions (Sali metrics Europe Ltd,Suffolk, UK). The detection limits for the testosteroneand cortisol assays were 17 pmol/L and 33 nmol/L,respectively, with intra-assay and interassay coefficientsof variation <9.1%.

Statistical AnalysesChanges in the mean of each measure were used toassess magnitudes of effects by dividing the changesby the appropriate between-athletes standard devia-tions. Pairwise comparisons were made betweentraining conditions, and differences were interpretedin relation to the likelihood of exceeding the smallestworthwhile effect with individual change thresholds foreach variable. Magnitudes of the standardized effectswere interpreted using thresholds of 0.2, 0.6, 1.2, and2.0 for small, moderate, large, and very large, respec-tively.'^ Standardized effects of -0.19 to 0.19 weretermed trivial. Quantitative chances of higher or lowerdifferences were evaluated qualitatively as follows:<1%, almost certainly not; 1% to 5%, very unlikely; 5%to 25%, unlikely; 25% to 75%, possible; 75% to 95%,likely; 95% to 99%, very likely; >99%, almost certain.To make inferences about the large-sample value of aneffect, the uncertainty in the effect was expressed as90% confidence limits. An effect was deemed unclearif the confidence interval overlapped the thresholds forboth small positive and negative effects. The significancelevel was set at P < .05. An intraclass correlation (ICC)of .98 for power in a countermovement jump has beendemonstrated previously.-^^ Similarly, high reliabilityfor the 40-m-sprint (ICC = .91) and strength measures(ICC >.96) used in the current study has been reportedin trained rugby athletes.^'

ResultsAll athletes completed the experimental protocol. Overthe 8-week preseason period, mean improvements (± 90%confidence limits) were observed in bench press (8.6 ± 5.8kg; ES 0.78) and leg squat ( 12.0 ± 6.7 kg; ES 0.93). Whenthe 2 training interventions were compared, occlusionresulted in significantly greater improvements in benchpress (P = .0044; 1.4% ± 0.8%), squat (P = 1.03 x lO'̂ ;2.0% ± 0.6%), maximal-sprint time (P = .0162; 0.4% ±0.3%), and countermovement-jump power (P = .0003;1.8% ± 0.7%; Figure 1). The occlusion intervention alsosignificantly improved performance maintenance in therepeated-sprint test by 0.74% ± 0.37% (P = .0023) com-pared with the nonoccluded intervention.

Salivary hormone concentrations before the firstexperimental session were 118.7 ± 14.2 pg/mL for tes-tosterone and 2.15 ± 0.7 ng/mL for cortisol. The salivarytestosterone and cortisol exercise-induced responsedata from sessions 1, 4, and 7 (the first session of eachweek in each 3-wk training block) are shown in Figure2. Large to very large increases in testosterone wereobserved in response to these 3 BFR training sessions

Occlusion and Strength Training 169

Post Pre Post

Time relative to 3-week training biock

Figure 1 — Adaptive responses within a rugby preseason training block with or without occlusion. Solid line: 180-mmHg occlu-sion applied to the lower limbs during exercise. Dotted line: no occlusion stimulus applied during training. Abbreviations: 1-RM,1 -repetition maximum; CMJ, countermovement jump. **P < .01 ; *P < .05 between conditions. Pre: Data collected before the 3-weektraining block; Post: Data collected after the 3-week training block. Error bars represent standard deviations.

(ES 1,50-2,19) in comparison with moderate increasesin response to nonoccluded training (ES 0,73-1,19), Theacute testosterone increases as a result of BFR trainingwere consistently and almost certainly (likelihood >99%)greater than the increases in the nonoccluded trainingsituation. Overall, significant associations were alsoobserved between the mean acute salivary testosteroneresponse to exercise and leg-squat strength (r =: ,68, P= ,0005), bench-press strength (/•= ,45, P - ,0233), andcountermovement-jump power-production gains (r =,46, P=,0201),

In contrast to the testosterone data, the cortisolresponses to BFR were significantly attenuated over the3-week training period (P-l.\2x 16^). Specifically, thequalitative chance that the increase in cortisol was greaterin response to BFR fell from almost certain (99.99%;ES 0.65) in the first week, to only possible (49.77%; ES0,20) in the third week. The preexercise salivary testos-terone was observed to significantly increase from 120,5± 13.2 to 130.1 ± 13,6 pg/mL (8,0%; P = ,0284) acrossthe training blocks during the BFR intervention, whilea nonsignificant decrease from 120,5 ± 13,2 to 117,1 ±12,3 pg/mL (-2.4%; P= ,5268) was seen across the sametime period when no occlusion was applied. This chronictestosterone change represented a clear difference (ES0,85 ± 0,82) between the 2 interventions.

DiscussionOur data demonstrate that the intermittent applicationof a 180-mmHg occlusive stimulus to the lower limbsduring exercise significantly enhances multiple training

gains from 3-week structured training blocks comparedwith nonoccluded training in trained male athletes. Theability of bilateral BFR training applied to the lowerbody to enhance upper-body strength gains is suggestiveof a systemic mechanism that is not limited to localizedhypoxia or metabolite accumulation. Previous researchhas shown that growth hormone secretion is significantlyincreased after BFR training at low-intensity loads,̂ -̂ '*Here we present the novel finding that the bilateralocclusive intervention was also associated with differ-ential hormonal profiles, with large elevations in freetestosterone that were maintained across the trainingblock and cortisol responses that were attenuated overthe training period,

Madarame et al'^ have demonstrated a cross-transfer effect with an increase in cross-sectional areaof the elbow flexor muscles when leg exercise wasperformed with BFR. A similar phenomenon has beendemonstrated in trained athletes where BFR applied tothe limbs produced an increase in upper- and lower-chest girth and an increase in bench-press strength,^Our data showing an improvement in bench-pressstrength corroborate these findings by demonstratingthat the application of an occlusion cuff to the lowerlimbs can modulate adaptation in the upper body. Itshould also be noted that the strength gains seen in thecurrent study, and those reported by Yamanaka et aPin trained athletes, were achieved in relatively shorttime frames ( 3 ^ wk) and only 9 to 12 experimentalintervention sessions, suggestive of an acceleratedtime course of adaptation compared with nonoccludedtraining,22

170 Cook, Kilduff, and Beaven

Time relative to 3-week training block|~äcontrol "BFR |

Figure 2 — Salivary hormone responses to selected sessionswithin a rugby preseason training block with or without occlusion.Solid bar: 180-mmHg occlusion applied to the lower limbs duringexercise. White bar: no occlusion stimulus applied during train-ing. Percent change: Change in salivary hormone concentrationsfrom data collected before 1 training session to data collectedafter the same training session. Abbreviations: BFR, blood-flowrestriction. **P < .01. Error bars represent standard deviations.

A number of mechanisms have the potential toexplain the systemic adaptations seen in response to thecombination of BFR and resistance exercise. Elevatedsystemic blood lactate levels have been consistentlyreported after occlusion.*'^'" The low pH resultant fromelevated lactate stimulates sympathetic nerve activity,and this pathway has been shown to be involved in thesecretion of human growth hormone.^^ Large increasesin growth hormone concentration have been commonlyreported with BFR training,"*"*'* and, although the role ofgrowth hormone in muscular hypertrophy is equivocal,it does appear to have some permissive effects whencombined with resistance exercise.̂ "*

The hypoxic and acidic intramuscular milieu resultingfrom BFR has also been hypothesized to result in addi-tional motor-unit recruitment,"^ and electromyographicdata have demonstrated enhanced muscle activation in thepectoralis major in response to BFR of the upper limbs.^'Furthermore, BFR combined with low-intensity resistanceexercise has been shown to potentiate the skeletal-muscleexpression of mRNA responsible for angiogenesis,' ' attenu-ate the mRNA expression of proteolytic transcripts,' andenhance the phosphorylation of downstream targets of the

mTOR-signaling pathway, extracellular signal-regulatedkinases, and increase muscle protein synthesis.*' It is alsoknown that the application of an intermittent ischémiestimulus to the upper arm using a blood-pressure cuff canproduce cardioprotective effects in humans.̂ ^ All of thesemechanisms demonstrate the potential of BFR training toelicit remote training effects.

Our study shows for the first time consistent andocclusion-dependent elevations in salivary testosteroneimmediately after resistance-exercise sessions. Althoughthe dose-reliance hypothesis of testosterone in relationto muscle hypertrophy via protein accretion has beenchallenged,^^ data do strongly suggest that a testosteroneconcentration within the normal physiological range isrequisite for a normal adaptive response to resistanceexercise.'^''' The correlations observed in the currentwork between acute testosterone responses and functionalstrength gains agree with earlier work demonstrating thatelevated testosterone concentrations during exercise arerelated to improved adaptation.'̂ '̂ ^^^ As a result, testos-terone can be described as playing a permissive role inactualizing specific functional adaptations.^'

It should be noted that previous studies investigatingBFR failed to observe acute testosterone increases. '̂-''-''- '̂' Itis possible that the more intense nature of the exercise pre-scribed (70% of 1 -RM), the intermittent nature of the occlu-sive stimulus, and/or the sampling methodology (saliva vsplasma) contributed to the different results observed in thisstudy. Saliva samples may provide more physiologicallyrelevant endocrine information, as they empirically reflectthe free-steroid levels capable of interacting with hormonereceptors'' and can exhibit a more dynamic response toexercise than the total blood hormone concentrations.-" It isalso reasonable to assume that the physiological phenomenaassociated with numerous large and rapid reperfusion cyclesbetween exercise sets would differ from those experiencedwith a continuous occlusion protocol.

Salivary cortisol was also observed to increase inresponse to both occluded and nonoccluded training, withlarger increases resulting from BFR training. It seemsreasonable to speculate that the addition of occlusionimposes additional (non-weight-load dependent) meta-bolic stress, with similar results having been previouslyobserved in response to BFR exercise.*-^" The cortisolresponse to BFR training was attenuated across the3-week training block (albeit only to tbe level seen in thenonoccluded training), while the cortisol response to thenonoccluded training remained relatively consistent. Thisattenuation is probably indicative of a stress adaptation tothe BFR exercise, and the degree of familiarization witbthe occlusive stimulus or the salivary collection methodmay partially explain the lack of cortisol responsesobserved in earlier studies'*'* that contrast with our data.

Practical ApplicationsOur data demonstrate that bilateral lower-limb BFRtraining was more beneficial than traditional resistancetraining in terms of increasing strength, power, and speed

Occlusion and Strength Training 171

measures in trained male athletes over a relatively short3-week training block. These results are suggestive of anadvantage of combining occlusion with moderate resis-tance loads (70% 1-RM) in eliciting strength and powergains during an intense training phase or potentiallywithin a competitive season. It is also worth consideringthe potential benefits of BFR training on athletes return-ing from injury or those who are not able to toleratehigh loads due to tendon- and joint-loading issues. Wealso demonstrate herein that the significant functionalbenefits of BFR training in an elite group correlate withenhanced salivary testosterone responses to the exercisesessions. While any causal relationship remains equivo-cal, it is apparent that acute hormonal elevations maycontribute to the cross-transfer signaling effects observedwith increases in upper-body strength in response to thelower-body occlusive stimulus.

ConclusionsBilateral lower-limb BFR training with a moderate loadproduced significant benefits compared with nonœcludedtraining and thus can be considered an effective trainingstimulus capable of eliciting functional improvementsin well-trained athletes. The distinct salivary hormonalprofile associated with BFR training and the observedcorrelation between testosterone and strength and powermeasures are suggestive of an important role for endog-enous steroids in actualizing functional gains.

AcknowledgmentsWe wish to express our gratitude for the time and effort givenfreely by squad members and management.

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