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Peak ATP: Studien / klinische Tests Beta TOR: Studien / klinische Tests

Journal of Strength and Conditioning Research Publish Ahead of PrintDOI: 10.1519/JSC.0000000000002198

A SINGLE DOSE OF ORAL ATP SUPPLEMENTATION IMPROVES

PERFORMANCE AND PHYSIOLOGICAL RESPONSE DURING LOWER BODY

RESISTANCE EXERCISE IN RECREATIONAL RESISTANCE TRAINED MALES

Short title: ATP supplementation and performance inresistance trained males.

Marcelo C. Freitas,1 Jason M. Cholewa,2 Jose Gerosa-Neto,1 Daniela C. Gonçalves,3 Erico C. Caperuto,4 Fábio S. Lira,1 Fabrício E. Rossi*5.

1 Exercise and Immunometabolism Research Group, Department of Physical Education, São Paulo State University (UNESP), Presidente Prudente, SP, Brazil. 2 Department of Kinesiology, Recreation, and Sport Studies, Coastal Carolina University,

Conway, SC, USA.

3 Biosciences Department, universidade Federal de São Paulo, UNIFESP, Santos, SP, Brazil.

4 University São Judas Tadeu. São Paulo, SP, Brazil.

5 Immunometabolism of Skeletal Muscle and Exercise Research Group, Department of

Physical Education, Federal University of Piauí (UFPI), Teresina, PI, Brazil.

*Corresponding Author Fabrício E. Rossi.

Department of Physical Education, Federal University of Piauí (UFPI), “Ministro

Petrônio Portella” Campus, 64049-550, Teresina-PI, Brazil. Telephone: (86)3215-5525,

Fax (86)3215-55264391. e-mail: rossifabricio@yahoo.com.br

ACCEPTED

Copyright ª 2017 National Strength and Conditioning Association

SHORT REPORT Open Access

Adenosine-5'-triphosphate (ATP) supplementationimproves low peak muscle torque and torquefatigue during repeated high intensity exercisesetsJohn A Rathmacher1,2*, John C Fuller Jr2, Shawn M Baier2, Naji N Abumrad3, Hector F Angus4 and Rick L Sharp4

Abstract

Background: Intracellular concentrations of adenosine-5’-triphosphate (ATP) are many times greater thanextracellular concentrations (1–10 mM versus 10–100 nM, respectively) and cellular release of ATP is tightlycontrolled. Transient rises in extracellular ATP and its metabolite adenosine have important signaling roles; andacting through purinergic receptors, can increase blood flow and oxygenation of tissues; and act asneurotransmitters. Increased blood flow not only increases substrate availability but may also aid in recoverythrough removal of metabolic waste products allowing muscles to accomplish more work with less fatigue. Theobjective of the present study was to determine if supplemental ATP would improve muscle torque, power, work,or fatigue during repeated bouts of high intensity resistance exercise.

Methods: Sixteen participants (8 male and 8 female; ages: 21–34 years) were enrolled in a double-blinded,placebo-controlled study using a crossover design. The participants received either supplemental ATP (400 mg/ddivided into 2 daily doses) or placebo for 15 d. After an overnight fast, participants underwent strength and fatiguetesting, consisting of 3 sets of 50 maximal knee extensions performed on a Biodex® leg dynamometer.

Results: No differences were detected in high peak torque, power, or total work with ATP supplementation;however, low peak torque in set 2 was significantly improved (p < 0.01). Additionally, in set 3, a trend was detectedfor less torque fatigue with ATP supplementation (p < 0.10).

Conclusions: Supplementation with 400 mg ATP/d for 15 days tended to reduce muscle fatigue and improved aparticipant’s ability to maintain a higher force output at the end of an exhaustive exercise bout.

Keywords: ATP, Adenosine-5’-triphosphate, Muscle strength, Muscle fatigue

BackgroundThe intracellular role of ATP as the energy source fortissues has long been recognized [1]. However, the extra-cellular metabolic functions of ATP have only recentlybeen investigated, and primary to this function is therole of ATP in signal transduction through purinergicreceptors found in most cell types [2]. Extracellularfunctions of ATP include vasodilation [3] and reduced

pain perception [4]. Additionally, ATP is often referredto as a cotransmitter that affects local tissue changes inneurotransmission and neuromodulation by acting uponboth peripheral and central nervous systems [5,6].Whereas intracellular concentrations of ATP are rela-

tively high (1-10 mM), extracellular concentrations aretightly regulated at very low levels (10-100 nM) [7,8].When ATP is infused into the arterial blood flow of mus-cle, the half-life has been shown to be <1 second [9] asATP is rapidly degraded to adenosine by several surface-expressed and soluble enzymes of the ectonucleosidefamilies [10]. ATP in blood is primarily carried by erythro-cytes [8]. Therefore, measurement of circulating free

* Correspondence: Rathmacher@mti-hmb.com1Department of Animal Science, Iowa State University, Ames, IA 50010, USA2Metabolic Technologies Inc, Iowa State University Research Park, Ames, IA50010, USAFull list of author information is available at the end of the article

© 2012 Rathmacher et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of theCreative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,distribution, and reproduction in any medium, provided the original work is properly cited.

Rathmacher et al. Journal of the International Society of Sports Nutrition 2012, 9:48http://www.jissn.com/content/9/1/48

RESEARCH Open Access

Effects of oral adenosine-5′-triphosphatesupplementation on athletic performance,skeletal muscle hypertrophy and recovery inresistance-trained menJacob M Wilson1*, Jordan M Joy1, Ryan P Lowery1, Michael D Roberts2, Christopher M Lockwood3,Anssi H Manninen4, John C Fuller Jr.5, Eduardo O De Souza6, Shawn M Baier5, Stephanie MC Wilson7

and John A Rathmacher5,8

Abstract

Background: Currently, there is a lack of studies examining the effects of adenosine-5′-triphosphate (ATP)supplementation utilizing a long-term, periodized resistance-training program (RT) in resistance-trained populations.Therefore, we investigated the effects of 12 weeks of 400 mg per day of oral ATP on muscular adaptations intrained individuals. We also sought to determine the effects of ATP on muscle protein breakdown, cortisol, andperformance during an overreaching cycle.

Methods: The study was a 3-phase randomized, double-blind, and placebo- and diet-controlled intervention. Phase1 was a periodized resistance-training program. Phase 2 consisted of a two week overreaching cycle in whichvolume and frequency were increased followed by a 2-week taper (Phase 3). Muscle mass, strength, and powerwere examined at weeks 0, 4, 8, and 12 to assess the chronic effects of ATP; assessment performance variables alsooccurred at the end of weeks 9 and 10, corresponding to the mid and endpoints of the overreaching cycle.

Results: There were time (p < 0.001), and group x time effects for increased total body strength (+55.3 ± 6.0 kgATP vs. + 22.4 ± 7.1 kg placebo, p < 0.001); increased vertical jump power (+ 796 ± 75 ATP vs. 614 ± 52 wattsplacebo, p < 0.001); and greater ultrasound determined muscle thickness (+4.9 ± 1.0 ATP vs. (2.5 ± 0.6 mm placebo,p < 0.02) with ATP supplementation. During the overreaching cycle, there were group x time effects for strengthand power, which decreased to a greater extent in the placebo group. Protein breakdown was also lower in theATP group.

Conclusions: Our results suggest oral ATP supplementation may enhance muscular adaptations following 12-weeksof resistance training, and prevent decrements in performance following overreaching. No statistically or clinicallysignificant changes in blood chemistry or hematology were observed.

Trial registration: ClinicalTrials.gov NCT01508338

Keywords: Adenosine triphosphate, Exercise performance, Power, Strength, Muscle hypertrophy, Sports nutrition

* Correspondence: jmwilson@ut.edu1Department of Health Sciences and Human Performance, The University ofTampa, Tampa FL, USAFull list of author information is available at the end of the article

© 2013 Wilson et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly cited.

Wilson et al. Nutrition & Metabolism 2013, 10:57http://www.nutritionandmetabolism.com/content/10/1/57

�is is an Open Access article distributed under the terms of the Creative Commons At-tribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Copyright © 2018 Korean Society of Exercise Rehabilitation http://www.e-jer.org pISSN 2288-176XeISSN 2288-1778

671

*Corresponding author: Fabrício Eduardo Rossi https://orcid.org/0000-0002-0594-2529

Department of Physical Education, Federal University of Piauí (UFPI), “Ministro Petrônio Portella” Campus, 64049-550, Teresina-PI, BrazilTel: +86-3215-5525, Fax: +86-3215-55264391, E-mail: rossifabricio@yahoo.com.brReceived: May 13, 2018 / Accepted: July 14, 2018

Oral adenosine 5 -triphosphate supplementation improved hemodynamic and autonomic parameters after exercise in hypertensive womenMarcelo Conrado de Freitas1,2, Ana Laura Ricci-Vitor3, Renan Valero Freire1, Erico Chagas Caperuto4, Luiz Carlos Marques Vanderlei3, Fábio Santos Lira5, Fabrício Eduardo Rossi6,*

1 Skeletal Muscle Assessment Laboratory (LABSIM), São Paulo State University (UNESP), School of Technology and Sciences, Department of Physical Education, Presidente Prudente, Brazil

2Department of Nutrition, São Paulo Western University-UNOESTE, Presidente Prudente, Brazil3Department of Physiotherapy, São Paulo State University (UNESP), Presidente Prudente, Brazil4University São Judas Tadeu, São Paulo, Brazil5Exercise and Immunometabolism Research Group, Department of Physical Education, São Paulo State University (UNESP), Presidente Prudente, Brazil6Immunometabolism of Skeletal Muscle and Exercise Research Group, Department of Physical Education, Federal University of Piauí (UFPI), Teresina, Brazil

The aim of this study was to verify the autonomic modulation and blood pressure after adenosine-5’-triphosphate (ATP) supplementation asso-ciated to acute aerobic exercise in hypertensive women. Eleven hyper-tensive women (age, 61.8± 5.0 years) completed a randomized, double blind trial: ATP supplement condition (ATP= 400 mg) or placebo. After 30 min of supplementation or placebo intake, the subjects performed 30 min of aerobic exercise (70%–75% of maximum heart rate). The auto-nomic modulation was assessed by heart rate variability during rest and recovery (postexercise until 30 min of recovery), the square root of the mean squared difference between adjacent RR intervals (RMSSD), standard deviation of successive values (SDNN), low frequency (LF) and high frequency (HF) were measured. The blood pressure (systolic blood pressure [SBP] and diastolic blood pressure, mmHg) were re-corded at rest, immediately postexercise, post-10, post-20, and post-30 min after exercise. For RMSSD, there was statistically significant differ-

ence during recovery, with higher RMSSD for ATP compared to placebo (rest= 16.4± 8.5 vs. placebo= 11.6± 4.0; ATP= 18.5± 9.7 msec; P= 0.020). When analyzing the delta (recovery minus rest), the RMSSD (ATP= 2.1± 7.2 msec vs. placebo= -4.7± 7.5 msec; P= 0.009), LF (ATP= -19.8± 122.7 vs. placebo= -94.1± 200.2 msec2; P= 0.02), and SDNN (ATP= -2.8± 12.2 msec vs. placebo= -10.6± 10.5 msec; P= 0.010) were higher for ATP than placebo. Furthermore, there was a greater postexercise hypotension at 20 min for ATP (SBP: ATP= -13.2± 8.4 mmHg vs. placebo= -6.1± 9.9 mmHg; P= 0.006). Acute ATP supplementation promoted greater postexercise hypotension for systolic blood pressure and induced faster recovery of heart rate variability in hypertensive women.

Keywords: Aerobic exercise, ATP supplementation, Nutrition, Autonom-ic nervous system, Hypertension

INTRODUCTION

High blood pressure has been associated with cardiovascular risk and mortality (Heidenreich et al., 2011; Mozaffarian et al., 2015), and this disease is considered a major public health prob-lem, with worldwide prevalence rate around one billion and in-creasing direct healthcare costs (Kearney et al., 2005; Mills et al.,

2016; Ostchega et al., 2008). Furthermore, previous studies demonstrated that hypertensive subjects have several dysfunctions on the autonomic nervous system (ANS) and vascular tissue (Grassi and Ram, 2016; Kario et al., 1997), generating the in-crease of blood pressure. On the other hand, regular exercise has been effective in preventing this disease and is strongly recom-mended for hypertension treatment (Besnier et al., 2017; Corne-

https://doi.org/10.12965/jer.1836256.128

Original Article

Journal of Exercise Rehabilitation 2018;14(4):671-679

in offspring of sows fed HMB for the final 2 weeks of preg-nancy; increased bone density and plasma amino acid con-centrations in pigs with fundectomy-induced osteopaenia(23);and improved somatotrophic axis and accelerated bone meta-bolism in lambs fed HMB for the first 21 d after birth(24). Theimprovement in somatotrophic axis function was furtherdemonstrated in rats when chronic HMB administration wasshown to stimulate the GH/IGF-1 axis(25). Recently, HMB sup-plementation was shown to enhance the exercise-stimulatedincrease in GH and IGF-1 response in humans, similar to whatthe previous studies in animals had demonstrated(26).The pharmacokinetics of orally ingested Ca-HMB in

capsules were originally described by Vukovich et al.(14)

and showed a time to peak plasma level of HMB of 2 h aftera 1 g dosage. Recently, Fuller et al.(15) demonstrated thatHMB-FA gel form increased plasma HMB concentrationsin a shorter period of time (30–40 min) with a greaterblood clearance rate of HMB compared with the Ca-HMBcapsule. A recent 12-week exercise study by Wilson et al.(27)

used these favourable advantages to test the efficacy ofHMB-FA administered 30min before exercise in a periodisedtraining programme and showed increased strength, lean bodymass gain and muscle power in a highly trained athletepopulation(27), demonstrating the importance of dosage timingand peak levels of HMB for maximisation of exercisebenefits. The current human study was thus designed tocompare the pharmacokinetics of the current commerciallyavailable delivery form of Ca-HMB in a capsule and comparedthis with the newly designed delivery form of HMB-FA in agelcap. Our results confirmed the previous findings of Fulleret al.(15) and showed that HMB-FA had superior bioavailabilityin humans as assessed by blood levels, and improvedclearance.

Methods

Human subjects

We performed a randomised crossover study consisting offive men and five women (aged 21–32 years). The study wasconducted according to the guidelines laid down in theDeclaration of Helsinki, and all procedures involving humansubjects were approved by the Iowa State UniversityInstitutional Review Board. Written informed consent wasobtained from all subjects before participation. The study waslisted on ClinicalTrials.gov (NCT01914952, https://clinicaltrials.gov). The subjects were not currently taking amino acid, proteinor HMB supplements.

Treatments

The treatments were given to each subject in random order withat least a 48 h washout period between treatments. The treat-ments were as follows: (1) Ca-HMB in a commercial gelatincapsule (Optimum Nutrition); (2) HMB-FA capsule (gelcap)(Capsugel); (3) HMB-FA as a gel as previously described(15);(4) Ca-HMB mixed in water or (5) HMB-FA mixed in water.All treatments delivered 0·8 g of HMB orally, confirmed by

HPLC analysis, and were given with 355 ml of water. Althoughthe pH of the free acid itself is <3, this is similar to the pH of thestomach. For the treatments used in this study, the free acidwas given either in capsule form, a buffered gel form or as adilute solution in water. In contrast, the Ca-HMB is neutral toslightly alkaline when in solution. None of the participantsreported any oesophageal or gastrointestinal irritations with anyof the treatment forms of HMB. For the capsule treatments,samples of the capsules were sent to an independent laboratoryand tested for dissolution times (Eurofins). Because of thenature of the various treatments, the study could not be fullyblinded.

Study design

All studies were conducted after a 10- to 12-h overnight fast.Subjects arrived at the laboratory in the morning, and anintravenous catheter was inserted into a forearm vein usingsterile procedures. A preingestion blood sample, of approxi-mately 7 ml, was drawn. The treatment was then consumedover approximately a 2 min period, and additional blood sam-ples (7 ml) were taken at 2, 5, 10, 15, 25, 35, 45, 60, 90, 120, 180,360 (6 h), 720 (12 h) and 1440 (24 h) min after the ingestion ofthe supplement; 24 h urine collection was also obtained. Plasmaand urine samples were stored at −80°C until later analyses ofHMB. Serum and blood samples at times 0 and 1440 min wereanalysed by a commercial laboratory (LabCorp.) for glucose,uric acid, blood urea nitrogen, creatinine, Na, K, Cl, Ca, CO2, P,protein, albumin, globulin, total bilirubin, alkaline phosphatase,estimated glomerular filtration rate (eGFR), creatine kinase,lactate dehydrogenase, aspartate aminotransferase, alanineaminotransferase, γ-glutamyl transpeptidase, Fe, TAG, HDL,LDL, VLDL and cholesterol; a complete blood count was alsoperformed. Subjects completed a brief health questionnaire toreport any physical symptoms (such as nausea, headache andso on) they may have experienced during the experiment.

After the 180 min blood sampling, each subject was providedwith a standardised lunch (1673·6–2092 kJ (400–500 kcal)),which was consumed at approximately 240min postingestion;the subjects returned to the laboratory for the 720 min bloodsample. Each subject was then instructed to eat a normal eve-ning meal before 22.00 hours. Subjects were also instructed torefrain from any strenuous physical activity or exercise duringeach testing period, and diet and activity patterns were to bereplicated for each treatment testing period. Subjects reportedback to the laboratory the following morning for the fasted1440 min blood sample. Urine collection containers were pro-vided, and subjects collected all urine produced during the 24 hexperimental period. The urine was stored refrigerated whenpossible.

Plasma and urine β-hydroxy-β-methylbutyrate analysis

The plasma and urine HMB were analysed as previouslydescribed using GC/MS(28). Briefly, HMB in the free acid form isquantified from standards using d6-HMB as an internal standard.This method has a CV of approximately 4·1 %.

1404 J. C. Fuller et al.

Statistical analysis and calculations

The AUC was calculated for each subject using the trapezoidalmethod that sums the area above the baseline(29). The followingequations were used in the calculation of the half-life ofplasma HMB:

Kel ¼ln Cpeak

� �� ln Ctrough

� �

Tinterval

; (1)

t1=2

¼ 0�693Kel

: (2)

The peak plasma concentration was the highest HMBconcentration at a measured time point for each subject andwas used for Cpeak. Trough concentrations, Ctrough, were theconcentrations measured at 12 h, which were not significantlydifferent from baseline concentrations. The Tpeak was the timeat which Cpeak was measured for each subject and Tinterval was12 h (time at Ctrough) minus Tpeak. The extracellular fluidcompartment was assumed to be 20 % of body weight. Vd wascalculated using equation (3) below(30). The plasma clearanceof HMB was calculated by multiplying the extracellular fluidcompartment, Vd, by the elimination constant, Kel, as shown inequation (4)(31).

Vd ¼ Bodyweight 0�20ð Þ; (3)

Clearance ¼ Vd Kelð Þ: (4)

The data for comparable treatments were analysed using acrossover design with the general linear models (GLM) proce-dure in SAS(32). A priori power analysis (G*Power, version 3.1.7)was completed based on our previously published pharmaco-kinetic study(15). Assuming a similar degree of variability, apower analysis indicated that ten subjects were required todetect a P value of 0·05 at a power of 0·90 in a crossoverdesigned study. A repeated-measures polynomial model wasused for the timed sampling of plasma HMB, and the modelincluded subject, treatment order, treatment main effects andtime by treatment interaction where appropriate. For otherparameters, Proc GLM was used with subject, treatment orderand treatment main effects included in the model, and theP values are reported for the treatment main effect. Althoughthe study was neither designed nor powered to detect sexdifferences, sex by treatment interaction was determined byGLM. In addition, the main effects of Ca-HMB and HMB-FAwhen given in water and by capsule were determined usingGLM and least square means, and these data are shown inonline Supplementary Table S3. Statistical significance wasdetermined for P< 0·05.

Results

Subject characteristics

Subject characteristics of the five male and five female subjectsare shown Table 1. The average age of the subjects was25·1 (SEM 1·0) years and the average weight and BMI were69·1 (SEM 3·1) kg and 23·0 (SEM 0·8) kg, respectively. The malesubjects had greater body weights (P< 0·05) and BMI (P< 0·05)than the female subjects; however, there were no significant sex

by treatment interactions for any of the pharmacokinetic para-meters measured, even though all subjects were administeredthe same HMB dose.

Free acid form of β-hydroxy-β-methylbutyrate gel kinetics

The HMB-FA gel treatment in the present study showedsimilar pharmacokinetics as we had previously shown(15).HMB-FA in a gel had no comparator in the current study. TheCpeak was 261·7 (SEM 15·0) µmol/l at 35·5 (SEM 4·0)min post-administration. The half-life of HMB delivered in the gel form was2.24 (SEM 0·10) h and the AUC was 54·1 (SEM 3·1) µmol/l×1440min. The clearance from plasma was 71·7 (SEM 3·6)ml/min, and24·6 (SEM 4·4) % of the dosage was excreted in urine over the24 h study.

Acute β-hydroxy-β-methylbutyrate kinetics for capsule andwater administration

The 3 h plasma HMB pharmacokinetics for subjects adminis-tered the HMB-FA and Ca-HMB capsule treatments are shownin Fig. 1(a). Compared with Ca-HMB capsules, HMB-FAadministration in capsules resulted in significantly greaterplasma levels at all time points from 15 to 120min afteradministration (P< 0·001 at 15, 25, 35, 45, 60 and 90 min andP< 0·05 at 120min). The 180 min AUC was 75 % greater(P< 0·001) for the HMB-FA in capsule form. In addition,administration of HMB-FA in capsule form resulted in 76 %greater peak levels (P< 0·006) in one-third the time (P< 0·009).The dissolution time of the capsules could not account for theseresults; it was 13 min for the HMB-FA capsules and 5min for theCa-HMB capsules, thus favouring the release of Ca-HMB fromthe capsules.

Fig. 1(b) shows the 3 h plasma HMB pharmacokineticsfor the administration of HMB-FA and Ca-HMB when mixed inwater. Administration of HMB-FA in water resulted in greaterplasma HMB levels at 15, 25, 35 and 45min (P< 0·05, 0·001,0·004, and P< 0·05, respectively). The inset shows that HMB-FAadministered in water had a significantly greater AUC during thefirst hour of administration (P< 0·03). Compared with Ca-HMBadministered in water, the Cpeak tended to be greater for

Table 1. Subject descriptors(Mean values with their standard errors)

Mean SEM

Sex (n)Male/female 5/5

Age (years) 25·1 1·0Body weight (kg)

All 69·1 3·1Female 64·3 3·0Male 73·8 4·9

BMI (kg/m2)All 23·0 0·8Female 21·9 0·8Male 24·2 1·3

β-Hydroxy-β-methylbutyric acid clearance 1405

HMB-FA in water, whereas the Tpeak level was not differentbetween the HMB-FA and Ca-HMB treatments.

24 h β-hydroxy-β-methylbutyrate kinetics for capsule andwater administration

Fig. 2(a) shows the 24 h plasma HMB levels in subjects giveneither Ca-HMB or HMB-FA in capsule form. As shown in theinset, the HMB-FA capsule administration resulted in a 37 %increased clearance of HMB from plasma (P< 0·0001), resultingin a 29 % decrease in half-life (P< 0·0003). The 24 h AUC forHMB and for urinary excretion rates were the same for bothforms.Similarly, Fig. 2(b) shows the 24 h plasma HMB levels in

subjects given either Ca-HMB or HMB-FA mixed in water. Wenoted significant differences in plasma HMB levels during thefirst hour, with no further observed differences during the 24 hmeasurement period. As seen in the inset, there were also nodifferences observed for plasma HMB half-life, clearance ratesor AUC over the 24 h measurement period. In addition, 24 hurinary excretion as a percentage of the initial dose was thesame for both treatments.

Blood chemistry and haematology

There were no untoward effects of the treatments on bloodchemistries or haematology and the data are presented inonline Supplementary Tables S1 and S2.

Discussion

In this study, we tested the human pharmacokinetics of the twocommercially available forms of HMB, used for the promotionof muscular strength and mass. Our results demonstrate that,irrespective of the capsule delivery form used, HMB-FA is morereadily available and has a higher clearance rate than Ca-HMB(Fig. 2(a)), indicative of higher efficiency and faster utilisation.All human studies to date have consistently demonstrated thesuperiority of the HMB-FA form to reach a higher HMB plasmapeak in a much shorter time than the Ca-HMB form, with similarurinary excretion of HMB(14,15). When Ca-HMB was adminis-tered, peak plasma HMB levels were 115(14), 131(15) and131 µmol/l(15), which were comparable to the 154 µmol/l deter-mined in the current study. Previous studies with HMB-FA foundthe peak plasma HMB levels to be 259(15) and 239 µmol/l(15)

300

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0

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00 1 2 3

Time (h)

0 1 2 3

Time (h)

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sma

HM

B (

µmo

l/l)

Pla

sma

HM

B (

µmo

l/l)

Cpeak (µmol/l)

Tpeak (min)

AUC (µmol/l × 180 min)

Cpeak (µmol/l)

Tpeak (min)

AUC (µmol/l × 60 min)

HMB-FA water Ca-HMB water

HMB-FA capsule Ca-HMB capsule

Mean SEM Mean SEM P

Mean SEM Mean SEM P

270.2

44.5

28.3

17.8

5.5

1.4

153.9

133.5

16.2

17.9

29.2

1.8

0.006

0.009

0.001

274.4

36.0

10.9

24.6

2.8

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247.4

42.5

9.1

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4.1

0.9

0.11

0.23

0.03

***

***

***

****** *** ***

*

**

*

*

(b)

(a)

Fig. 1. (a) The 3 h plasma levels of β-hydroxy-β-methylbutyrate (HMB) after administration of either free acid form of HMB (HMB-FA) gelcaps (-●-) or Ca salt of HMB(Ca-HMB) capsule (- -○-). (b) The 3 h plasma levels of HMB after administration of either HMB-FA mixed in water (-●-) or Ca-HMB mixed in water (- -○-). All treatmentscontained 0·8 g of HMB. Values are means with their standard error of means for five men and five women. Significance between the treatments is indicated as follows:* P< 0·05; ** P< 0·004; and *** P< 0·001. The inset table shows the peak concentration reached (Cpeak), time to reach peak concentration (Tpeak) and AUC.The P value indicated is for differences between the treatment means.

1406 J. C. Fuller et al.

for the gel form, which was equivalent to the levels, 262 and270 µmol/l for the gel and gelcap, respectively, in the currentstudy. Similarly, the times to peak HMB level previously deter-mined for Ca-HMB administration were 120(14), 122(15) and 135min(15), which are comparable to the 134min in the current study.When HMB-FA was administered in a gel, the times to peak levelswere 33(15) and 42min(15), and in the current study the times topeak level for HMB-FA as a gel and gelcap were 36 and 45min,respectively. Urinary losses were similar across all studies anddosage forms, and including our present study were between 14and 25% of the dosage(14,15). The findings have several practicalimplications for the average athlete. Although both forms of HMBare equally effective on muscle function and are equally retainedby the body over a 24 h period, the use of HMB-FA allows formore predictive timing of intake of HMB in relation to the plannedexercise, thus achieving better outcomes, as was recently con-firmed by Wilson et al.(27).Our human data differ considerably from the recently pub-

lished data in rodents(33), which reported that Ca-HMB hadbetter availability as measured by peak blood levels whencompared with HMB-FA. In that study, the investigators com-pared Ca-HMB with HMB-FA administration both orally in aliquid suspension and by intravenous injection,(33) and showed

that similar amounts of HMB given as either Ca-HMB orHMB-FA resulted in the Ca-HMB having greater peak bloodHMB concentrations. There are several concerns with com-parison with the rodent study; the most notable is the concernrelated to species differences. For example, the half-life of HMBin blood after Ca-HMB dosing is reported as approximately 1, 2and 3 h for the rat, pig and sheep, respectively(33–35), comparedwith humans, with a half-life of 2·4 to 3·2 h for a 1 g dosage ofCa-HMB(14,15). Other concerns relate to the experimentaldesign, and the analytical methods used, as well as methodo-logical differences related to the accuracy of HMB intake. Forexample, in the rodent study, there is no mention of themethodology for the administration of the oral forms in themethods section of the paper; hence, the method and accuracyof the amount given is in question. In addition, both forms ofHMB were dissolved in solutions containing carboxy-methylcellulose and Tween 80 with the pH adjusted to 4·5. Thistype of solution is likely to affect the bioavailability of theCa-HMB by increasing its ionisation, dissociation and absorp-tion, thus leading to overestimates of the true pharmacokineticparameters measured. Last, but not least, there is concernrelated to the accuracy of the measured plasma HMB levels.The authors used warfarin, which is structurally different fromthe natural HMB form, as an internal standard for the LC-MS/MSmeasurements, in contrast to our use of a similar HMBcompound, namely d6-HMB, as an internal standard(36).

To reconcile any potential differences attributed to thedelivery forms, we carried out a head-to-head comparison of anoral dose of HMB-FA and Ca-HMB given mixed in water insteadof in capsule form. The data from the current study confirm ourprevious findings(15) and demonstrate that even when deliveredmixed in water HMB-FA is still superior to Ca-HMB in deliveringHMB, albeit to lesser degree than when both forms are deliv-ered in capsules. This was quite evident within the first hour ofthe absorptive period (Fig. 1(b)). In addition, we noted nodifference in 24 h urinary excretion of HMB (Fig. 2(b)),suggesting an earlier and greater tissue availability of HMBwhen given in the free acid form.

Our study has few limitations, albeit minor in nature. The firstlimitation relates to the few number of subjects studied (n 10);this limitation, however, is countered by the use of the subjectsas their own control in a crossover design. Another theoreticallimitation may relate to our calculation of the amount of HMBavailable for tissue utilisation, as the difference between theamount consumed minus the amount excreted in the urine. Thisassumption would be accurate with additional measurement ofHMB oxidation rates, which were not examined in this study.Wilkinson et al.(11) recently demonstrated that after an oraldosage of HMB-FA intramuscular HMB concentrationsincreased almost 14-fold from baseline at 150 min after thedose, suggestive of enhanced utilisation of HMB by humanmuscle following intake of HMB-FA.

In conclusion, the use of the commercially available forms ofHMB as either the HMB-FA or Ca-HMB resulted in earlier andincreased plasma concentrations, with increased clearancerates, when the HMB was given as HMB-FA. This finding can beused favourably by athletes to gauge their intake of HMB beforean exercise bout, as recently observed by Wilson et al.(27).

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(µm

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(µm

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)

HMB-FA water Ca-HMB water

Mean SEM Mean SEM P

HMB-FA capsule Ca-HMB capsule

Mean SEM Mean SEM P

2.23

72.0

52.3

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0.10

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3.4

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2.30

70.7

54.6

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2.15

74.8

53.8

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0.07

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3.02

54.5

48.8

20.3

0.24

3.2

3.7

3.2

0.0003

0.0001

0.16

0.65

(b)

(a)

Fig. 2. (a) The 24 h plasma levels of β-hydroxy-β-methylbutyrate (HMB) afteradministration of either free acid form of HMB (HMB-FA) gelcaps (-●-) or Casalt of HMB (Ca-HMB) capsule (- -○-). (b) The 24 h plasma levels of HMB afteradministration of either HMB-FA mixed in water (-●-) or Ca-HMB mixed in water(- -○-). All treatments contained 0·8 g of HMB. See Fig. 1 for significantdifferences in plasma HMB concentrations in the initial 3 h. Values are meanswith their standard error of means for five men and five women. The inset tableshows the half-life, clearance, 24 h AUC and 24 h urinary excretion of HMB.The P value indicated is for differences between the treatment means.

β-Hydroxy-β-methylbutyric acid clearance 1407

Acknowledgements

The present study was funded by Metabolic Technologies, Inc.,Ames, IA.The authors’ contributions were as follows: J. A. R. designed

the research. J. A. R., H. F. A., P. Y. K. and R. L. S. conductedthe research including sample analysis. J. C. F. Jr analysed thedata and wrote the paper. J. A. R. had primary responsibility forfinal content. All authors read and approved the final manuscript.J. C. F. Jr and J. A. R. are employed by Metabolic Technolo-

gies Inc., Ames, IA. R. L. S. received funds from MetabolicTechnologies to conduct the study. H. F. A. and P. Y. K. had noconflicts of interest to declare.

Supplementary material

For supplementary material/s referred to in this article, pleasevisit http://dx.doi.org/doi:10.1017/S0007114515003050

References

1. Nissen S, Sharp R, Ray M, et al. (1996) Effect of the leucinemetabolite β-hydroxy β-methylbutyrate on muscle metabo-lism during resistance-exercise training. J Appl Physiol 81,2095–2104.

2. Panton LB, Rathmacher JA, Baier S, et al. (2000) Nutritionalsupplementation of the leucine metabolite β-hydroxyβ-methylbutyrate (HMB) during resistance training. Nutr 16,734–739.

3. Knitter AE, Panton L, Rathmacher JA, et al. (2000) Effects ofβ-hydroxy-β-methylbutyrate on muscle damage following aprolonged run. J Appl Physiol 89, 1340–1344.

4. Wilson GJ, Wilson JM & Manninen AH (2008) Effectsof beta-hydroxy-beta-methylbutyrate (HMB) on exerciseperformance and body composition across varying levels ofage, sex, and training experience: a review. Nutr Metab(Lond) 5, 1.

5. Wilson JM, Fitschen PJ, Campbell B, et al. (2013) InternationalSociety of Sports Nutrition Position Stand: beta-hydroxy-beta-methylbutyrate (HMB). J Int Soc Sports Nutr 10, 6.

6. Eley HL, Russell ST & Tisdale MJ (2008) Mechanism ofattenuation of muscle protein degradation induced by tumornecrosis factor alpha and angiotensin II by beta-hydroxy-beta-methylbutyrate. Am J Physiol Endocrinol Metab 295,E1417–E1426.

7. Smith HJ, Wyke SM & Tisdale MJ (2004) Mechanism of theattenuation of proteolysis-inducing factor stimulated proteindegradation in muscle by beta-hydroxy-beta-methylbutyrate.Cancer Res 64, 8731–8735.

8. Smith HJ, Mukerji P & Tisdale MJ (2005) Attenuationof proteasome-induced proteolysis in skeletal muscle byβ-hydroxy-β-methylbutyrate in cancer-induced muscle loss.Cancer Res 65, 277–283.

9. Eley HL, Russell ST, Baxter JH, et al. (2007) Signaling path-ways initiated by β-hydroxy-β-methylbutyrate to attenuate thedepression of protein synthesis in skeletal muscle in responseto cachectic stimuli. Am J Physiol Endocrinol Metab 293,E923–E931.

10. Eley HL, Russell ST & Tisdale MJ (2008) Attenuation ofdepression of muscle protein synthesis induced by lipopoly-saccharide, tumor necrosis factor and angiotensin II byβ-hydroxy-β-methylbutyrate. Am J Physiol Endocrinol Metab295, E1409–E1416.

11. Wilkinson DJ, Hossain T, Hill DS, et al. (2013) Effects ofleucine and its metabolite beta-hydroxy-beta-methylbutyrateon human skeletal muscle protein metabolism. J Physiol 591,2911–2923.

12. Wilson JM, Kim JS, Lee SR, et al. (2009) Acute and timingeffects of beta-hydroxy-beta-methylbutyrate (HMB) on indir-ect markers of skeletal muscle damage. Nutr Metab (Lond)6, 6.

13. Wilson JM, Lowery RP, Joy JM, et al. (2013) ) β-Hydroxy-β-methylbutyrate free acid reduces markers of exercise-induced muscle damage and improves recovery inresistance-trained men. Br J Nutr 110, 538–544.

14. Vukovich MD, Slater G, Macchi MB, et al. (2001) ) β-Hydroxy-β-methylbutyrate (HMB) kinetics and the influence of glucoseingestion in humans. J Nutr Biochem 12, 631–639.

15. Fuller JC Jr, Sharp RL, Angus HF, et al. (2011) Free acid gelform of β-hydroxy-β-methylbutyrate (HMB) improves HMBclearance from plasma in humans compared to the calciumHMB salt. Br J Nutr 105, 367–372.

16. Dreyer HC, Fujita S, Cadenas JG, et al. (2006) Resistanceexercise increases AMPK activity and reduces 4E-BP1 phos-phorylation and protein synthesis in human skeletal muscle.J Physiol 576, 613–624.

17. Phillips SM, Tipton KD, Aarsland A, et al. (1997) Mixed muscleprotein synthesis and breakdown after resistance exercisein humans. Am J Physiol 273, E99–E107.

18. Kerksick C, Harvey T, Stout J, et al. (2008) InternationalSociety of Sports Nutrition Position Stand: nutrient timing. J IntSoc Sports Nutr 5, 17.

19. American College of Sports Medicine, American DieteticAssociation & Dieticians of Canada (2000) Joint positionstatement: nutrition and athletic performance. Med Sci SportsExerc 32, 2130–2145.

20. Coyle EF, Coggan AR, Hemmert MK, et al. (1985) Substrateusage during prolonged exercise following a preexercisemeal. J Appl Physiol (1985) 59, 429–433.

21. Tatara MR (2009) Effect of beta-hydroxy-beta-methylbutyrate(HMB) administration on volumetric bone mineral density,and morphometric and mechanical properties of tibia in maleturkeys. J Anim Physiol Anim Nutr (Berl) 93, 669–677.

22. Tatara MR, Krupski W, Tymczyna B, et al. (2012) Effects ofcombined maternal administration with alpha-ketoglutarate(AKG) and beta-hydroxy-beta-methylbutyrate (HMB) on pre-natal programming of skeletal properties in the offspring. NutrMetab (Lond) 9, 39.

23. Tatara MR, Sliwa E, Krupski W, et al. (2008) 3-Hydroxy-3-methylbutyrate administration diminishes fundectomy-induced osteopenia of the lumbar spine in pigs. Nutr 24,753–760.

24. Tatara MR (2008) Neonatal programming of skeletal develop-ment in sheep is mediated by somatotrophic axis function.Exp Physiol 93, 763–772.

25. Gerlinger-Romero F, Guimaraes-Ferreira L, Giannocco G,et al. (2011) Chronic supplementation of beta-hydroxy-betamethylbutyrate (HMβ) increases the activity of the GH/IGF-Iaxis and induces hyperinsulinemia in rats. Growth Horm IGFRes 21, 57–62.

26. Townsend JR, Hoffman JR, Gonzalez AM, et al. (2015) Effectsof beta-hydroxy-beta-methylbutyrate free acid ingestion andresistance exercise on the acute endocrine response. Int JEndocrinol 2015, article ID 856708.

27. Wilson JM, Lowery RP, Joy JM, et al. (2014) The effects of12 weeks of beta-hydroxy-beta-methylbutyrate free acidsupplementation on muscle mass, strength, and power inresistance trained individuals: a randomized, double-blind,placebo-controlled study. Eur J Appl Physiol 114, 1217–1227.

1408 J. C. Fuller et al.

Comparison of availability and plasma clearance rates ofβ-hydroxy-β-methylbutyrate delivery in the free acid and calciumsalt forms

John C. Fuller Jr1, Rick L. Sharp2, Hector F. Angus2, Paul Y. Khoo2 and John A. Rathmacher1,3*1Metabolic Technologies Inc., Iowa State University Research Park, Ames, IA 50010, USA2Department of Kinesiology, Iowa State University, Ames, IA 50010, USA3Department of Animal Science, Iowa State University, Ames, IA 50010, USA

(Submitted 22 February 2015 – Final revision received 14 July 2015 – Accepted 17 July 2015 – First published online 16 September 2015)

Abstractβ-Hydroxy-β-methylbutyrate (HMB), a leucine metabolite, has long been supplemented as a Ca salt (Ca-HMB) to increase strength and performancegains with exercise and to reduce recovery time. Recently, the free acid form of HMB (HMB-FA) has become commercially available in capsule form(gelcap). The current study was conducted to compare the bioavailability of HMB using the two commercially available capsule forms of HMB-FA andCa-HMB. We also compared the pharmacokinetics of each form when administered mixed in water. Ten human subjects (five male and five female)were studied in a randomised crossover design. There was no significant sex by treatment interaction for any of the pharmacokinetic parametersmeasured. HMB-FA administered in capsules was more efficient than Ca-HMB capsule at HMB delivery with a 37% increase in plasma clearance rate(74·8 (SEM 4·0) v. 54·5 (SEM 3·2)ml/min, P<0·0001) and a 76% increase in peak plasma HMB concentration (270·2 (SEM 17·8) v. 153·9 (SEM 17·9) μmol/l,P<0·006), which was reached in one-third the time (P<0·009). When HMB-FA and Ca-HMB were administered in water, the differences still favouredHMB-FA, albeit to a lesser degree. Plasma HMB with HMB-FA administered in water was greater during the early phase of absorption (up to 45minpostadministration, P<0·05); this resulted in increased AUC during the first 60min after administration, when compared with Ca-HMB mixed in water(P<0·03). In conclusion, HMB-FA in capsule form improves clearance rate and availability of HMB compared with Ca-HMB in capsule form.

Key words: β-Hydroxy-β-methylbutyrate: Free acid form of hydroxy-β-methylbutyrate: Calcium salt of hydroxy-β-methylbutyrate:Gelcaps: Capsules: Clearance

The leucine metabolite β-hydroxy-β-methylbutyrate (HMB) has along history of use as a nutritional supplement for enhancingrecovery, and for increasing strength, power, aerobic performanceand lean body mass with exercise(1–5). HMB improves muscleprotein balance by decreasing muscle protein breakdown and byincreasing muscle protein synthesis(6–11), resulting in reducedmuscle damage and faster and improved recovery(3,12,13). Thesebenefits with HMB to improve muscle performance with vigorousexercise have generally been achieved with the Ca salt of HMB(Ca-HMB) administered in capsule form. However, as shown inprevious studies, and confirmed by the findings of the currentstudy, peak plasma levels of HMB are not reached untilapproximately 120min after ingestion of Ca-HMB, which makes itinconvenient for scheduling exercise sessions to coincide withpeak plasma HMB levels(14,15). In this study, we show that the timeto peak HMB level decreased by two-thirds when HMB wasdelivered as the free acid in capsule form (HMB-FA), thus makingit more convenient to time peak HMB level with exercise.The anabolic stimulus of exercise results in an increase in

muscle protein synthesis in as little as 1 h postexercise(16), and

it can persist for up to 48 h postexercise(17). Theseanabolic events are also accompanied by depletion of muscleenergy stores in the form of glycogen, resulting in decreasedexercise intensity, and associated with increased muscledamage(18–20). The changes have been attributed to increasedskeletal muscle AMP-activated protein kinase activity andreduced phosphorylation of 4E-BP1 in the mTOR pathway,as occurs with resistance exercise(16). HMB supplementationhas been shown to increase phosphorylation of 4E-BP1 inhuman muscle(11), prompting us to hypothesise that HMB asHMB-FA would offer a more convenient delivery form resultingin an improved anabolic effect of HMB on muscle proteinsynthesis and diminishing protein breakdown.

Other metabolic effects of HMB have been demonstratedin animal models. Turkeys fed HMB during the last 15 weeksof rearing had increased bone density and strength andan increase in some plasma amino acids including thebranched-chain amino acids(21). Tatara et al.(22) also demon-strated increased growth and bone density, and increasedgrowth hormone (GH) and insulin-like growth factor-1 (IGF-1),

* Corresponding author: Dr J. A. Rathmacher, fax +1 515 296 0908, email rathmacher@mti-hmb.com

Abbreviations: Ca-HMB, calcium salt of HMB; HMB, β-hydroxy-β-methylbutyrate; HMB-FA, free acid form of HMB.

British Journal of Nutrition (2015), 114, 1403–1409 doi:10.1017/S0007114515003050© The Authors 2015

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