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Myths and Facts About the Effects of Ischemic
Preconditioning on Performance

Article in International Journal of Sports Medicine · October 2015
DOI: 10.1055/s-0035-1564253

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Moacir Marocolo Gustavo Ribeiro Da Mota
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Simim1. by ligating the thighs for some time before start- Federal University of Triângulo ity on skeletal muscle function and effectiveness ing to run. R. Moacir Marocolo Human Performance and Sport the heart from ischemic injury by calcitonin populations before traveling long distances. The German physiologist E. Ischemic Preconditioning and Performance …  Int J Sports Med . addressed this scope. How- Mineiro on exercise performance was not well described. including a meta-analysis for both performance and physiological variables and evaluation of the quality of the papers that when comparing IPC. resulting in a reasonable number of Int J Sports Med attention [19].. the effectiveness of this pro. the conditioning”. Marocolo1. healthy subjects. 38]. 2. ­forgotten. 30. Copyrighted material. M. 45]. Physiology & Anatomy. ever. this procedure has received much decade.-J. A. Therefore. G. Dot. sports performance [23. Review Myths and Facts About the Effects of Ischemic Preconditioning on Performance Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais). but did not refer to skeletal published a paper in 1958 [42] confirming unani­ Fax:  + 55/343/3185 067 muscle function. 28. 2015 Since it was first demonstrated in vitro that eventually becomes more resistant to ischemia ischemic preconditioning (IPC) may ensure and its potential deleterious effects [34. the IPC proce- Correspondence myocardial protein kinase C [58]. Many mechanisms of IPC effect experimental researches attempting to demon- © Georg Thieme regarding tissue protection have been described strate beneficial effects of IPC on skeletal muscle Verlag KG Stuttgart · New York previously as humoral factors related to the strength [10. 54]. Department of Sport Sciences circulation nitrites [53]. early studies on blood flow occlusion and Av Tutunas 490 Most of the earlier studies demonstrated an eval.com ­co-worker Nukada [44]. Federal University of Triângulo Mineiro. Department of Sport Sciences. [all significant differences mainly described an fields]) and other online journals were searched.” combined with “exer. The few studies with Google Scholar (using [advanced search]. b) “blood flow” and “hyperemia”. This might or might not be true.05) review was performed. 39. da Mota1. e. way for cardioprotection [17]. Cologne Key words Abstract “performance”. Appell Coriolano2 1 Affiliations  Human Performance and Sport Research Group. cise performance”. Müller Brazil Tel. high quality scores (87 %). Therefore a systematic studies lacked statistical significance (P < 0. They had occluded the Marocolo M et al. subsequent work have been almost entirely 38061-500 Uberaba uated cardioprotection effect in disease condi. placebo and control groups. 32.A. up-regulation of Based on anecdotal information. if ● ▶ blood flow occlusion ▼ they conformed to strict pre-formulated criteria. M. meta-anal- ● ▶ sports the effect of ischemic preconditioning (IPC) in yses and studies with only animals or non- ● ▶ testing clinical application.:  + 55/32/9936 8901 tions [7. altered physiological parameters. “exercise” and Introduction This concept. improvement only in performance without for the following descriptors: a) “ischemic pre. influence on performance. its applicabil. 33]. Research Group gene-related peptide [59] and up-regulation of to transmit information to other communities.doi. and physiologically highly debatable. Uberaba. 20] or general ISSN 0172-4622 release of adenosine activating the neural path. Lib Information. influence of IPC on performance is still unclear c) “blood flow occlusion. The 20 studies included had cedure on performance and physiological varia. g. Brazil 2  German Sport University. The electronic databases of Most studies showed that IPC has no significant the National Library of Medicine (PubMed). Bibliography greater resistance of myocardial tissue to obviously attracted many researchers in sports DOI http://dx. Authors M. However. H.org/ 10. based on the assumption that a tis- accepted after revision ▼ sue with some “history” of ischemic conditions September 14. endurance [1. ● ▶ hyperemia Although numerous studies have demonstrated excluding systematic review articles. “athletes”. The majority of the bles is still debatable. mously the results of an earlier paper by his isamjf@gmail.1055/s-0035-1564253 ischemic events by reducing an infarct area by medicine and exercise science during the last Published online: 2015 ~75 % [43]. protection of dure was applied by South American indigenous Dr. Relevant studies were included.

Copyrighted material. ments of Müller. 46]. which were reduced to a num- results. in contrast to the majority of other maximal test of 7 × 200-m swimming after IPC. The term “clearly. and other they did not find increases in the working capacity of muscle online journals. Almost 20 years tioning”. ahead of print articles and a master thesis. However. in accordance with the other author. another author checked all selected performance during sprints [36] or during incremental exercise papers according to the quality criteria and arrived at the con- and anaerobic power output cycling tests [8. refers to the fact that information is However. [57]. b) ischemic preconditioning performed prior to exer- The de novo discovery of IPC as a potential tool for improving cise.” even without finding a significant difference in any of imum possible score was 14 points. and Nukada. studies about IPC. 309 were selected. for anaerobic After this initial screening. 1. De Groot and colleagues Quality assessment and data extraction [15] studied the effect of IPC in subjects performing an incre. ii) the intensity of the required workload. the longer the tourniquet had been applied. b) “blood flow” and “hyperemia”. where some features such as hydrostatic pressure and b) physiological variables associated with performance. tion and inclusion process is illustrated in ● ▶  Fig. after checking those papers for our defined inclusion cri- men and women was described [38]. raising the pos. These classical papers shed some light on the Relevant studies were included on the basis of conforming to potential ambiguity of IPC in the context of muscle work and strict criteria as determined by 2 investigators including: a) orig- performance. Out of these demonstrated on vertical jump power output [29]. the exercise environment in this case was The variables were divided into 2 categories: a) performance or water. many other researchers have performed experiments to evaluate the context of IPC and exercise. Shortly after the publica. In fact. [all fields]). The overall quality of each other studies in terms of the peak exercise capacity when tested publication was defined using the sum of the 14 criterion scores. Review blood flow to the lower extremities completely and subjected In fact. and no = 0 points). sion” were combined with “exercise performance”. to determine whether they met criteria for inclusion and further sibility that a hyperemia might be the most important among evaluation or had to be otherwise discarded. Ischemic Preconditioning and Performance …  Int J Sports Med . Studies selected were limited to ter and sustained contraction on a hand-grip dynamometer. After having observed a 4 % improvement in the total workload Initially. the duration of maximum performance. Black [18] and van Velzen. exercise literature located primarily through the PubMed data- tion of these results. Barcroft and colleagues [3] tried to replicate the experi. This buoyancy are very different from the non-aquatic environments. that out of 22 iden- Another study demonstrated that performance of elite swim. exercise capacity at high altitude [27] or work output under hypoxic conditions [21] also revealed hetero­ Data analysis geneous results. only used one bout of IPC. and In addition. e. We excluded sys- Libonati and colleagues [37]. isometric wrist flexion maximal voluntary contraction in both Finally. van Bennekom. but those written in the English language and included journal arti- their results completely failed to support the findings of Müller cles. c) evaluation of healthy subjects. of human performance and physiological parameters related to niquet. et al. The search This research group carried out 2 more studies with inconsistent revealed a total of 2 819 papers. Dot. it has been speculated that animals or non-healthy subjects. They associated IPC with a higher tematic review articles. Lib Information. The search. meta-analyses and studies with only force generation [37]. due to the relatively small number of studies involving the individuals to workloads of varying intensities immediately IPC and skeletal muscle performance. using rhythmic exercises on a bicycle ergome. experiments using IPC aimed at improving the time most of the studies evaluated more than one variable. selec- the potential mechanisms involved in IPC. the effectiveness of IPC has not been demonstrated in explicitly provided in the publication. classification aimed at a better description of the results. In addition. appears in several questions. tified candidate papers 2 should be excluded from the mers increased in 100-m crawl sprints [32] but not in a sub­ meta-analysis because they. Google Scholar (using [advanced search]. Selected studies were read thoroughly the forearm region after the occlusion protocol. The quality of all relevant studies was evaluated according to a mental cycling test and found an improvement in the peak checklist based on and adapted from the studies by Downs and power values and maximum oxygen consumption (VO2max). c) “blood flow occlu- later. “exercise” and “performance”. Crisafulli and colleagues ▶  Table 1) were scored on 3 levels ity. 22 papers remained to be analyzed.” which the analyzed physiological variables. d) conduction of exercise skeletal muscle performance in the late 90s can be attributed to or effort test and e) analysis of performance. the higher the improvement. and the max- doping. The following key terms a) “ischemic precondi- during hyperemia after a tourniquet of 5 min. While no significant effect of ischemia over 40s was ber of 913 after exclusion of duplicate publications. if their title matched our objectives. the higher the intensity. unclear = ½ point. increases in papers. “athletes”. We calculated the weight of the Marocolo M et al. They explained these sur. The meta-analysis was performed separately for physiological and performance variables. Unlike the other studies. it would be appropriate to upon ­reperfusion. improvement with shorter intervals. inal study. at sea level and in simulated high altitude [27]. of apnea [33].. the longer IPC in this systematic review. and iii) the duration of the interval between the Methods end of the ischemia and the beginning of the work. The items in the checklist ( ● [14] suggested that IPC might be considered a sort of “natural (yes = 1 point. clusion. Polomski. The last day of the literature there is an increased blood flow of approximately 3–4 times in search was 01 July 2015. teria. Database search prising results by a manifold increased blood flow during the This review identifies relevant ischemic preconditioning and reactive hyperemia upon reperfusion. i. only one investigator assessed the methodological qual- in a similar incremental cycling test. Collier and Percival [12] doubted these base with second-order internet search engines including stunning results and performed a similar experiment. The maximum time the subjects were able to evaluate the current status of the content from the perspective perform depended on various factors: i) the duration of the tour. more ▼ Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais).

2). The sample was used for the analysis. Dot.5 and 12. and heterogeneity was assessed by the Q level was 0. Ischemic Preconditioning and Performance …  Int J Sports Med . CA. The criterion for statistical significance was Results P < 0. prior to exercise”.05 for the Q test and I2 value of  ≤ 25 %. USA) Cochran test [9].0. The Shapiro-Wilk test was applied to verify the normal distribu. The most noteworthy results are as follows: (i) the mean score tion of the data. Copyrighted material. The effect size (ES) was calculated to deter.2). The analysis was performed with a the guidelines from Batterham and Hopkins [5]. confidence interval (95 % CI) and mean difference for ES was classified as trivial ( < 0. small ( > 0. type ● mine the meaningfulness of the difference [11] in performance of exercise.2–0. Lib Information. and physiological variables of the studies. (ii) only one publica- correlation between the percentage changes in the performance tion achieved the maximum score of 14 [32]. large ( > 1. 46] vided in each study). and (v) only 2 studies [33. The magnitude of the including statistical significance and ES.3. version 5. San Diego.2.6). The quality scores of the analyzed studies are shown in ●  ▶  Table 2. scores between 11. and GraphPad® (Prism 6.0) and very large ( > 2. 2014. Preconditioning occlusion and hyperemia AND Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais). The general purpose of the analysis was tested using the Z test [61].05 for 95 % CI. Review Fig. IPC protocol.  ▶  Table 3 presents the main information regarding subjects. which was completed with I2 [26].6–1.2–2.5. was homogeneous with a value of P ≥ 0. The Spearman test was used to examine the for the 20 selected publications was 12. Copenhagen: The Nordic Quality of the papers Cochrane Centre. These analyses were performed using the ▼ Review Manager Software. “Exercise “Performance” “Athletes” “Exercise” Performance” i (n = 197) i (n = 6) i (n = 238) i (n = 33) ii (n = 453) ii (n = 26) ii (n = 871) ii (n = 74) iii (n = 100) iii (n = 22) iii (n = 748) iii (n = 51) Search (n = 2819) Duplicates excluded (n = 1906) First Selection (n = 913) Excluded by Title (n = 604) Second Selection (n = 309) Excluded according to inclusion criteria (n = 289) Included (n = 20) a-original studies b-ischemic preconditioning use c-healthy subjects d-exercise or effort tests e-performance analysis studies. duration and time prior to exercise. 1  The procedure to select the publications (i) Ischemic (ii) Blood flow (iii) Blood flow for final analysis. The significance random effects model.05. (iii) 5 studies and physiological variables that showed statistical significance scored 13.0–4. “total time of IPC procedure” and “time scored 11. these values were then combined for ( > 0. It already becomes Marocolo M et al. moderate each study individually. The Cochrane Collaboration. (iv) most of the sample (n = 12 publications) obtained with “duration of exercise” (extracted from the information pro.0) based on the analysis of the studies.

[27] 1 1 1 1 1 1 1 0. Gibson [23] and Paterson [48] procedure and the onset of exercise.5 (89 %) 2015 Tocco et al. [15] 1 0. Were the statistical analyses used appropriate? Yes Unclear No 12.5 (82 %) 2015 Marocolo et al.5 0 1 11. For physiological Marocolo M et al. Does the study provide estimates of the random variability in the data for the main outcomes? Yes Unclear No Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais). Was the presentation of results satisfactory? Yes Unclear No 13.0 (93 %) 2011 Jean-St-Michel et al. Are the characteristics of the subjects included in the study clearly described? Yes Unclear No 4.5 (82 %) 2012 Clevidence et al.001? 10.5 20 4 21 12. 4 shows homogeneous results from 2 swimming studies ● duration. Was a follow-up duration sufficiently described and consistent within the study? Yes Unclear No ANALYSIS AND PRESENTATION 1 ½ 0   9. Lib Information. [23] 1 1 1 1 1 1 1 1 0 1 1 0.5 21 15 12 21 20. g. [2] 1 1 1 1 1 1 1 0. I2 = 0 %). their  ▶  Fig.0 (93 %) 2011 Crisafulli et al. REPORTING 1 ½ 0 1.5 (82 %) 2013 Cochrane et al.5 1 1 1 1 0 1 12. 3a). Dot.5 1 1 1 1 0 1 11. [47] 1 1 1 1 1 1 1 0. Was there a statement adequately describing or referencing all statistical procedures used? Yes Unclear No 11.5 1 1 1 1 0 1 12.” whether the IPC procedure resulted in a favorable effect (Panel A The majority of the variables from the selected studies showed p = 0. 2– 4) were divided into different catego.0 (79 %) 2014 Paixão et al.5 19. Cochrane [10]. the results were heterogeneous (p = 0. 7.5 1 1 1 0.0 (100 %) 2012 Bailey et al.2 (87 %) apparent at first glance that a consensus obviously does not exist exercise may be quite different from water-based exercise. 2).5 (82 %) 2014 Kjeld et al.5 (89 %) 2014 Gibson et al. [45] 1 1 1 1 1 1 1 0.5 1 1 1 1 1 1 13.5 21 21 21 19.0 (93 %) 2013 Gibson et al. and the reperfusion periods vary considerably among (p = 0.5 1 1 1 11.. I2 = 47 %).09. Bailey [1]. bles.0 (86 %) 2011 Foster et al.5 1 1 1 1 0 1 12. Have actual probability values been reported (e.5 0.5 1 1 1 1 1 1 0. 32] 1 1 1 1 1 1 1 1 1 1 1 1 1 1 14.5 0 1 1 1 0 1 11. the number of IPC sets.5 1 1 1 1 0 1 12.5 0 1 1 1 0 1 11.99. more or less homogeneous results were centage changes in the performance and physiological variables identified (p = 1. Are the interventions of interest clearly described? Yes Unclear No 5. Were confidence intervals given for the main results? Yes Unclear No 14. 3c). For oxygen No significant correlation (P > 0. [22] 1 1 1 1 1 1 1 0. the studies of Barr [4].5 1 1 0 1 0.0 (86 %) All studies 20.0 (93 %) 2015 Hittinger et al.5 0 1 1 1 0 1 11.” “total time of IPC procedure” and of short duration ( ● ▶  Fig.0 (79 %) 2014 Paterson et al. Is the hypothesis/aim/objective of the study clearly described? Yes Unclear No 2. Are the main outcomes to be measured clearly described in the introduction? Yes Unclear No 3. [1] 1 0.5 1 1 1 1 1 0.5 (82 %) 2014 Barbosa et al.5 1 1 1 1 0 1 12. the studies influenced the meta-analysis results for various varia- forest plot data ( ● ▶  Fig. Are the main findings of the study clearly described? Yes Unclear No 6. [10] 1 1 1 1 1 1 1 1 1 1 1 1 0 1 13. ( ● ▶  Table 4). indicating that these For easier comprehension and more coherent presentation.05) was found between the per- consumption ( ● ▶  Fig. Date-Author Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Q9 Q10 Q11 Q12 Q13 Q14 Score ( % of max) 2010 De Groot et al. only in 2 studies were also encountered (p = 0. 0. [6] 1 0. Were the instruments of testing reliable? Yes Unclear No 8. [8] 1 1 1 1 1 1 1 0. as well as the period between cessation of the IPC [12].5 1 1 1 1 1 0. Moreover. [55] 1 1 1 1 1 1 1 1 0 1 1 1 0 1 12.05) for the main outcomes Yes Unclear No except where the probability value is less than 0.97. ries allowing the analysis of comparable parameters. it was not possible to identify “time prior to exercise. Was the conclusion drawn from the statistical analysis justified? Yes Unclear No Table 2  Scores assigned to each of the studies (in chronological order) for each of the quality (Q) criteria. Since land-based a placebo or sham intervention was carried out. [40] 1 1 1 1 1 1 1 0. I2 = 0 %).05) improvements.5 (89 %) 2015 Lalonde and Curnier [36] 1 1 1 1 1 0 1 0. with regard to the IPC procedure. I2 = 56 %). In contrast. [33] 0.5 (89 %) 2014 Foster et al.5 1 1 1 1 1 13. showed a higher weight in the forest plot. heterogeneous results presented significant (P < 0.5 0 1 1 0. Review Table 1  Quality criteria used to analyze the publications.0 (86 %) 2011 Barr [4] 1 1 1 1 1 1 1 1 1 1 1 1 0 1 13.0 (93 %) 2012 Beaven et al. 3b). 21] 1 1 1 1 1 1 1 1 1 1 1 1 0 1 13. With regard to time of performance with “duration of exercise. Crisafulli the studies. Copyrighted material.5 0 1 11. I2 = 0 %).035 rather than  < 0. for longer duration performance non-significant differences for performance or physiological ▶  Fig. Ischemic Preconditioning and Performance …  Int J Sports Med . [20] 1 1 1 1 1 1 1 0. 14] 1 1 1 1 1 1 1 1 0 1 1 1 0 1 12.00.02. Among the 10 performance variables that variables ( ● Concerning power outcomes ( ● ▶  Fig.

28 [2] 2014 Foster 5 days- Healthy running 12 P/IPC 20 ~200–40/thigh prior 12.05 0.03 2011 Barr [4] Cycling active 24 3 × 5 min C/IPC 15 220/thigh 20 min Wingate Mean Power 0.01 Cycling amateur cyclists 8 4 × 5 min C/IPC 20 20 > SAP/one thigh 90 min Time Trial [21] 100 KJ Hypoxia  − 2.06 [23] athletes 30 m sprint 0.02 [22] tion Total Power  − 1.6 NS 0.1 NS Ω Jump/Sprints healthy 14 2 × 3 min C/IPC 6 220–15/thigh 0–24 h [6] CMJ Height 0.60 2014 Kjeld [33] Rowing/Apnea rowers/divers 11–6–14 4 × 5 min C/IPC 20 40 > SAP/forearm 30 min Static apnea Time 17.05 0.93 2014 Paixão 3 Wingate/10 min Cycling cyclists 15 4 × 5 min P/IPC 20 250–20/thigh 12 min Mean Pw.25 Peak Power  − 0. .09 SJ (w)  − 5.04 Fat.48 0.7  < 0.1 0.35 Review Marocolo M et al.05 0.8 Km Time Trial 7.2 NS 0. Date-Author Exercise Pro.2  < 0.1  < 0. Ischemic Preconditioning and Performance …  Int J Sports Med Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais).01 1.06 2011 Crisafulli VO2max 3.3 NS 0.86 Distance time T.6 NS 0.2  < 0. HR *   − 5.0 NS 0.42 ­Clevidence [8] tal + 90 %max Ex.00 healthy and ECC Exercise CK 0. Index  − 1.8  < 0.32 [20] 4 × 5 min Lactate  − 11.4  < 0.13 2013 Gibson team sport Sprint 25 3 × 5 min C/P/IPC 15 220–50/thigh 15 min 20 m sprint Time  − 0. 1 000 m 0.9  < 0.05 0.2 NS 0. 0. 2  − 2. 10.5 NS 0.7 0.67 0. Fat.03 0. 1  − 2.1 NS 0. Copyrighted material.05 0.00 2014 Barbosa Handgrip healthy 9/13 3 × 5 min C/IPC 15 200–10/thigh 25 min Rhythmic Handgrip T.05 0.13 Time Trial 2.0 NS 0.6 0.0 NS Ω 2013 Cochrane Strenuous Ec.3 NS 0.0 NS 0.35 [45] break Mean Pw. 1  − 2.22 2011 Foster 100 KJ Normoxia 0.0 0.26 2012 Bailey [1] Running healthy 13 4 × 5 min P/IPC 20 220–20/thigh 45 min Incremental 5 Km Heart Rate 0.2  < 0.1 0. Table 3  Characteristics of the studies examining the effect of IPC on performance.22 Max Pw.54 2012 Incremen- Cycling cyclists 20 3 × 5 min C/IPC 15 220–0/thigh 5 min Peak HR *  *   − 4.32 Cycling healthy 17 3 × 5 min C/IPC 15 50 > SAP/thigh 5 min Maximal Incremental [14] Workload 3. 30 min-30 s 10 > pulse pressure/ involved in 10 C/IPC 15 24–48–72 h [10] centric Exercise alternating leg (3 × 100 rep) VJPP 0.6  < 0.7 NS Ω CMJ SJ Height 9 NS Ω Avg.40 0.05 0.9 NS Ω physical activity 10 m sprint 1.10 Cycling healthy 15 3 × 5 min C/IPC 15 220/thigh 5 min Maximal Incremental [15] VO2max 2.4 NS 0.2 NS Ω Squat jump 2012 Beaven CMJ (w)  − 0.05 0.50 2014 Gibson trained popula- Sprint 16 3 × 5 min C/P/IPC 15 220–50/thigh 5 min Sprint 5 × 6 s Peak Power  − 0.003 0.06 Dynamic apnea Time 8. Lib Information.00 Exhaust. Dot.11 Michel [32] VO2max 1.4  < 0.8 NS 0.0 NS 0. Time 1.6 0. Subjects N IPC Sets Group Total IPC Ischemia Pressure Time to Test Protocol Variable Change P ES tocol time (min) (mmHg)/Limb Test Analyzed ( %) 2010 De Groot Max Power 1.07 2011 Jean-St- Swimming elite swimmers 18 4 × 5 min P/IPC 20 15 > SAP-10/arm ~45 min 100 m Time Trial Time Trial 1.Toler.01 1.03 0.8 0.05 0.

Copyrighted material. = Exercise tolerance. Dot. C = Control. = time to fatigue. However. but only one study tested the sub- time before tests ( ● 14 28 17 15 11 N jects in a “second window” [10].6  − 3. IPC procedure was not found in our analysis. The IPC 2015 Tocco effects were primarily tested in individual modalities and incre- mental cycling was the most common test. 15].0 2. Capacity Ex. 60]. followed by running [47] [27] [36] [40] [55] (~43 % and ~14 % of the studies. g.11 0. mVO2(l.12  * Average Heart Rate (bpm) 30 %VO2max.9 1.3  − 0.min − 1) Variable of them did not use a sham procedure to control the experi- mVO2 ments for a potential placebo effect and this could have gene­ rated biased results. Exhaust. A consensus 220–20/thigh 220–5/arm apparently does not exist with regards to the time of IPC dura- tion and this also holds true for the time between the last IPC thigh arm procedure and testing.7 The main finding in this review was that the studies appeared to ( %) be of high quality and that most of them failed to describe statis- Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais).  *  * Peak Heart Rate (bpm) 30 % VO2max. T. VJPP = vertical jump peak power. Moreover. Analyzing the studies dex = fatigue index. α the study did not provide P-value were discarded from our analysis. an effective and “positive” use of Incremental high alt. active in sprint skilled runners When analyzing the statistical significance. the duration of the Continued.s )  − 1 VO2 (l. most Time Trial Analyzed (l. IPC procedures were applied repetitively. no improvements were found. Capacity = exercise capacity. Also. performance varied considerably (i.05 NS NS NS NS NS NS NS NS NS P α α Discussion ▼ Change 2. once the early and late effects of IPC on the cardiovas- IPC Sets of the studies examining the effect of IPC on performance. mean Pw1 = mean power wingate 1. Mean Pw. which also should apply to exercise intensities. Progressive 6 × 6 s Incremental/sea 100 m time trial 12 × 6 s sprints Test Protocol Inconsistency among IPC protocols The overall picture emerged that there is obviously no consen- Wingate sus among researchers on IPC with regard to exercise type and 5 Km level duration. e. cular system were demonstrated in clinical experimental set- tings [24. 20 20 20 20 15 The only methodological consistency among the studies is related to the fact that limbs underwent IPC bilaterally. it would be interesting to identify the ideal window of time after which IPC could result in exercise benefits. with 50 > SAP-10 < DAP/ 10–20 > SAP/thigh 50 > SAP-10/right (mmHg)/Limb various occlusions of 30 s each [10] up to 5 min [56]. The present analysis identified considerably different periods of ▶  Table 3). Ω Ω Ω Ω ES 8 used a placebo/sham.29 0. 46]. Ex. cycling ( ● ▶  Table 3).4  − 0. Review variables. tical significance in the measured performance or physiological Speed (m. = maximal power in wingate.. number and durations of tourniquet procedures.15 0. Among the few that demonstrated significance. Pw. Therefore. we noted that from 10 studies. Time to 45 min 15 min Total occlusion periods range from 6 min [6] up to 20 min [36] Test 30 with the complete IPC protocol (including occlusion and reper- – 5 fusion) up to 40 min.1 0. Other exercise Marocolo M et al. IPC = ischemic preconditioning. duration from ~10 s up to 2015 Marocolo 2015 Hittinger 2014 Paterson 2015 Lalonde Date-Author 5 400 s). Exer.. which is speculated to open ~24 h after ischemic preconditioning. Fat. 2 = mean power wingate 2. While some authors described increases in power and in workload in cycling test conducted after 5-min interval [14. and 2 studies applying just one bout of ischemia study did not provide enough data to calculate effect size (ES).15 0.8 1. T. at the C/P/IPC C/P/IPC Group C/IPC P/IPC P/IPC same time or alternating. most of the studies high trained recreational recreational cyclists and ­triathletes Subjects demonstrated non-significant differences ( ● ▶  Table 4). P = Placebo. 3 × 5 min 4 × 5 min 4 × 5 min 4 × 5 min 3 × 5 min Moreover. Max. and the period between cessation of IPC and the start of the exercise ( ● ▶  Table 3).8 1.3 1. Ischemic Preconditioning and Performance …  Int J Sports Med .min − 1) = mean VO2. 1 000 m = time to 1 000 m. e. Ω the 0. Capacity Peak Power Peak Power Peak Power variables. swim- Table 3  Characteristics ming.Fat.13 0.5 3.29 0.18 0.3 2. Toler. Exercise Pro- Exercise type and subjects involved Swimming Running The exercises and performance tests included in this review pre- Cycling Cycling Cycling tocol sented a wide range of types of exercise.min − 1) Time to 5 km Mean Power Mean Power Ex.  < 0. Time = time to exhaustion. Lib Information. the period of occlusion (followed by Ischemia Pressure reperfusion) is being administered quite heterogeneously. It leads to athletes healthy sports suspect that the ideal IPC protocol could not yet be found or some parts of the experimental protocols need more detailed control. running. In- with non-significant differences. others scheduled testing for cycling perfor- time (min) Total IPC mance or sprinting 12 or even 15 min after the procedure [23. respectively).

b longer duration performance and.97 11 17.1 % – 0.9 13 22.3 3.1 27.00 [– 35. – 0.4 374.3 13 25.0 % – 8000 [– 1042. 0. Marocolo M et al.78.27.5 13 19.63 0.7 5. Fixed. The square is the weight for a given study and is proportional to the weight of the study in the meta-analysis.60 [– 2. I2 = 56 % – 100 – 60 0 50 100 Test for overall effect: Z = 3. 95 % CI Tocco [46] – Speed 4.2 15 56. 4.1 0. I = 0 % Test for overall effect: Z = 0. 4.8 12 0. The diamond at the bottom represents the overall effect calculated using a fixed-effects model.7 % 1.4 17 40.33.46] De Groot [27] – VO2max 58.77 (P = 0.4% – 0.53] Barr [41] – Fatigue Index 49.00 [– 32.0% – 0.15 [– 0.53 8.5 17 31.25 25 15.02] Heterogeneity: Chi2 = 9.4 % 0. Fixed.02] Paterson [45] – VO2max 34.8 0.0002) Favors [IPC] Favors [control/placebo] Fig.7 % 1.46] Barr [41] – Mean Power 766.2 11 0.0 % – 0.10. df = 9 (P = 0. 95 % CI IV. – 4.3 11 53.20 [– 1.16 25 1.40 [– 1. 184.58 2.06 25 99.17.7 % – 0.60 [– 3.2 25 5.53.90] Paixão [31] – Mean Power 2 712 16 15 733 15 15 15. Lib Information.12] Foster [17] – Time Trial (12.58 [– 145.5 24 0.80 [– 1.13.8 15 13. 2.61.1 16 1 583.1 % 0.12 0.46. c power outcomes. The diamond at the bottom represents the overall effect calculated using a fixed-effects model. Toler 1 121 69.0 % – 0.97). 1.44) Favors [IPC] Favors [control] c Experimental – IPC Control or Placebo Mean Difference Mean Difference Study or Subgroup Mean SD Total Mean SD Total Weight IV.6 2.13 [– 0.2 368.07] Gbson [18] – 30 m sprint 4.0 % – 20.26] Tocco [46] – VO2max (control) 55.9 24 59. 95 % CI IV.02 [– 0.15.60.11.25 11 4.22.29 25 4.11.80) – 100 – 60 0 50 100 Favors [IPC] Favors [control/placebo] b IPC Control or Placebo Mean Difference Mean Difference Study or Subgroup Mean SD Total Mean SD Total Weight IV.66. 95 % CI Gibson [44] – Total Power 6 668.51 0.01 [– 0.11 0.5 13.1 % 3600 [– 112. 882.8 10.10.5 4. Total (95 % CI) 81 81 100.80 [– 15.3 % – 21.19 0.01] Bailey [16] – Time Trial 22. 4.1 20 1 121 64. 2. The horizontal line indicates the 95 % confidence interval (CI) for an effect.00 [– 32. The square is the weight for a given study and is proportional to the weight of the study in the meta-analysis. 95 % CI IV.6 11 1.6 0.10. 2  Forest plot of physiological variables (maximal oxygen consumption): Studies are listed according to the effect size. a Experimental Control or Placebo Mean Difference Mean Difference Study or Subgroup Mean SD Total Mean SD Total Weight IV.4 6.82 0.8 2. 0.02).9 % 1.1 11 1.7 18.0% – 9.1% 0.65 1.7 % – 1.6 1 364 16 6 748.45 0.08 10.8 33.90] Paixão [31] – Max Power 1 870 21 15 890 22 15 8. 0.1 % 0. – 9.24. Studies are listed according to the effect size.21] Gbson [18] – 20 m sprint 1. 95 % CI Tocco [46] – VO2max (placebo) 55.39.97] Heterogeneity: Chi2 = 20. 0.6 3.82 121.31 [– 12.2 14 33.15 25 33.02 1.10] Gibson [44] – Peak Power 1 577. 1.09).1 4.1 % – 7.28.62 24 0. 11. 6.53] Paixão [31] – Mean Power 1 725 15 15 746 16 15 15. 72.31 11 6.37.61] Barr [41] – Peak Power 1 104 238 24 1 111.00 [– 0.51 0.9 5.80 [– 263.2 0.19) Favors [IPC] Favors [control/placebo] Fig.05.0 % 0. I = 0 % – 100 – 50 0 50 100 Test for overall effect: Z = 1.24.30 [– 2.50.07. Fixed.15] Gbson [18] – 10 m sprint 3.02] Kjeld [20] – Static apnea (time) 4.0 % – 5. Fixed.57.70 [– 34.40] Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais). The horzintal line indicates the 95 % confidence interval (CI) for an effect. Review IPC Control or Placebo Mean Difference Mean Difference Study or Subgroup Mean SD Total Mean SD Total Weight IV.01 [– 0.43 13 0.8 % – 0.50] Bailey [16] – VO2max 52.56 248. 0.3 11 57.04] Total (95 % CI) 99 99 100.4 12 137.11] Total (95 % CI) 86 86 100. Fixed.00 [– 41. Ischemic Preconditioning and Performance …  Int J Sports Med . Dot. 95 % CI IV. 130.88 24 50.10.27] Tocco [46] – Time to 5 km 18.6 1 413.01 [– 0.0% 0.9 14 25.88] 2 2 Heterogeneity. df = 5 (P = 0.99 1. 14. – 9.07] Clevidence [32] – Ex.06 25 3. Fixed.00). df = 5 (P = 1.06.8 6. Chi = 0.28] Total (95 % CI) 183 183 100.31 (P = 0. 251.25.90 [– 10. Copyrighted material.0 % 1.21 25 3. I2 = 47 % – 100 – 60 0 50 100 Test for overall effect: Z = 0.4 % 4.09.6 20 1.79 [– 63.75 (P = 0. 14.32.69] Paterson [45] – Peak Power 1 630 192 14 1 594 208 14 0. 3  Forest plot of performance variables: a. Fixed.04. 41.56 [– 2.65.05] 2 2 Heterogeneity: Chi = 0.15 25 45.26 (P = 0. time of performance of short duration. 5.6 13 51.56 [– 6.3 % – 21.8 Km) 128.92] Kjeld [20] – Distance time 3.01 [– 0.70] Crisafulli [28] – VOmax 41.65 25 0. 0.4% – 0. 95 % CI Bailey [16] – Exhaust Time 19.82.0 % – 8.03 [– 0.2 13 0.7 18.6 16 0.09 24 76203 118.6 % 1. Fixed.6 16 0. – 3. 0. df = 3 (P = 0.

I = 0 % – 100 – 50 0 50 100 Test for overall effect: Z = 0. which depends on how well the statis- Decrement 03 (7. a description of physiological responses are in some respects different from non.90 [– 2. Review IPC Control or Placebo Mean Difference Mean Difference Study or Subgroup Mean SD Total Mean SD Total Weight IV. the subjects involved in the IPC and performance studies were which referred to reports of the actual probability values.02 5. 4  Forest plot of specific swimming performance parameters.18] 2 2 Heterogeneity: Chi = 0.02 5.6) 02 (25) 05 (10. Therefore.11 15 70. The horizontal line indicates the 95 % confidence interval (CI) for an effect. larly the few studies showing significant improvements (P < 0.13 18 27.11 15 71. unless P < 0. 3. Lib Information. which is rather a performance of ambitious from a rabbit having undergone simultaneous IPC of both. [32] found an improvement of 1. healthy individuals or amateur practitioners of physical activity.9 % – 0. Dot. many of the assessed studies had some limitations. jumps. The diamond at the bottom represents the overall effect calculatedusing a fixed-effects model. 12 studies did not report any follow-up analysis tors). that could reach another tissue and provides protective effects.29 5.40) Favors [IPC] Favors [control/placebo] Downloaded by: IP-Proxy CONSORTIUM:CAPES (UFMG Universidade Federal de Minas Gerais). double-blind study). athletes individuals. all of these studies failed to reference at least ever.0 % – 0. the 100-m trial time of the athletes evaluated in this study This idea was based on experiments. When this blood was transfused into another rabbit. Copyrighted material.99).61] Total (95 % CI) 48 48 100. The CI is based on the fact that Improvement 10 (25. analyzing handgrip fatigue during exer- are in line with the idea of a possible placebo effect.92 [– 4. it becomes obviously difficult to generally transfer a possi.6) tics represent the target population. e. Jean-St. this fact is comprehensible design was transversal. sprinting. However. This trivial ES could be important for idea has been derived from experimental clinical studies. Despite the high mean score observed for quality (87 %). paper [40].06 4. some researchers spec- might be disputed in general whether the outcome of IPC with ulated about a variety of endogenous substances generated by swimming test is comparable to other performance tests (i. all experimental ples but not top athletes. Table 4  Summary of number and percentage of variables from analyzed Quality of the papers studies that showed statistical description (P-value). Ischemic Preconditioning and Performance …  Int J Sports Med . such as the ble positive effect of IPC to elite athlete populations. 2.3) there is a sampling error. Among the studies included quite heterogeneous.45. However. some studies suggested a humoral hypothesis postulat- highlight the IPC procedure as potentially interesting tool to ing that an ischemic event leads to the production of substances improve. where blood was collected [32] was about 60 s. 95 % CI IV.6 % – 0. This is par- Statistical Performance-n Physiological-n Total-n ticularly important because the CI is influenced by the sample significance ( %) ( %) ( %) size. of the participants in the studies. Fig.34 15 37.1) level selected by the researcher.. On the other hand. endocannabinoids [25] and different. Fixed.67 [– 4. such as bradykinin [52].27] Marocolo [40] – Time to 100-m swimming (control) 70. 8. rowing.84 (P = 0. Specifically.76 15 34. one of the relevant issues for experimental studies. Fixed.92 18 59.43. opioids [47]. In this practical applications. elite athletes present a minor window of IPC in experimental clinical and sports science settings adaptation. It means that the dose to generate a response in The term “ischemic preconditioning” (IPC) was first used in the highly-trained subjects would need to be much higher than for scientific literature in 1986 [43].02.61. as their study design (randomized.96 6. How. In addition. They are suggested as candidates to affect the Marocolo M et al. ever.05.35] Marocolo [40] – Time to 100-m swimming (SHAM) 70. How. mainly with clinical background but also in the con- swimming performance (100-m trial time) used self-designated text with performance evaluations. diving and swimming. and these findings than the exercised one. the homogeneity of the data sample and the confidence Non-significant 26 (66. While the responsiveness of untrained indi- viduals is large. The term “remote ischemic untrained ones [13].05) Finally. when found in elite athletes. Considering particu. Indeed. RIPC is related to an intervention that does not directly affect the Michel et al. In this way. df = 2 (P = 0. swimming performance. Only 4 studies Variables included the CI for the main results (criterion 13). 1. On one hand. 27. 32]. the definition of elite [32] or recreational [40] swimmers. the only 2 studies that verified the effect of IPC on procedure. allows each reader to reject it. since the breathing pattern in swimming is related peptide [55]. The majority of Other studies lacked information about quality criterion 9. in the second swimming and kidney. the study dropouts or relocation of the subjects. Reporting the exact P-value provides more information about It appears that only 3 papers analyzed competitive elite athletes the strength of the evidence against the null hypothesis and or highly trained individuals [23. for whatever reasons. This with a trivial ES (0. adenosine [49]. subjects from a sham group also in this review. vertical the estimate of the average of the population. although showing significant improvements across whose heart subsequently was made ischemic. the individual responses of the subjects were infarct size was reduced by 77 % [16].97.5 % – 1.7) 00 (0) 10 (21. It would respect. 95 % CI Jean-St-Michel [32] – Time to 100-m swimming 59. 2. On one hand.1 % in performance same part of system of the body where it is applied [50]. there were deficiencies with regard to quality criterion on exercise performance (or associated physiological indica. Moreover.94 4. gene- running or cycling). tion. a report of the CI values provides a range. which may explain this lack of informa- due the difficulty of finding athletes available for research. which likely includes types included various models of resistance exercise. remote tissues after ischemia.04 [– 4. only one applied the occlusion in a different limb demonstrated decreases in swimming time. The square is the weight for a given studyand is proportional to the weight of the study in the meta-analysis.11). the majority of them used healthy subjects in their sam.7) 06 (75) 32 (68. preconditioning” (RIPC) is also described in studies using this Interestingly. heart amateur swimmers. it cise after thigh occlusion [2]. not a single point. the myocardial the IPC group.

Effect verum and the placebo procedures in most of the studies did not of ischemic preconditioning on lactate accumulation and running per- formance. Ohio University 2011. 6 Beaven CM. as in most sports the lower extremities CAPES. since the 1 Bailey TG. Mowery RE. with about one sixth of the total muscle mass are required for performance. 112: able effects on performance. Giri PC. Hillsdale. such a cular power: Part 2-training considerations for improving maximal study might be useful to potentially explain possible placebo or power production. Thijssen DH. Barnes MJ. J Thromb Thrombolysis 1999. Fisman EZ. Zhang MM. Renzi FP. J Epidemiol Commun of uniformity in the studies on this topic and variations in the Health 1998. NJ: Lawrence Erlbaum. but rather demonstrate any physio­ 3649–3654 9 Cochran WG. it should be reasonable to suppose magnitudes. Heard score and provide support for the present findings. Reinhardt CP. Caria MA. Ischemic preconditioning: nearly two decades potential placebo effects (e.12229 3 Barcroft H. J Am Coll Cardiol 2006. Mundel T. Cox PN. Marocolo M et al. Ellenkamp R. Porcaro WA. Silva BM. 19 Eisen A. but none of these studies Acknowledgments described this concept with regard to performance in skeletal ▼ muscle. 111: 530–536 Conclusion 15 de Groot PC. Adler Y. McKechnie R. 18 Downs S. Black N. Since none of the studies had already emia. Newton RU. Making meaningful inferences about metabolic pathways [35. 68 5 Batterham AM. Rand- sion) generated a positive hyperemic effect. In fact. Sanchez M. ▼ Ischemic preconditioning improves maximal performance in humans. 15: 155–161 when it comes to improved performance in sports. Kushnick MR. emerged that IPC does not relevantly influence exer. 2: 114–118 13 Cormie P. 172: 201–210 procedure). Redington AN. had been informed they could expect improvements from IPC doi:10. The lack of influence of reactive hyper- and placebo/sham (when applied) interventions. Eur J Appl Physiol Based on previous assumptions that IPC could improve anaero. Anholm JD. and ed. Gill N. 37: 1132–1139 tion has been described [37]. 2nd ration. 1: 50–57 that a muscle occluded previously could potentiate its perfor. Sports Med 2011. J. Remote ischemic preconditioning delays fatigue devel- ment mechanism. 1978. as most of the studies lacked significant differ- myocytic apoptosis in rabbit heart in vivo. Med Sci Sports Exerc 2012. rate of force development. 108: 141–146 The papers included in this review have a reasonable quality 16 Dickson EW.1111/sms. Biometrics 1954. Ischemic preconditioning of the muscle improves maximal exer- cise performance but not maximal oxygen uptake in humans. Conflict of interest: The authors have no conflict of interest to declare. Mulliri G. Vianna LC. 14 Crisafulli A. The working capacity of muscle during reactive hyper- most effective procedures. Fernandes IA. submaximal cycling performance. etc. Ergonomics 1959. Intermittent lower-limb mance. Rubenfire M. 44: 2084–2089 elicit different effects. and it was speculated that an 7 Cheung MM. as some studies reported that the subjects opment during handgrip exercise. this procedure can be considered a myth rather than a fact nary vasoconstriction at high altitude. Tenenbaum None of the analyzed studies seriously considered evaluating A. Rogers DM. Copyrighted material. 34: 969–974 blood analyses. ments. This so far has been omized controlled trial of the effects of remote ischemic precondition- suggested as the underlying mechanism of IPC [37]. emia on exhausting rhythmic or static exercise. preconditioning on aerobic and anaerobic variables associated with Future research on IPC should not concentrate only on question. 51]. Freimark D. Concu A. 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