International Journal ofEnvironmental Researchand Public Health

ArticleIschemic Preconditioning with High and Low Pressure
Enhances Maximum Strength and Modulates Heart
Rate Variability
Luiz Guilherme Telles 1,2 , François Billaut 3 , Aline de Souza Ribeiro 4 , Christian Geórgea Junqueira 5 ,Luís Leitão 6,7, * , Ana Cristina Barreto 8 , Patricia Panza 4 , Jeferson Macedo Vianna 4
and Jefferson da Silva Novaes 1
1

2
3
4

5
6

7
8

*

Physical Education and Sports Department, Federal University of Rio de Janeiro,
Rio de Janeiro 21941-901, Brazil; guilhermetellesfoa@hotmail.com (L.G.T.); jeffsnovaes@gmail.com (J.d.S.N.)
Estácio de Sá University (UNESA), Rio de Janeiro 20261-063, Brazil
Department of Kinesiology, Laval University, Quebec, QC G1V 0A6, Canada; francois.billaut@kin.ulaval.ca
Physical Education and Sports Department, Federal University of Juiz de Fora, São Pedro 36036-900, Brazil;alinevalencaedfisica@gmail.com (A.d.S.R.); paty_panza@yahoo.com.br (P.P.); jeferson.vianna@ufjf.edu.br (J.M.V.)
Volta Redonda University Center, Rio de Janeiro 27240-560, Brazil; christian.junqueira@hotmail.com
Sciences and Technology Department, Superior School of Education of Polytechnic Institute of Setubal,
2910-761 Setúbal, Portugal
Life Quality Research Centre, 2040-413 Rio Maior, Portugal
Celso Lisboa University Center, Rio de Janeiro 20950-092, Brazil; educacaofisica@celsolisboa.edu.br
Correspondence: luis.leitao@ese.ips.pt

Citation: Telles, L.G.; Billaut, F.;
de Souza Ribeiro, A.; Junqueira, C.G.;Leitão, L.; Barreto, A.C.; Panza, P.;
Vianna, J.M.; da Silva Novaes, J.
Ischemic Preconditioning with Highand Low Pressure Enhances
Maximum Strength and ModulatesHeart Rate Variability. Int. J. Environ.
Res. Public Health 2022, 19, 7655.
https://doi.org/10.3390/
ijerph19137655
Academic Editors: Valerio
Bonavolontà, Francesca Latino andPaul B. Tchounwou
Received: 28 April 2022
Accepted: 20 June 2022
Published: 23 June 2022
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in

Abstract: Background: The application of ischemic preconditioning (IPC) to resistance exercise has
attracted some attention, owing to increases in muscle performance. However, there is still noconsensus on the optimal occlusion pressure for this procedure. This study compared the acute effectsof IPC with high and low pressure of occlusion on upper and lower limb maximal strength and heart
rate variability in recreationally trained individuals. Methods: Sixteen recreationally trained men(25.3 ± 1.7 years; 78.4 ± 6.2 kg; 176.9 ± 5.4 cm; 25.1 ± 1.5 m2 kg−1 ) were thoroughly familiarizedwith one repetition maximum (1 RM) testing in the following exercises: bench press (BP), front
latissimus pull-down (FLPD), and shoulder press (SP) for upper limbs, and leg press 45º (LP45),
hack machine (HM), and Smith Squat (SS) for lower limbs. The 1 RM exercises were then randomly
performed on three separate days: after a high pressure (220 mmHg, IPChigh ) and a low pressure(20 mmHg, IPClow ) IPC protocol and after no intervention (control, CON). Heart rate variability
was also measured at rest, during and after the entire IPC protocol, and after the exercises. Results:
Maximal strength was significantly (p < 0.05) higher in both IPChigh and IPClow compared with
CON in all upper- and lower-limb exercises. There was no difference between the two experimental
conditions. No significant differences were found in the comparison across the different experimental
conditions for LFnu , HFnu , LF/HF ratio, and RMSSDms . Conclusions: IPC performed with both
high and low pressures influenced heart rate variability, which may partly explain the maximal
strength enhancement.

published maps and institutional affiliations.

Keywords: ischemic preconditioning; maximum strength; resistance exercises; heart rate variability

Copyright: © 2022 by the authors.

1. Introduction

Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms andconditions of the Creative Commons
Attribution (CC BY) license (https://creativecommons.org/licenses/by/

The efficacy of ischemic preconditioning (IPC) has been investigated substantiallyin the health context in the last 34 years, and it has been robustly demonstrated that thismaneuver induces protection of the heart such as a reduction in myocardial infarction
area [1] and of the skeletal muscle such as a reduction in ischemic necrosis and lowering ofenergy metabolism during sustained ischemia [1]. In the context of physical exercise and4.0/).

Int. J. Environ. Res. Public Health 2022, 19, 7655. https://doi.org/10.3390/ijerph19137655

https://www.mdpi.com/journal/ijerph

Int. J. Environ. Res. Public Health 2022, 19, 7655

2 of 13

performance, studies have mainly investigated the impact of IPC on endurance and poweroriented activities [2,3]. More recently, the application of IPC to resistance exercise has
attracted some attention, demonstrating very interesting and relevant benefits on muscle
performance and adaptations [4–6].
The improvement in muscle performance after application of IPC has been
demonstrated for isometric [7,8], dynamic [9,10], and isokinetic strength [11]. Recently,
Carvalho et al. [12] showed that IPC can further enhance the chronic increase in maximum
strength after 6 weeks of intervention combined with resistance exercise. However, surprisingly, the acute effect of IPC on maximum strength has not yet been verified. According
to the American College of Sports Medicine [13], maximum strength is defined as the highest
resistance of a muscle or muscle group that can be moved along the range of motion of thejoint, in a controlled manner and with the correct posture. Kilduff et al. [14] has suggested
that there is an additional window on the day of competition during which performancecan be enhanced with various acute strategies. Among them, IPC has been proposed tobe such an efficient strategy. In fact, Winwood et al. [15] recommended the use of IPC for
Strongman athletes on the day of the competition to improve maximum strength and muscle power. Recently, Telles et al. [16] demonstrated an increase in the number of repetitions
at 80% 1 RM using IPC as a warm-up strategy for strength exercises in trained men.
In addition to the lack of data on maximal strength capacities in trained individuals,
there is also a lack of consensus in the literature about the vascular occlusion pressures whenusing IPC. The pressures typically range from 10 to 300 mmHg [8,17], and it appears thatboth partial (low pressure) and total (high pressure) vascular occlusion can positively affectmuscle performance. Marocolo and colleagues compared the effects of IPC with 220 mmHg
to a SHAM procedure using 20 mmHg on muscle resistance during resistance exercise withthe lower limbs [9] and upper limbs [10] and reported that IPC increased the number ofmaximum repetitions in both occlusion pressures. Similarly, De Souza et al. [5] reported
improved muscle endurance at both high (220 mmHg) and low pressure (20 mmHg) whencompared to CON. However, Paradis-Deschênes et al. [11] observed strength benefits
during knee extensions with a high pressure (200 mmHg) only. Da Silva Novaes et al. [4]demonstrated that only 220 mmHg IPC procedure increased the total volume (i.e., thenumber of repetitions) within a resistance exercise session.
In the sport sciences, the low occlusion pressures (ex. 20 mmHg) have especially beenused as SHAM treatments [4,16] to demonstrate the potency of ischemic episodes. However,some authors [5,9,10] have suggested that there may be a potentially beneficial psychophysiological effect associated with low pressures. In fact, a pressure as low as 10% ofarterial occlusion pressure in the right arm (which equates to 15 mmHg) has been reported
to induce a 30% significant reduction in blood flow, and blood flow further decreased byalmost 50% when arterial occlusion pressure was increased to 30 mmHg only [18].
In addition, some authors [17,19] have suggested that a possible neural stimulus
acting through types III and IV afferent fibers may affect the neural drive, thereby increasing muscle strength. Along this line of reasoning, IPC has been shown to modulate theautonomic nervous system [20,21]. Heart rate variability (HRV) has been used to indirectly and non-invasively estimate sympathovagal balance after application of IPC [20–22].
Lopes et al. [21] demonstrated that IPC can accelerate recovery of HRV after high-intensity
exercise. Gardner et al. [20] showed that 2 weeks of IPC application positively changed thesympathovagal balance in healthy individuals. In this context, the use of HRV during theapplication of IPC at different pressures could be useful to elucidate part of the mechanisms
involved in the ergogenicity of low-pressure IPC.
Therefore, our goal was to evaluate the acute effects of ischemic preconditioning withhigh (IPChigh ) and low pressure of occlusion (IPClow ) on upper and lower limbs maximum
strength and heart rate variability in recreationally trained individuals. We hypothesizedthat both occlusion pressures would have positive effects on heart rate variability andmaximum strength.

that both occlusion pressures would have positive effects on heart rate variability andmaximum strength.
Int. J. Environ. Res. Public Health 2022, 19, 7655

2. Materials and Methods

3 of 132.1. Experimental Design
2. TheMaterials
andstudy
Methods
present
included 5 visits to the laboratory, separated by 3–7 days, always
2.1. Experimental
Designat thesame time of
day to avoid the circadian influence (Figure 1). In the first visit, all
The present
included 5consent
visits to thelaboratory,
separatedby 3–7 days,
alwaysparticipants
signedstudy
the informed
form
and fulfilled
the Physical
Activity
Readiat
the
same
time
of
day
to
avoid
the
circadianinfluence(Figure
1).
In
the
first
visit,
allness Questionnaire/PAR-Q. Anthropometric data collection and a familiarization of the 1
participants
signed theconsent
form and were
fulfilled
theperformed
Physical Activity
Readiness
repetition
maximum(1 informed
RM) testingprocedures
also
at thatvisit. During
Questionnaire/PAR-Q.
Anthropometricdatacollection
andafamiliarizationofthe
1 repe- In
the second visit, 1 RM retest was performed to access the load for the three protocols.
tition maximum (1 RM) testing procedures were also performed at that visit. During thethe third, fourth, and fifth visits, all participants were randomly assigned to three experisecond visit, 1 RM retest was performed to access the load for the three protocols. In thementalhighpressure
IPC (220
mmHg)(IPCassignedhigh) + 1 RM testing; (b) low presthird,protocols:
fourth, and(a)fifthvisits,all participants
wererandomly
to three experimental
sure
IPC
protocol
(20
mmHg)
(IPC
low
)
+
1
RM
testing;(c)
RM testingCON(controlprotocols: (a) high pressure IPC (220 mmHg) (IPChigh ) + 1 RM1 testing;(b) lowpressure
IPC protocol).
protocol (20 mmHg) (IPClow ) + 1 RM testing; (c) 1 RM testing CON (control protocol).

Figure 1. Study design. 1 RM TEST: one maximum repetition testing; IPC HP: ischemic precondition-

Figure 1. Study design. 1 RM TEST: one maximum repetition testing; IPC HP: ischemic precondiing high pressure (220 mmHg); IPC LP: ischemic preconditioning low pressure (20 mmHg); CON:tioning high pressure (220 mmHg); IPC LP: ischemic preconditioning low pressure (20 mmHg);
control protocol; HRV: heart rate variability.
CON: control protocol; HRV: heart rate variability.
2.2. Sample and Ethical Procedures

2.2. Sample
and EthicalProcedures
The study
included
16 men between 18 and 35 years of age, normotensive, physically

active,withat least one
year betweenof experience
in resistance1). Subjectsphysicallythat
The andstudy
included
16 men18 and35 yearsexerciseof age, (Table
normotensive,
responded
positively
to
any
of
the
items
Physical
Activity
Readiness
Questionnaire/PAR-Q[23],
active, and with at least one year of experience in resistance exercise (Table 1). Subjects
missed one or more visits of the collection procedures in the laboratory, presented somethat
responded positively to any of the items Physical Activity Readiness Questionnaire/PARtype of osteoarticular injury in the upper or lower limbs, had been taking some medication
Q [23], missed one or more visits of the collection procedures in the laboratory, presented
or supplements in the last 3 months before the collection, and smokers, were excluded fromsome
osteoarticular
injurythe
inrisks
the upper
or lowerlimbs,
had beentakingsigned
some medthe typestudy.ofAfterbeing explained
and benefitsof theresearch,
the subjects
icationor
supplements
in
the
last
3
monthsbeforethecollection,andsmokers,
were exthe informed consent form prepared according to the Helsinki declaration and approved
cludedfromexperiments
the study. by
AfterbeingRedonda
explained
the risksand benefitsof andthe Researchresearch, thefor human
the Volta
University
Center’s
local Ethics
Committee
underprotocol number
2,699,294.
During thestudy period,
were
subjects
signedthe informed
consent
form preparedaccordingto theparticipants
Helsinki declaration
instructedtorestrainfrom
exercise
as
well
as
avoid
caffeine,
nutritional
supplements,
and approved for human experiments by the Volta Redonda University Center’s local
and andalcoholintake 48
h before, during,after theentire2,699,294.
study, sleep
for a minimum
EthicsResearch
Committee
under andprotocolnumberDuringthe study peof six hours on the night before the test session, and not perform the valsava maneuver
riod, participants were instructed to restrain from exercise as well as avoid caffeine, nuduring the execution of the exercises. The average time between visits to the laboratory
tritional supplements, and alcohol intake 48 h before, during, and after the entire study,
was 3.5 ± 0.6 days.

Int. J. Environ. Res. Public Health 2022, 19, 7655

4 of 13

Table 1. Characteristics of subjects (n = 16).
Age (years)
Height (cm)Weight (kg)BMI (kg m−2 )Training history (years)
Bench press 1 RM (kg)Leg Press 1 RM (kg)Lat pull down 1 RM (kg)Hack machine 1 RM (kg)Shoulder press 1 RM (kg)
Back squat 1 RM (kg)
LFnu
HFnu
LF/HF ratio
RMSSD (ms)SDNN (ms)pNN50 (%)
Heart rate (BPM)

27.8 ± 3.8
180.4 ± 6.1
82.6 ± 8.8
25.3 ± 1.8
2.4 ± 1.0
84.6 ± 10.6
267.4 ± 50.8
94.2 ± 7.8
117.5 ± 23.2
70.2 ± 7.6
92.9 ± 16.5
62.5 ± 9.2
40.2 ± 10.1
1.6 ± 0.6
41.9 ± 19.6
30.5 ± 4.0
4.4 ± 2.9
66.1 ± 11.9

BMI: body mass index; 1 RM: one repetition maximum; LF = low frequency in normalized units; HF = highfrequency in normalized units; LF/HF ratio; RMSSD (ms) = square root of the sum of the square of the differences
between the R-R intervals divided by the number of R-R intervals; SDNN (standard deviation of all normal RR
intervals (ms); pNN50 corresponds to the percentage difference between adjacent NN intervals that are greaterthan 50 ms.

2.3. Procedures
2.3.1. Ischemic Preconditioning Protocols
The IPChigh protocol session consisted of 4 cycles of 5 min of occlusion at 220 mmHg
pressure using a 57 × 9 cm pneumatic tourniquet applied around the subaxillary regionof the upper arm (komprimeterRiester® , Jungingen, Germany) with 5 min alternation ofreperfusion at 0 mmHg. This resulted in a total intervention of 40 min. The pressure used
and the breadth of the cuff are in accordance with previous studies [4,16]. In order to verify
that the individuals had the blood flow obstructed during the intervention, the radial pulse
was manually checked by digital palpation.
The IPClow protocol session consisted of 4 cycles of 5 min of occlusion at 20 mmHg
pressure, as proposed in previous studies [4,16], alternating with 5 min at 0 mmHg for a
total of 40 min. The subjects remained seated during the intervention, lasting 40 min [4,16].
2.3.2. Anthropometric Evaluation
Height and body mass were measured with a 0.5 cm precision stadiometer and a
0.1 kg precision Filizola® scale, respectively. All measurements were performed following
the recommendations of ACSM [13]. These measurements were subsequently equated toobtain the body mass index (BMI) in kg m−2 .
2.3.3. One Repetition Maximum (1 RM) Testing
The intervention’s load prescription was evaluated through the 1 RM test [13]. The
evaluations were performed on the days of the laboratory visits as described in Figure 1.
The flowing exercises were performed in that same sequence every time, with 10 minof rest in-between: bench press (BP), front latissimus pull-down (FLPD), and shoulderpress (SP) for upper limbs, and leg press 45º (LP45), hack machine (HM), and Smith Squat(SS) for lower limbs. Individuals started warming-up with two sets of 5–10 repetitions
at 40–60% of the maximum perception of the individual’s strength, separated by 1 min.
After a 1 min interval, they performed a third set of 3–5 repetitions at 60–80% of the
maximum perceived strength. After another minute of rest, the strength testing evaluation
was initiated. Five trials were performed for every exercise, adjusting the load before every
trial to obtain a precise evaluation of the 1 RM. The recovery time between the attempts
was standardized in 5 min. The test was interrupted when the individual could not execute

Int. J. Environ. Res. Public Health 2022, 19, 7655

5 of 13the movement correctly, being considered that repetition of the maximum load with theexecution completed.
The following strategies were adopted to reduce the margin of error in data collection
procedures: (a) standardized instructions given before the tests, so that each tested subject
was aware of the routine involved in data collection, (b) the tested subject was instructed on
the proper technique for performing the exercise, (c) all participants received standardized
verbal encouragement during the tests, and (d) all tests were performed at the same time of
day for each session. The highest load achieved between the two days was considered the
1 RM [4].
2.3.4. Heart Rate Variability (HRV)A Polar Electro Oy (Kempele, Finland) 800CX monitor was used 10 min before IPC
maneuvers, during IPC maneuvers (every 5 min up to 40 min), and after each experimental
protocol and always before performing the 1 RM tests, with the volunteers in the sitting
position during the rest. During recordings, participants were asked to keep their eyes
open, breathe calmly, and avoid movement. The cardiofrequencemeter had a sampling
frequency of 1000 Hz, fixed by an elastic belt at the height of the sternum (1/3 lower)
and with simultaneous transmission to the clock fixed on the left arm handle, where theregister was stored. Later, through the infrared sensor serial port interface the data wastransported and stored in the Polar Precision Performance program on an Acer® branded
computer. This data was exported and analyzed in Kubios HRV Analysis Program 2.0
software (version 2.2, Kuopio, Finland). After noise removal through visual inspectionof the iRR distribution (ms), the most stable period over 5 min was selected [22] andtime-domain and frequency-domain were extracted. For time-domain analysis, the squareroot of the sum of the differences between the R-R intervals divided by the number of R-R
intervals was calculated, and for frequency-domain spectral analysis LF (low frequency),
HF (high frequency), and LF/HF ratio were calculated.
2.4. Statistical Analysis
The results are presented in mean ± standard deviation values. The normality wasverified by the Shapiro–Wilk test and the homoscedasticity was confirmed by the Levene
test. One-way ANOVA with repeated measurements was used to test interactions andcompare the means of the 1 RM tests. Significant differences were identified by Tukey’s
post-hoc test. The two-way ANOVA analysis of variance for repeated measurements
was performed to determine the differences in experimental protocols for dependent
variables (RMSSD, HFnu , LFnu , LF/HF, SDNN, pNN50, and HF). To determine the specificdifferences, Tukey’s post-hoc test was performed. The Effect Size (ES) (Cohen’s d) estimates
were calculated using the standardized mean difference to determine the magnitude of
the treatment effects. The magnitude of each ES was interpreted using the scale proposedby Rhea [24]. The changes in (∆%) were calculated for the variables (RMSSD, HFnu , LFnu ,LF/HF, SDNN, pNN50, and HF) comparing the baseline moment with the moments
after the exercises. All the analyses were performed in the SPSS software (SPSS Inc.,
V.21, Chicago, IL, USA) and considered an alpha value of 5% (p < 0.05). The sample size
calculation [25] for the study was performed with G*Power (ver. 3.1.9.7; Heinrich-HeineUniversität Düsseldorf, Düsseldorf, Germany) with an N of 16 individuals for a power of
0.8, α = 0.05, correlation coefficient of 0.5, nonsphericity correction of 1, and an effect sizeof 0.32.
3. Results
High intra-class coefficients of correlation (ICCs) were found for the 1 RM test–retest
for all exercises: BP (0.954), LP (0.976), LPD (0.964), HM (0.948), SP (0.990), and SS (0.988).
All variables tested demonstrated a normal distribution (p > 0.05). The ES, p-values,
and percentage changes (∆%) for experimental conditions for LFnu , HFnu, LF/HF ratio,

Int. J. Environ. Res. Public Health 2022, 19, 7655

6 of 13RMSSDms SDNNms , pNN50 (%), and heart rate for each condition and time point arepresented in Table 2.
Table 2. IPC high and low pressure effects on HRV variables.
IPC High Pressure
P

ES

∆%

20 min During
5 min Post

0.88
1.00

0.80
1.08

14.09
18.92

20 min During
5 min Post
LF/HF
20 min During
5 min PostRMSSD ms.
20 min During
5 min Post
SDNN ms.
20 min During
5 min Post
pNN50 (%)
20 min During
5 min Post
Heart rate (BPM)
20 min During
5 min Post

1.00
1.00

−1.24
−1.03

0.91
1.00

IPC Low Pressure
P

ES

∆%

P

1.16
1.26

16.55
17.98

0.04
0.03

−31.10−36.84

LF-n.u.
0.19
0.01
HF-n.u.
0.01
0.01

−1.13
−0.56

−36.91−39.47

0.07
0.84

2.58
2.75

110.89118.53

0.28
0.20

4.86
4.14

149.85127.87

0.01
0.07

0.25
1.00

−0.26
−3.55

−17.22−41.61

0.98
0.13

−3.81
−3.62

−50.62−49.83

0.02
0.02

1.00
1.00

0.24
0.62

5.08
14.04

1.00
0.65

0.16
0.60

2.26
14.09

1.00
1.00

1.00
1.00

0.15
−0.42

10.74
−22.09

1.00
1.00

−0.02
0.07

−1.63
7.35

1.00
1.00

1.00
1.00

0.60
0.60

6.72
6.67

0.94
0.94

0.88
0.80

8.91
8.06

0.71
0.82

IPC high pressure: ischemic preconditioning protocol 220 mmHg; IPC low pressure: ischemic preconditioning
protocol 20 mmHg; ES = effect size; ∆% = difference between post and baseline moments in percentage; LF = lowfrequency in normalized units; HF = high frequency in normalized units; LF/HF ratio; RMSSDms = square root of
the sum of the square of the differences between the R-R intervals divided by the number of R-R intervals; SDNN
(standard deviation of all normal RR intervals (ms)); pNN50 corresponds to the percentage difference between
adjacent NN intervals that are greater than 50 ms.

The maximal strength was significantly (p < 0.05) higher in both IPChigh and IPClow
compared with CON for BP, LPD, and SP (Figure 2). Significant protocol x treatment for
BP (F(15,30) = 63.2; p = 0.0001; eta2 = 0.954) displayed increases from CON with IPChighand IPClow (Figure 2). Significant protocol x treatment for LPD (F(15,30) = 27.2; p = 0.0001;
eta2 = 0.884) displayed increases from CON with HP and LP (Figure 2). Significant protocol
x treatment for SP (F(15,30) = 48.8; p= 0.0001; eta2 = 0.933) displayed increases from CON
with IPChigh and IPClow (Figure 2).
The maximal strength was significantly (p < 0.05) higher in IPChigh and IPClow compared with CON for LP45, HM, and SS (Figure 3). Significant protocol × treatment for
LP45 (F(15,30) = 40.2; p = 0.0001; eta2 = 0.924) displayed increases from CON with IPChighand IPClow (Figure 3). Significant protocol × treatment for HM (F(15,30) = 35; p = 0.0001;
eta2 = 0.894) displayed increases from CON with IPChigh and IPClow (Figure 3). Significant
protocol x treatment for SS (F(15,30) = 164; p = 0.0001; eta2 = 0.976) displayed increases from
CON with IPChigh and IPClow (Figure 3).

Environ. Res. Public Health 2022, 19, x FOR PEER REVIEW
Int. J. Environ. Res. Public Health 2022, 19, 7655

7 of 13

Figure 2. Maximal strength in control and IPC high and low pressure. 1 RM: one maximum repeti-

Figure2. Maximal
strength
in control
and
IPC(220highand lowlowpressure:pressure.
1 RM: ontion; highpressure: ischemic
preconditioninghighpressuremmHg);
ischemicpreconditioning
low pressure(20 mmHg);* p < 0.05 vs. baseline.
tion;high pressure:ischemicpreconditioning
high pressure (220 mmHg); low
preconditioning low pressure (20 mmHg); * p < 0.05 vs. baseline.

The maximal strength was significantly (p < 0.05) higher in IPChighpared with CON for LP45, HM, and SS (Figure 3). Significant protoco
LP45 (F(15,30) = 40.2; p = 0.0001; eta2 = 0.924) displayed increases from CON
IPClow (Figure 3). Significant protocol × treatment for HM (F(15,30) = 35;
0.894) displayed increases from CON with IPChigh and IPClow (Figure 3). S
col x treatment for SS (F(15,30) = 164; p = 0.0001; eta2 = 0.976) displayed incr
with IPChigh and IPClow (Figure 3).

Environ. Res. Public Health 2022, 19, x FOR PEER REVIEW
Int. J. Environ. Res. Public Health 2022, 19, 7655

8 of 13

Figure 3. 1 RM in control and IPC high and low pressure. 1 RM (one maximum repetition) in control

Figure3.401 min
RMifincontroland IPC highand(220
lowpressure.
RM(onepressure.
maximum r
and after
ischemicpreconditioning
with highmmHg)
and low1(20mmHg)* p <after
0.05 vs.
and
40control.
min if ischemic preconditioning with high (220 mmHg) and low (2* p < 0.05
vs. control.
No significant
differences were found in the comparison across the different experi-mental conditions for LFnu , HFnu , LF/HF ratio (Figure 4), RMSSDms ., SDNNms ., pNN50(%), Noand heartrate (Figure5). However, significant
intra-protocol
were identisignificant
differenceswere foundin thedifferencescomparison
across thefied. LFnu increased (p < 0.05) from baseline at 10, 15, 25, 30, 35, 40 min and 5-min-post formentalconditions
for baseline
LFnu, HF
, LF/HF
ratio(Figure4), RMSSD
ms., SDN
IPChigh (Figure4) and fromat 5,nu10,
20, 25, 30,
40 minand 5-min-post
for IPClow(Figure4).
HF
decreased
(p
<
0.05)
from
baseline
at
10,
15,
20,
25,
30,
35,
40
min
and
nu (Figure 5). However, significant intra-protocol difference
and heart rate
5-min-post for IPChigh (Figure 4) and from baseline at 5, 10, 25, 30, and 40 min for IPClow
LF(Figurenu increased< increased0.05) frombaseline
at 10,at15,
25,
35,and4040minand 5-m4). LF/HF (pratio(p < 0.05)
from baseline
5, 10,
20,30,
25, 30,min for
IPClow only
(Figurefrom
4).
(Figure4) andbaseline at 5, 10, 20, 25, 30, 40 min and 5-min-post4). HFnu decreased (p < 0.05) from baseline at 10, 15, 20, 25, 30, 35, 40 mi
for IPChigh (Figure 4) and from baseline at 5, 10, 25, 30, and 40 min for
LF/HF ratio increased (p < 0.05) from baseline at 5, 10, 20, 25, 30, and 40 m
(Figure 4).

nt. J. Environ. Res. Public Health 2022, 19, x FOR PEER REVIEW
Int. J. Environ. Res. Public Health 2022, 19, 7655

9 of 13

Figure 4. 4.LF,
HF,HF,
and and
LF/HF
ratio during
after IPC
andIPClow highpressure.
LF pressure.
= low
FigureLF,
LF/HF
ratio andduringandhighafter
and(A)
low(A
frequencyinnormalized
units;
(B)
HF
=
high
frequencyinnormalized
units;(C)
LF/HF
ratio;
highquency in normalized units; (B) HF = high frequency in normalized units; (C) LF
pressure: ischemic preconditioning protocol 220 mmHg; low pressure: ischemic preconditioningpressure:ischemic preconditioning protocol 220 mmHg; low pressure: ischemic p
protocol 20 mmHg; * p < 0.05 IPChigh vs. baseline; † p < 0.05 IPClow vs. baseline; a p < 0.05 IPChighprotocol20 mmHg; * p < 0.05 IPChigh vs. baseline; † p < 0.05 IPClow vs. baseline; a p <vs. IPClow .
IPClow

Furthermore, RMSSDms decreased (p < 0.05) from baseline at 5, 10, 15,
40 min and 5-min-post for IPClow only (Figure 5).

es. Public Health 2022, 19, x FOR PEER REVIEW

10 of 13

Int. J. Environ. Res. Public Health 2022, 19, 7655

10 of 13

Figure 5. RMSSD and
pND50
duringandandafter during
IPC highlow
Figure5. RMSSD
pND50
andandafter
IPCpressure.
high and (A)low RMSSD;
pressure. (B)(A) SDNN;RMSSD; (B) SDNN;(C) pNN50; (D) heart
rate;
high
pressure:ischemicpreconditioning
protocol220
mmHg;
pres-low pressure:(C) pNN50; (D) heart rate; high pressure: ischemic preconditioning protocol 220low
mmHg;† p < 0.05 IPClow vs. baseline.
sure: ischemic preconditioning
protocol20
mmHg;
ischemic preconditioning protocol 20 mmHg; † p < 0.05 IPC
vs. baseline.
low

4. Discussion

Furthermore, RMSSDms decreased (p < 0.05) from baseline at 5, 10, 15, 20, 25, 30, 35,
40min
5-min-post
for IPClowthe
only(Figure5). of ischemic preconditionThe objective of thisandstudy
was to evaluate
acute
effects

ing with high (IPC
) and low pressure of occlusion (IPClow) on upper and lower limb
4.highDiscussion
maximum strength andrateofvariability
in torecreationallytrainedindividuals.
The
Theheart
objective
this study wasevaluate the acuteeffectsof ischemic preconditioning
main findings were:
IPC(IPCwithboth pressures equally increased maximal strength forwith(1)high
high ) and low pressure of occlusion (IPClow ) on upper and lower limb
all exercises comparedtoCON
testing;
IPC rate
withvariability
both pressures
induced higher
maximum strength and(2)heart
in recreationallytrainedactivity
individuals. Theof the low frequencynu) andlowerof boththe high
frequencynu) during
the strength
main(LF
findings
were:(1)activity
IPC withpressures
equally(HF
increased
maximalforonly
all exercises
compared
to CON increased
testing; (2) the
IPC sympathovagal
with both pressures
induced higher
maneuver; and (3)IPC with
low pressurebalanceactivity ofthe
the RMSSD-ms
low frequencyvs.
(LF
lower activity
themaneuver.
high frequency(HFnu ) duringnu ) andvalues(LF/HF ms2) and reduced
restingduringofthe
To ourthe
maneuver;
and
(3)
only
IPC
with
low
pressure
increasedthesympathovagal
best knowledge, this study is the first to investigate the acute effects of IPC on maximum balance(LF/HF ms2) and reduced the RMSSD-ms vs. resting values during the maneuver. To ourstrength development in six multi-articular, upper and lower limb resistance exercises.
best knowledge, this study is the first to investigate the acute effects of IPC on maximum
IPC at high pressures(i.e., >200 mmHg) has consistently been shown to increase isostrength development in six multi-articular, upper and lower limb resistance exercises.
metric [7,8] and dynamic
strength[4,5,10], (i.e.,
as wellasmmHg)the numberof repetitions
exercises
IPC at high pressures>200
has consistently
beeninshownto increase isoinvolving both lower[4,5,9]anddynamic
upper limbs[4,10,16].
oc-in exercises
metric[7,8] andstrength[4,5,10],Thus,
as welltheseas thetransientnumber ofvascular
repetitions
clusions have been
proposeda potential
enhancestrengthvascularin
involving
both aslower[4,5,9] andwarm-up
upper limbsstrategy[4,10,16].toThus,
these transient
occlusions
have
been
proposedasapotential
warm-upstrategytoenhancestrengthintrainedtrained men [16]. Although high pressures induce local hypoxia, benefiting from the hymen [16]. Althoughhigh pressures
local
hypoxia,
benefiting
the hypoxia- andpoxia- and reperfusion-related
complexcascadeinduce
events,they
do notalwaysfrom
promotereperfusion-related
complexcascadeevents,theydonotalwayspromotehigher muscle
higher muscle performance as compared with a placebo application with low pressure.
performance as compared with a placebo application with low pressure. For example,
For example, both IPC and placebo interventions were reported to enhance acute muscle
both IPC and placebo interventions were reported to enhance acute muscle endurance
endurance duringduring
knee extensions[9]. Such benefits were also reported after 4–5 days ofknee extensions [9]. Such benefits were also reported after 4–5 days of daily IPC
daily IPC and placebo
applicationonmaximalloadload
duringa 12-RM
test
and placebo application
on maximal
duringa 12-RM
testofofthe
theelbow
elbow flexflexors [10] andors [10] and endurance during knee extensions [5]. Our current results add to the literatureby showing that IPC with high and low pressures may equally increase acute maximal
strength capacity.
Marocolo et al. [9,10] and De Souza et al. [5] have suggested that there may actually
be a psycho-physiological effect of the maneuver instead of only a placebo effect, which

Int. J. Environ. Res. Public Health 2022, 19, 7655

11 of 13endurance during knee extensions [5]. Our current results add to the literature by showingthat IPC with high and low pressures may equally increase acute maximal strength capacity.
Marocolo et al. [9,10] and De Souza et al. [5] have suggested that there may actually bea psycho-physiological effect of the maneuver instead of only a placebo effect, which could
explain the increased performance with both low and high occlusion pressures. However,
unfortunately, they did not analyze any physiological nor psychological responses to
IPC so their conclusions remain speculative. The current study is therefore the first toevaluate the heart rate variability during and after the maneuvers, in order to ascertain
the presence of a possible neurophysiological effect that could explain the ergogenic effectof IPClow observed here and elsewhere. Our findings showed that both IPC at 220 and
20 mmHg induced a predominance of the low frequency over the high frequency during
the maneuvers. However, only the IPClow increased the sympathovagal balance (LF/HFms2) and reduced the RMSSD-ms.
Heart rate variability has been used to indirectly and non-invasively evaluate parasympathetic and sympathetic activity after application of IPC [20–22]. The changes observed
during IPClow may be related to a spontaneous inhibition of afferent fibers of type III and IV
caused by the acute release of opioids, a specific group of autacoids, after the application of
the IPC [26]. According to Cruz et al. [26], IPC can alter the receptors’ activation threshold,desensitizing the groups III and IV afferent fibers. Such phenomenon can maintain or evenincrease the neural drive and the number of motor units recruited; thus, increasing thestrength production. Some studies have examined the autonomic nervous activity after
IPChigh maneuvers [19–21]. Lopes et al. [21] investigated the effect of IPChigh on autonomic
cardiac recovery after repeated high-intensity sprints. They demonstrated an increase in HR
recovery within 60 s, which indicates a higher activity of parasympathetic nervous system(PNS) and a reduction in SNS activity. On the other hand, Incognito et al. [19] reported
no impact of IPChigh on SNS activity up to 3 min after a handgrip isometric strength test.
Enko et al. [27] (14) showed an increase in PNS activity and a reduction in noradrenaline
after 30 min of IPChigh applied to the arms. Recently, Gardner et al. [20] demonstrated that
2 weeks of IPChigh (220 mmHg) changed the sympathovagal balance in healthy individuals.
Importantly, all of the above studies used a high pressure and, to our best knowledge,
there is no report of autonomous nervous system activity during and after a low-pressure
maneuver. The pressure of 20 mmHg used in the current investigation did induce changes
in the heart rate variability. This is in line with the observation that a pressure as low
as 15 mmHg can cause significant physiological changes [18]. Therefore, the “placebo”
effect that some studies reported [5,9,10], may represent a true physiological effect in somepeople. In fact, Mouser and colleagues [28] have suggested that the restriction pressure
should be individualized since a given absolute pressure may induce completely different
restriction values among different individuals. As a future direction in this field, it may
be relevant to identify low- vs. high-pressure “responders” to determine the individual
IPC limit of effectiveness and implement more comfortable, but still efficient, protocols forvaried people.
Main methodological limitations of the study and perspectives include the following:(a) the short interval between the IPC maneuver and the maximum strength test may haveinterfered with the effects of IPChigh , as reported in previous studies [28,29], and could
have reduced the amplitude of change compared with IPClow . Thus, future research should
elucidate the impact of such a methodological parameter in the efficacy of IPC in increasing
maximum strength; (b) in the present study, the autonomic nervous system was not directly
evaluated limiting our interpretation of the data; and (c) HRV is an indirect measure ofcardiac vagal control, as it relies on heart rate measurements rather than direct neuralrecording of cardiac vagal control. Therefore, our conclusions still need to be correlatedwith and validated by more direct evaluation of the activity of the autonomic nervous
system, such as peroneal microneurography or plasma catecholamines measurements.
Future study protocols will need to verify the current data.

Int. J. Environ. Res. Public Health 2022, 19, 7655

12 of 13

5. Conclusions
In conclusion, both IPC maneuvers with high and low pressure acutely increased
the maximum strength in varied resistance exercises compared with the CON condition.
Our findings showed that there seems to be a physiological effect acting through thesympathovagal balance evaluated through heart rate variability, which may explain, atleast in part, the psycho-physiological hypothesis argued in previous studies [5,9,10]. This
physiological effect may explain the increased performance in both experimental conditions
when compared with the CON protocol. Therefore, a total occlusion may not be necessary
to cause the acute effects on the maximum strength in every individual.
For coaches of strength and conditioning sports who seek new strategies to improve
athlete’s competition performance and neuromuscular adaptations, we recommend the useof IPC before resistance training and before competitions with the objective of increasing
maximum strength. In this study, the interventions consisted of 4 × 5 min of occlusion
with two intensities (20 and 220 mmHg) alternated with 4 × 5 min of reperfusion, totaling 40 min of pre-conditioning, and both improved maximum strength. Coaches may
choose to substantially decrease the occlusion pressure considering the athlete’s perceptionof discomfort.
Author Contributions: Conceptualization, L.G.T., J.M.V. and J.d.S.N.; data curation, F.B. and J.d.S.N.;
formal analysis, F.B, L.L. and J.d.S.N.; investigation, L.G.T., C.G.J., A.d.S.R., J.M.V., P.P. and J.d.S.N.;
methodology, L.G.T., A.d.S.R.; C.G.J., P.P., J.M.V. and J.d.S.N.; project administration, L.G.T. and
J.d.S.N.; resources, C.G.J., A.d.S.R., A.C.B., J.d.S.N. and J.M.V.; supervision, J.d.S.N., J.M.V. and L.L.;
validation, L.G.T., L.L., A.C.B. and F.B.; visualization, L.G.T., F.B. and J.d.S.N.; writing—original draft,
L.G.T., F.B. and J.d.S.N.; writing—review and editing, L.G.T., L.L., J.M.V. and J.d.S.N. All authors
have read and agreed to the published version of the manuscript.
Funding: The Portuguese Foundation for Science and Technology (I.P., Grant/Award Number
UIDB/04748/2020) funded this research.
Institutional Review Board Statement: Study was approved by Volta Redonda University Center’s
local Ethics and Research Committee under protocol number 2,699,294 and carried out in accordancewith the Declaration of Helsinki guidelines.
Informed Consent Statement: All subjects of the study delivered informed consent.
Data Availability Statement: Available through the corresponding author by request.
Acknowledgments: The authors gratefully acknowledge the financial support from the Polytechnic
Institute of Setúbal.
Conflicts of Interest: The authors declare no conflict of interest.

References
1.
2.
3.
4.

5.
6.

7.

Murry, C.E.; Jennings, R.B.; Reimer, K.A. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium.
Circulation 1986, 74, 1124–1136. [CrossRef] [PubMed]
De Groot, P.C.E.; Thijssen, D.H.J.; Sanchez, M.; Ellenkamp, R.; Hopman, M.T.E. Ischemic preconditioning improves maximal
performance in humans. Eur. J. Appl. Physiol. 2010, 108, 141–146. [CrossRef] [PubMed]
Paull, E.J.; Van Guilder, G.P. Remote ischemic preconditioning increases accumulated oxygen deficit in middle-distance runners.
J. Appl. Physiol. 2019, 126, 1193–1203. [CrossRef] [PubMed]
Novaes, J.D.S.; Telles, L.G.D.S.; Monteiro, E.R.; Araujo, G.D.S.; Vingren, J.L.; Panza, P.S.; Reis, V.M.; Laterza, M.C.; Vianna,
J.M. Ischemic Preconditioning Improves Resistance Training Session Performance. J. Strength Cond. Res. 2020, 35, 2993–2998.
[CrossRef] [PubMed]
De Souza, H.L.; Arriel, R.A.; Hohl, R.; da Mota, G.R.; Marocolo, M. Is ischemic preconditioning intervention occlusion-dependent
to enhance resistance exercise performance. J. Strength Cond. Res. 2019, 35, 2706–2712. [CrossRef]
Surkar, S.M.; Bland, M.D.; Mattlage, A.E.; Chen, L.; Gidday, J.M.; Lee, J.-M.; Hershey, T.; Lang, C.E. Effects of remote limb
ischemic conditioning on muscle strength in healthy young adults: A randomized controlled trial. PLoS ONE 2020, 15, e0227263.
[CrossRef]
Barbosa, T.; Machado, A.C.; Braz, I.D.; Fernandes, I.A.; Vianna, L.; Nobrega, A.C.L.; Silva, B.M. Remote ischemic preconditioning
delays fatigue development during handgrip exercise. Scand. J. Med. Sci. Sports 2014, 25, 356–364. [CrossRef]

Int. J. Environ. Res. Public Health 2022, 19, 7655

8.
9.
10.
11.
12.

13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.

13 of 13

Tanaka, D.; Suga, T.; Tanaka, T.; Kido, K.; Honjo, T.; Fujita, S.; Hamaoka, T.; Isaka, T. Ischemic Preconditioning Enhances Muscle
Endurance during Sustained Isometric Exercise. Endoscopy 2016, 37, 614–618. [CrossRef]
Marocolo, M.; Willardson, J.M.; Marocolo, I.C.; Mota, G.R.; Simão, R.; Maior, A.S. Ischemic Preconditioning and PlaceboIntervention Improves Resistance Exercise Performance. J. Strength Cond. Res. 2016, 30, 1462–1469. [CrossRef]
Marocolo, M.; Marocolo, I.C.; da Mota, G.R.; Simão, R.; Maior, A.S.; Coriolano, H.-J.A. Beneficial Effects of Ischemic Preconditioning in Resistance Exercise Fade Over Time. Endoscopy 2016, 37, 819–824. [CrossRef]
Paradis-Deschênes, P.; Joanisse, D.R.; Billaut, F. Ischemic preconditioning increases muscle perfusion, oxygen uptake, and force instrength-trained athletes. Appl. Physiol. Nutr. Metab. 2016, 41, 938–944. [CrossRef] [PubMed]
Carvalho, L.; Concon, V.; Meloni, M.; De Souza, E.O.; Barroso, R. Effects of resistance training combined with ischemic
preconditioning on muscle size and strength in resistance-trained individuals. J. Sports Med. Phys. Fit. 2020, 60, 1431–1436.
[CrossRef] [PubMed]
ACSM. American College of Sports Medicine’s Guidelines for Exercise Testing and Prescription, 10th ed.; Guidelines for Exercise Testing
and Prescription Description; Wolters Kluwer Health: Philadelphia, PA, USA, 2018.
Kilduff, L.P.; Finn, C.V.; Baker, J.S.; Cook, C.; West, D. Preconditioning Strategies to Enhance Physical Performance on the Day ofCompetition. Int. J. Sports Physiol. Perform. 2013, 8, 677–681. [CrossRef] [PubMed]
Winwood, P.W.; Pritchard, H.J.; Wilson, D.; Dudson, M.; Keogh, J.W.L. The Competition-Day Preparation Strategies of Strongman
Athletes. J. Strength Cond. Res. 2019, 33, 2308–2320. [CrossRef] [PubMed]
Telles, L.G.D.S.; Carelli, L.C.; Bráz, I.D.; Junqueira, C.; Monteiro, E.R.; Reis, V.M.; Vianna, J.M.; Novaes, J.D.S. Effects of Ischemic
Preconditioning as a Warm-Up on Leg Press and Bench Press Performance. J. Hum. Kinet. 2020, 75, 267–277. [CrossRef] [PubMed]
Carvalho, L.; Barroso, R. Ischemic Preconditioning Improves Strength Endurance Performance. J. Strength Cond. Res. 2019, 33,
3332–3337. [CrossRef] [PubMed]
Mouser, J.G.; Ade, C.J.; Black, C.D.; Bemben, D.A.; Bemben, M.G. Brachial blood flow under relative levels of blood flow
re-striction is decreased in a nonlinear fashion. Clin. Physiol. Funct. Imaging 2018, 38, 425–430. [CrossRef]
Incognito, A.V.; Doherty, C.J.; Lee, J.B.; Burns, M.J.; Millar, P.J. Ischemic preconditioning does not alter muscle sympathetic
responses to static handgrip and metaboreflex activation in young healthy men. Physiol. Rep. 2017, 5, e13342. [CrossRef]
Gardner, R.N.; Sabino-Carvalho, J.L.; Kim, J.; Vianna, L.C.; Lang, J.A. Two weeks of remote ischaemic preconditioning alters
sympathovagal balance in healthy humans. Exp. Physiol. 2020, 105, 1500–1506. [CrossRef]
Lopes, T.; Sabino-Carvalho, J.L.; Ferreira, T.H.N.; Succi, J.E.; Silva, A.C.; Silva, B. Effect of Ischemic Preconditioning on the
Recovery of Cardiac Autonomic Control from Repeated Sprint Exercise. Front. Physiol. 2018, 9, 1465. [CrossRef]
Task Force of the European Society of Cardiology the North American Society of Pacing Electrophysiology. Heart rate variability:
Standards of measurement, physiological interpretation, and clinical use. Circulation 1996, 93, 1043–1065. [CrossRef]
Shephard, R.J. PAR-Q, Canadian Home Fitness Test and Exercise Screening Alternatives. Sports Med. 1988, 5, 185–195. [CrossRef][PubMed]Rhea, M.R. Determining the Magnitude of Treatment Effects in Strength Training Research Through the Use of the Effect Size.
J. Strength Cond. Res. 2004, 18, 918–920. [CrossRef] [PubMed]
Beck, T.W. The Importance of A Priori Sample Size Estimation in Strength and Conditioning Research. J. Strength Cond. Res. 2013,27, 2323–2337. [CrossRef] [PubMed]
Cruz, R.S.; Pereira, K.L.; Lisbôa, F.D.; Caputo, F. Could small-diameter muscle afferents be responsible for the ergogenic effect oflimb ischemic preconditioning? J. Appl. Physiol. 2017, 122, 718–720. [CrossRef] [PubMed]
Enko, K.; Nakamura, K.; Yunoki, K.; Miyoshi, T.; Akagi, S.; Yoshida, M.; Toh, N.; Sangawa, M.; Nishii, N.; Nagase, S.; et al.
Intermittent arm ischemia induces vasodilatation of the contralateral upper limb. J. Physiol. Sci. 2011, 61, 507–513. [CrossRef]
Lisbôa, F.D.; Turnes, T.; Cruz, R.S.; Raimundo, J.A.; Pereira, G.S.; Caputo, F. The time dependence of the effect of ischemic
preconditioning on successive sprint swimming performance. J. Sci. Med. Sport 2017, 20, 507–511. [CrossRef]
Salvador, A.F.; de Aguiar, R.A.; Lisbôa, F.; Pereira, K.L.; Cruz, R.; Caputo, F. Ischemic Preconditioning and Exercise Performance:
A Systematic Review and Meta-Analysis. Int. J. Sports Physiol. Perform. 2016, 11, 4–14. [CrossRef]