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Brazilian Journal of Motor Behavior
Special issue:
“Fatigue issue in the performance of motor skills”
!
Lemos, Santos,
Carpes
2023
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Sex differences in delayed onset muscle soreness induced by fatigue and measured by
different methods
ANDRESSA L. LEMOS | MILENA A. SANTOS | FELIPE P. CARPES
Applied Neuromechanics Research Group, Multicenter Graduate Program in Physiological Sciences, Federal University of Pampa, Uruguaiana, RS, Brazil
Correspondence to:!Felipe P Carpes, Ph.D.
Federal University of Pampa - Laboratory of Neuromechanics
97500-970, Uruguaiana, RS, Brazil
Phone office: +55 55 3911 0225
email: carpes@unipampa.edu.br
https://doi.org/10.20338/bjmb.v17i5.389
HIGHLIGHTS
• DOMS assessed with a NRS is comparable between
men and women.
• Absolute values of pressure pain thresholds were lower
in women.
• Pressure pain thresholds data require normalization for
sex-comparisons.
ABBREVIATIONS
CPGS Chronic Pain Grade Scale
DOMS Delayed onset muscle soreness
GEE Generalized estimating equation
MPQ McGill Pain Questionnaire
NRS Numeric pain rate scale
PPT Pressure pain thresholds
RF Rectus femoris
VAS Visual Analog Scale
VL Vastus lateralis
PUBLICATION DATA
Received 21 08 2023
Accepted 26 09 2023
Published 30 09 2023
BACKGROUND: Controversial outcomes from different methods for assessment of delayed
onset muscle soreness (DOMS) in male and female may influence clinical decisions.
AIM: In this study, we determine sex differences in pain perception and pain thresholds in a
DOMS condition resultant of a fatigue protocol.
METHOD: 11 male and 15 female healthy adults were submitted to an exercise fatigue
protocol to induce DOMS in the quadriceps muscles. Pain perception was determined using a
numeric pain rate scale (NRS) and pressure pain thresholds (PPT) were determined by
mechanical pressure in the vastus lateralis (VL) and rectus femoris (RF) regions. Data were
compared between methods and sexes at baseline, immediately after (0h), and 48 h after
DOMS induction.
RESULTS: Results showed normalized lower PPT and higher NRS outcomes after fatigue,
without sex differences. Absolute values of PPT showed lower values in females comparing
both time and sex (VL and RF, baseline p = 0.002 and p = 0.009; 0h p = 0.002 and p = 0.001;
48h p<0.0001 and p<0.0001) with a mean difference for females and males on 0h and 48h of
from baseline VL 16,52% and 19.7%; -15.64% and -10.89%; RF 12.18% and 20.7%; -9.18%
and -1.97%. No correlations were found between the number of repetitions of exercise nor the
rate of perceived effort and DOMS outcomes.
CONCLUSION: Men and women show similar DOMS when NRS and normalized PPT
outcomes are considered. Absolute PPT values may lead to a confusing analysis of fatigue
exercise-induced DOMS if merging both sexes in the sample.
KEYWORDS: Muscle damage | Physical exercise | Pain perception | Pain thresholds
INTRODUCTION
Delayed onset muscle soreness (DOMS) is often experienced after intense physical exercise, an abrupt increase in exercise
load, or performance of exercises involving unusual movement amplitude and speed
1
. DOMS involves a painful sensation associated
with joint and muscle stiffness that appears when muscles are stretched or palpated, muscle swelling, and strength deficits
2,3
. These
symptoms become significant from 6 to 12 h after exercise, with peak values observed between 48 and 72 h after exercise
2
. Despite its
general progression to a condition of full recovery, the time course of DOMS can cause functional limitations and negatively impact
training and rehabilitation protocols.
Methods for assessment of pain intensity are diverse and results can be controversial, which can difficult clinical decisions.
Pressure algometry is a valid method to assess experimental pain. It involves the application of a known magnitude of force at specific
points to stimulate nociceptors and cause a painful sensation, allowing to determine the pressure pain threshold
4
. However, the need for
specialized instrumentation and time required for the assessment of pain thresholds often result in DOMS being assessed by a
unidimensional scale, such as a numeric rate scale (NRS). Using an NRS, the patient is requested to self-report the perceived pain. NRS
results show a strong correlation with results from other tools for pain assessment
5
. Other tools rely on subject report as well as the
Visual Analog Scale (VAS), McGill Pain Questionnaire (MPQ) and Chronic Pain Grade Scale (CPGS)
6
. However, sex differences
7
and
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small variations in the perceived pain are difficult to identify when using unidimensional scales
5,8
.
Additionally, there are physiological differences between sexes related to exercise adaptations and pain. Males are more
susceptible to experiencing exercise-induced muscle damage or fatigue than women
9
. Females can be less fatigable at higher intensity
isometric exercise, they can sustain a long time to task failure, and may have more type I fibers and a higher density of capillaries per unit
of skeletal muscle in the vastus lateralis than males
10
. Additionally, females show a higher prevalence and sensitivity for pain compared
to males
11–13
. Hormonal differences between males and females may also account for differences in pain outcomes, such as the higher
levels of androgen hormones and testosterone in males that appear to be protective against chronic pain
14
. On the other hand, estrogen
hormones have analgesic and hyperalgesia effects in females
15
.
These physiological differences may suggest that pain perception outcomes could differ between males and females
depending on the measure tool, and baseline conditions. However, sex differences regarding exercise-induced pain are considered in a
few studies. It appears that when pain outcomes are compared between sex, even healthy females show lower pressure pain thresholds
considering absolute values
16
and higher perception of pain using a visual analog scale
17
. This could be relevant information to be
considered when comparing sexes, since the absolute values could lead to a misinterpretation on results. For instance, studies are not
clear regarding data normalization considering baseline measures, which would be sound considering sex differences
18
. In this study, we
determine whether there are differences in pain outcomes measured using an NRS and between absolute and normalized values using
pressure algometry in females and males submitted to physical exercise to induce DOMS in the lower limbs. We hypothesized that
females would report higher pain intensity and exhibit lower pressure pain thresholds than males. Also, we suggest that sex-based
differences in pain perception may be influenced by the methods used to normalize pressure pain measurements.
METHODS
Participants and experimental design
This observational study was approved by the local institution's Ethics Committee. Participants were recruited from the local
community through flyers posted in social media and signed a consent term agreeing to participate. Twenty-six participants, 15 females,
and 11 males were included (see Table 1 for participant characteristics). They answered an anamnesis questionnaire to collect
information about their physical activity routine. Leg preference was assessed by the Waterloo questionnaire
19
. Participants were adults
of age between 18 and 40 years old, enrolled with recreational physical exercise, without lower limb injuries at least six months before the
assessment, and not performing plyometric training. Data collection involved two visits to the laboratory. Participants were requested to
refrain from physical exercise 24 h before each visit to the laboratory and not use any medication with anti-inflammatory properties or
techniques for analgesia during the study participation. In the first visit, the pain was measured before and immediately after the exercise
to induce the fatigue and delayed onset muscle soreness considering pain perceived using an NRS, and pressure pain thresholds using
a digital algometer. After 48 h they visited the laboratory again to be evaluated for the presence of DOMS considering pain perceived
using the NRS, and pressure pain thresholds using the digital algometer. Figure 1 illustrates the experimental design.
Figure 1. Experimental design.
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DOMS induction protocol
To induce quadriceps DOMS, participants completed an exercise protocol for fatigue with maximum squat repetitions to
exhaustion with their body weight as workload
20
. A researcher demonstrated how squat movements should be performed in terms of
amplitude and movement speed. From the upright posture, the squat movement should be performed by flexing the knees to 90° and
returning to the upright position again. To ensure that the participants performed a 90º degree knee flexion, an adjustable height bench
was used, and whenever they felt the bench touching their thighs, they should return to the standing position. Participants were instructed
to maintain their feet and knees aligned with the shoulders and avoid a knee valgus movement. They performed the maximal number of
squats, as fast as possible, for repeated 1-min sets. The 1-min sets were repeated with a 15-s interval in between, until exhaustion.
Exhaustion was defined by the participant being no longer able to perform the squat movements or when movement technique
deteriorated, for example, reducing the range of motion. The rate of perceived exertion was reported at the end of the exercise using the
Borg scale of 6-20
21
.
DOMS assessment
DOMS was estimated using a numeric rating scale ranging from 0 (left side, absence of pain) to 10 (right side, most intense
pain) presented to participants in the pre, immediately after (0 h), 24 h, and 48 h post-DOMS induction. For NRS assessment the
participants were seated, at rest, and should consider the pain only in the lower limbs as a result of the exercise.
DOMS was also determined by the pressure pain threshold (PPT) measured in the pre (baseline), immediately after (0 h), and
48 h post-DOMS induction, using a digital algometer (Instrutherm DD-200, Portable Digital Dynamometer) with a resolution of 0.01 N and
a flat tip with an area of 1 cm
2 22
. The PPT assessment was done in two days because of the peak DOMS occurs between 48 and 72
hours after the exercise
2
, and we chose just two days with presential assessment because of the difficulty to bring the participants to the
lab. For bilateral assessment of PPT, patients were in the supine position, with muscles relaxed. The algometer was pressed
perpendicularly to the skin surface over the muscle belly of the rectus femoris (RF) and vastus lateralis (VL). For familiarization with the
assessment, the algometer was first pressed on the anterior region of the deltoid, a non-exercised body region evaluated to reduce
sensitization by systemic factors
23
. The algometer was gradually pressed against the sore region causing discomfort, and the participants
were instructed to notify the evaluator when this discomfort became painful
22,23
. Participants were previously advised on how to report the
moment when the sensation of pressure became uncomfortable pain. The PPT was recorded in N/cm
2
, and the same researcher
performed all assessments. Pre-exercise PPT measurement (baseline) was considered as a reference to normalize the subsequent PPT
measures. Absolute and normalized values (%baseline) were considered.
Statistical analysis
The normality of data distribution was checked by the Shapiro-Wilk test. Levene’s test was used to check the homogeneity.
Nonparametric data are presented as median and interquartile intervals and parametric as mean and standard deviation. Qualitative data
are reported by frequency and percentage among participants. The age, height, body mass index, the number of squat repetitions, and
rate of perceived effort were compared between males and females using the Mann-Whitney U test. Body mass was compared using an
independent t-test. Leg preferences were compared with a Pearson Chi-square test. PPT was compared between the preferred and non-
preferred legs using a paired t-test. As leg differences were not found, the legs average was used for posterior PPT analyses. A
generalized estimating equation (GEE) was used to compare sexes (males vs. females) and time (pre vs. 0 h vs. 48 h) for normalized
and non-normalized values of PPT at vastus lateralis, rectus femoris and deltoid and NRS points. A delta was calculated considering the
difference between baseline and the 48h absolute and normalized measures of PPT, and NRS. Mann-Whitney U test was used to
compare this delta between males and females, except for the Vastus Lateralis normalized PPT compared by independent t-test.
Pearson or Spearman’s correlations were used to verifying the correlations between the rate of perceived exertion, squat repetitions, and
PPT (normalized/non-normalized) and NRS outcomes, considering a pool of data from all participants. All analyzes considered a
significance level of 0.05 and were performed using a commercial statistical package (version 26.0. IBM SPSS Statistics for Windows
Armonk, NY: IBM Corp).
RESULTS
Table 1 summarizes the participants' characteristics and the exercise outcomes. Females showed lower body mass, body
mass index, and height than males.
Numerical rate scale outcomes
NRS values (points, Figure 2) did not differ between females and males at baseline (0.80 ± 0.31 and 0.64 ± 0.34, p = 0.727, for
females and males, respectively), 0 h (4.77 ± 0.52 and 5.27 ± 0.70, p = 0.567) and 48 h post DOMS induction (4.0 ± 0.78 and 3.47 ±
0.84, p = 0.649; Figure 2). The time course of NRS did not differ between females and males, with lower values in baseline compared to
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0 h (0.72 ± 0.23 and 5.02 ± 0.43, p < 0.001, for females and males, respectively) and 48 h post DOMS induction (0.72 ± 0.23 and 3.74 ±
0.57, p < 0.001), without differences between 0 h and 48 h (5.02 ± 0.43 and 3.74 ± 0.57, p = 0.177).
Table 1. Characteristics of the participants of the study and the outcomes of the fatigue protocol and report of leg preference. Results are presented as
median (interquartile interval), mean ± standard. The p-values are for the between-sex comparisons.
BMI: body mass index; RPE: rate of perceived exertion.
Figure 2. Numeric rate scale (NRS) outcomes for men and women before DOMS induction (Baseline), immediately after DOMS induction (0 h), and 48 h
post DOMS induction (48 h).
Absolute pressure pain thresholds
Females presented lower magnitudes of absolute (N/cm
2
) PPT than males at all times of measure (Figure 3b and 3d). The
lower absolute PPT in females were found for the vastus lateralis at baseline (23.45 ± 2.20 and 36.13 ± 3.37, p = 0.002, for females and
males, respectively), 0 h (26.98 ± 2.47 and 43.44 ± 4.59, p = 0.002) and 48 h post DOMS induction (19.44 ± 1.99 and 31.66 ± 2.71, p <
0.0001). Similar differences were found for the rectus femoris, with lower absolute PPT in females than males in the baseline (28.94 ±
2.63 and 40.23 ± 3.44, p = 0.009, for females and males, respectively), 0 h (32.20 ± 2.98 and 47.47 ± 3.38, p = 0.001) and 48 h post
(25.22 ± 1.88 and 38.58 ± 2.94, p < 0.0001).
The time course for changes in absolute PPT (N/cm
2
) for the vastus lateralis (Figure 3b) revealed a lower baseline threshold
compared to 0 h (29.79 ± 2.01 and 35.21 ± 2.60, p < 0.001) and a higher threshold compared to 48 h (29.79 ± 2.01 and 25.55 ± 1.68, p
< 0.0001). Absolute PPT on 0 h was higher than 48 h post (35.21 ± 2.60 and 25.55 ± 1.68, p < 0.0001). Rectus femoris absolute PPT
Total (N=26)
Men (n=11)
Women (n=15)
p-value
Age (years)
26 (22-29)
24 (22-27)
27 (22-29)
0.443
Body mass (kg)
66.3 ± 12.5
73.2 ± 70-80
60 ± 55-62
<0.01
Height (cm)
169.2
(160-172)
172
(170.5-180)
160
(157-165.5)
<0.001
BMI (kg/m
2
)
22.9
(21.7-25.0)
23.39
(22.9-26.3)
22.36
(12.3-23.5)
0.047
Squat repetitions
238
(168-337)
243
(168-307)
233
(174.5-361.5)
0.959
RPE (points)
17 (15-17)
17 (16-17.5)
15 (15-17)
0.281
Leg preference
Right n (%)
Left n (%)
Both n (%)
18 (69.2)
2 (7.7)
6 (23.1)
5 (45.4)
2 (18.9)
4 (36.4)
13 (86.7)
0 (0)
2 (13.4)
0.057
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(Figure 3d) was lower at baseline compared to 0 h (34.59 ± 2.16 and 39.84 ± 2.25, p < 0.001) and higher in 0 h than 48 h (39.84 ± 2.16
and 31.90 ± 1.74, p < 0.001). No differences were found in absolute rectus femoris PPT between baseline and 48 h (34.59 ± 2.16 and
31.90 ± 1.74, p = 0.072). A similar time course was found for each sex, except rectus femoris for females that showed higher values of
baseline compared to 48 h post (28.94 ± 2.63 and 25.22 ± 1.88 p =0.039).
Normalized pressure pain thresholds
Normalized PPT (%baseline, Figure 3b and 3d) showed differences between time, without differences between sexes. For
vastus lateralis normalized PPT (Figure 3b) no differences were found between females and males on 0 h (116.52 ± 5.84 and 119.70 ±
4.56, p = 0.668, for females and males, respectively) and 48 h (84.35 ± 6.06 and 89.10 ± 4.44 p = 0.528). The normalized PPT for vastus
lateralis at baseline (100%) was lower when compared to 0 h (118.11 ± 3.71 p < 0.001, respectively) and higher than 48 h (86.72 ± 3.76,
p = 0.001). Normalized PPT on 0 h was higher than 48 h post DOMS induction (118.11 ± 3.71 and 86.72 ± 3.76, p < 0.0001). Rectus
femoris normalized PPT (% baseline, Figure 3d) did not differ between females and males on 0 h (112.18 ± 4.86 and 120.70 ± 5.21, p =
0.232, females and males, respectively) and 48 h after DOMS induction (90.81 ± 4.86 and 98.02 ± 5.25, p = 0.314). The normalized
rectus femoris PPT was lower in the baseline compared to 0 h (116.44 ± 3.56, p < 0.001), and higher than in 48 h (116.44 ± 3.56 and
94.42 ± 3.58, p < 0.001, for females and males, respectively). Regarding the delta of NRS and PPT, both normalized/non-normalized,
there were no differences between males and females (Table 2).
Figure 3. Results for men and women before DOMS induction (Baseline), immediately after DOMS induction (0 h) and 48 h after DOMS induction (48
h). Left column shows results with values normalized by baseline and right column shows absolute values. A-B PPT vastus lateralis; C-D PPT rectus
femoris. # Represents the significant difference between times; * represents a significant difference between the sexes. Significant difference p< 0.05.
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Table 2. Sex comparison of deltas for NRS and absolute and normalized (%) PPT in Vastus Lateralis (VL) and Rectus Femoris (RF). Data are
presented as median (interquartile interval) and mean ± standard deviation. PPT VL: Pressure pain threshold of Vastus lateralis; PPT RF: Pressure
pain threshold of Rectus femoris; NRS: Numeric Rate Scale.
Correlation outcomes
The number of squat repetitions and RPE scores in the exercise protocol to induce fatigue and DOMS did not differ between
females and males. Furthermore, these exercise characteristics did not show significant correlations with DOMS outcomes. We found no
significant relationship between number of squat repetitions and: NRS on 48 h (r = -0.173 , p = 0.420), absolute PPT on 48 h (r = 0.012,
p = 0.953, and r = -0.073 , p = 0.725, for vastus lateralis and rectus femoris, respectively), and normalized PPT on 48 h (r = 0.120, p =
0.558, and r = -0.021, p = 0.917, for vastus lateralis and rectus femoris, respectively). No significant correlation was found between
RPE and NRS on 48 h (r = -0.103, p = 0.632) and absolute PPT on 48h (r = 0.025, p = 0.716, and r = - 0.119, p = 0.564, for vastus
lateralis and rectus femoris, respectively). No significant correlation was found between RPE and normalized PPT on 48 h (r = 0.092, p =
0.654, and r = 0.144, p = 0.484 for vastus lateralis and rectus femoris, respectively).
DISCUSSION
DOMS assessment is part of the daily routine in contexts of sports performance and rehabilitation, but the different methods
available for DOMS assessment may influence outcomes. Here we compared two different methods commonly used in clinical practice
for assessing pain in a condition of exercise-induced DOMS in males and females. Our main findings show that numerical rate scale
outcomes are comparable between females and males, but absolute values of pressure pain threshold are lower in females than males
despite of DOMS. To compare PPT considering patient sex, a normalization of the PPT value considering the baseline measure could be
recommended, which result in no difference between sex. We consider these results relevant to guide the clinical evaluation and patient
management, especially regarding the importance of a proper baseline measure.
All participants performed the same fatigue protocol for inducing DOMS and achieved a similar number of repetitions and
similar RPE. Although physical exercise may have different acute and chronic physiological effects in males and females
18
, the volume of
work performed, estimated by the number of repetitions performed, did not differ between the males and females participants. These
exercise characteristics did not correlate with DOMS outcomes. Therefore, we argue that the sex difference in DOMS measured by PPT
is the result of sensitivity for the pressure pain threshold in females rather than the exercise configuration. Furthermore, the lack of
difference in the delta of changes in DOMS outcomes between males and females further supports this assumption and reinforces the
need for proper normalization of PPT values considering a baseline measure.
The time course of changes in DOMS was similar for the males and females included in our study. DOMS is known to reach
peak values between 48 and 72 h after its induction
2
. In our study, the acute effect of the squat-to-exhaustion protocol reduced the
pressure pain threshold 48 h after exercise, but the magnitude of the DOMS considering PPT requires normalization for a proper
comparison. When sex comparison is discussed, one could always argue about the influence of the menstrual cycle. Indeed, hormonal
fluctuations during the menstrual cycle, as well as estrogen levels, can affect exercise-induced muscle damage causing DOMS and
reducing muscle strength
24
so we suggest caution when considering these results.
As we tried to mimetize a clinical condition in which the phase of the menstrual cycle for a patient can not be controlled, the
influences of this variable on DOMS outcomes may require an experiment aimed specifically at this research question. Despite this, the
baseline measures indicated sex differences in pain thresholds, which reinforces that sex differences might be present regardless of the
exercise and therefore there is a need to normalize PPT values, especially when aiming to compare both sexes. Finally, the
normalization also makes PPT outcomes similar those observed with NRS, suggesting that if the aim of the study is just control
magnitude of pain maybe there is no need to add more than NRS.
Men (n=11)
Women (n=15)
p-value
ΔPPT VL (N/cm
2
)
3.14
(1.71-9.89)
3.83
(1.87-9.19)
0.959
ΔPPT VL (%)
-10.89 ± 15.47
-15.64 ± 24.32
0.576
ΔPPT RF (N/cm
2
)
2.14
(0.50-9.96)
4.59
(3.50-7.78)
0.237
ΔPPT VL (%)
-0.30
([-22.13] – 9.25)
-18.17
([-11.35] – 1.34)
0.384
ΔNRS (points)
2.0
(0.5-4.0)
4.0
(0.5-6.0)
0.507
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Our study has some limitations. The limited sample size without randomization is assumed, although we understand that our
results present interesting directions for the guidance of the DOMS assessment. The presence of muscle damage due to fatigue protocol
is securely based in the DOMS outcomes, but we lack in measuring the baseline muscle damage condition in the participants.
CONCLUSION
Numerical rate scale and normalized pressure pain threshold outcomes are comparable between females and males subjected
to a fatigue protocol of exercise to induce delayed onset muscle soreness. Absolute values of pressure pain thresholds show higher pain
sensitivity in females regardless of exercise. Baseline measures can be used to normalize pain outcomes and allow sex comparisons in
the time course of DOMS.
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BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
Lemos, Santos,
Carpes
2023
VOL.17
N.5
215 of 215
Special issue:
“Fatigue issue in the performance of motor skills”
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Citation: Lemos AL, Santos MA, Carpes FP. (2023).!Sex differences in delayed onset muscle soreness induced by fatigue and measured by different methods. Brazilian
Journal of Motor Behavior, 17(5):208-215.
Editor-in-chief: Dr Fabio Augusto Barbieri - São Paulo State University (UNESP), Bauru, SP, Brazil. !
Associate editors: Dr José Angelo Barela - São Paulo State University (UNESP), Rio Claro, SP, Brazil; Dr Natalia Madalena Rinaldi - Federal University of Espírito Santo
(UFES), Vitória, ES, Brazil; Dr Renato de Moraes – University of São Paulo (USP), Ribeirão Preto, SP, Brazil.
Guest editors: Dr Bruno Bedo – University of São Paulo (USP), São Paulo, SP, Brazil; Dr Carlos Augusto Kalva-Filho - São Paulo State University (UNESP), Bauru, SP,
Brazil. !
Copyright:© 2023 Lemos, Santos and Carpes and BJMB. This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-
No Derivatives 4.0 International License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The Brazilian National Council for Scientific and Technological Development (CNPq – Brazil) supports FPC. This study was financed in part by the Coordenac!ão
de Aperfeic!oamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 awarded to ALL and MAS.
Competing interests: The authors have declared that no competing interests exist.
DOI:!https://doi.org/10.20338/bjmb.v17i5.389