The Effect of Muscle Strength on Marathon Race-Induced Muscle Soreness

d: Muscle soreness after a competition or a training session has been a concern of runners due to its harmful effect on performance. It is not known if stronger individuals present a lower level of muscle soreness after a strenuous physical effort. The aim of this study was to investigate whether the pre-race

*Correspondence: beat.knechtle@hispeed.ch; Tel.: +41-(0)-71-226-93-00; Fax: +41-(0)-71-226-93-01 Abstract: Background: Muscle soreness after a competition or a training session has been a concern of runners due to its harmful effect on performance. It is not known if stronger individuals present a lower level of muscle soreness after a strenuous physical effort. The aim of this study was to investigate whether the pre-race muscle strength or the . VO2max level can predict muscle soreness 24, 48 and 72 h after a full marathon in men. Methods: Thirty-one marathon runners participated in this study (age, 40.8 8.8 years old; weight, 74.3 10.4 kg; height, 174.2 7.6 cm; maximum oxygen uptake, . VO2max , 57.7 6.8 mL/kg/min). The isokinetic strength test for thigh muscles and the . VO2max level was performed 15–30 days before the marathon and the participants were evaluated for the subjective feeling of soreness before, 24, 48 and 72 h after the marathon. Results: The participants presented more pain 24 h after the race (median = 3, IQR = 1) than before it (median = 0, IQR = 0) (p< 0.001), and the strength values for the knee extensor muscles were signi cantly associated with muscle soreness assessed 24 h after the race (p= 0.028), but not 48 (p= 0.990) or 72 h (p= 0.416) after the race. The . VO2max level was not associated with the muscle pain level at any moment after the marathon. Conclusions: Marathon runners who presented higher muscular strength for the knee extensor muscles presented lower muscle soreness 24 h after the race, but not after 48 h or 72 h after the race. Therefore, the muscle soreness level 3 days after a marathon race does not depend on muscle strength. Keywords:DOMS; endurance; isokinetic strength; pain; peak toque; runners 1. Introduction Marathon races are among the most popular mass sporting events worldwide, with over 2.1 million participants around the world annually [1]. The 42,195 m of a marathon race represent an impressive effort imposed onto the human body, and it is well-documented that unusual or exhaustive exercise, whether mechanical or metabolic in nature, can cause exercise-induced muscle

toque; runners 1. Introduction Marathon races are among the most popular mass sporting events worldwide, with over 2.1 million participants around the world annually [1]. The 42,195 m of a marathon race represent an impressive effort imposed onto the human body, and it is well-documented that unusual or exhaustive exercise, whether mechanical or metabolic in nature, can cause exercise-induced muscle damage [2,3]. Indeed, muscle soreness is frequently reported by athletes after a marathon race [2–4]. Moreover, loss of muscle strength, muscle length and range of motion have also been reported after exhaustive exercises [3,5]. These transi- tory conditions can negatively affect the running economy [6], increase the blood lactate Int. J. Environ. Res. Public Health2021,18, 11258.

Int. J. Environ. Res. Public Health2021,18, 11258 2 of 8 concentration [7], and reduce the maximum oxygen uptake ( . VO2max ) [8,9]. Considering that there is a consensus that the performance in long-distance events depends on the physiological factors cited above (running economy, . VO2max and the sustained percent- age of . VO2max ) [10], it is reasonable to assume that the presence of muscle soreness can compromise athletic performance in training sessions in addition to delaying the return to training after a marathon race. Despite the fact that complete pathophysiology of muscle soreness after exhaustive ex- ercise is not completely understood, several possible mechanisms have been proposed [11]. The most accepted hypothesis is that the pain results from muscle microinjuries caused by eccentric movement [12]. After that, there are lysis in the sarcolemma and release of cytolytic enzymes and myoglobins, causing in ammation, edemas and production of free radicals [12,13]. This in ammation is characterized as an enzymatic reaction with in am- matory mediation, with elements such as thromboxanes, prostaglandins and leukotrienes coming from cyclooxygenases and lipoxygenases that cause increased vascular permeabil- ity and sensitization of nerve bers, mainly of types III and IV [14]. Many strategies have been studied to treat or even prevent muscle soreness [14–21]; however, it is unknown if muscular strength or . VO2max values are associated with muscle soreness after exercise. This knowledge could be useful for athletes and coaches in creating strategies that allow the runner to return to normal training as quickly as possible, without prejudice to the performance caused by pain [22]. Therefore, the aim of this study was to investigate whether pre-race muscle strength and . VO2max can predict muscle soreness 24, 48 and 72 h after a full marathon in men. We hypothesized that the stronger athletes would present with less muscle soreness in the days following a marathon race, and we also hypothesized that . VO2max would present no association with muscle soreness following a marathon race. 2. Materials and Methods 2.1. Participants Thirty- ve male amateur runners who applied for the 2017 S¢o Paulo Marathon (Brazil)

marathon in men. We hypothesized that the stronger athletes would present with less muscle soreness in the days following a marathon race, and we also hypothesized that . VO2max would present no association with muscle soreness following a marathon race. 2. Materials and Methods 2.1. Participants Thirty- ve male amateur runners who applied for the 2017 S¢o Paulo Marathon (Brazil) participated in the study. The invitation was made by the race administration. The inclusion criteria to participate in the study were to be enrolled in the 2017 S¢o Paulo Marathon with at least two years of running practice. The exclusion criteria included having acute pain in the lower limbs, edemas, taking medicines which affect the musculoskeletal system or not nishing the race. Of the 35 athletes who replied to the initial invitation, four athletes did not nish the race and were excluded from the study. Therefore, thirty-one athletes participated in the entire study. The athletes were 40.8 8.8 years old, weighted 74.3 10.4 kg and were174.2 7.6 cm tall, had 8.2 8.0 years of running experience and the distance covered per week was 48.7 24.6 km . The subjects were informed of the bene ts and risks of the investigation prior to signing an institutionally approved informed consent document to participate in the study. All the experimental procedures met the ethical standards of sports and exercise science research [23] and were approved by the Human Research Ethics Committee of the University Cruzeiro do Sul and the National Research Ethics Committee (CONEP) under number CAAE: 67318317.3.0000.8084 on 17 April 2017. The study conformed to the principles outlined in the Declaration of Helsinki [24]. 2.2. Procedures Each participant reported to the laboratory two days in the same week, with an interval of 2 or 3 days to prevent the results of one test from being in uenced by the results of the other [25,26]. Moreover, the athletes were instructed to avoid training within 24 h before each visit to the laboratory. On the rst visit, they answered a questionnaire about training habits; afterwards, anthropometric data measurements and the cardiorespiratory maximum text were

2 or 3 days to prevent the results of one test from being in uenced by the results of the other [25,26]. Moreover, the athletes were instructed to avoid training within 24 h before each visit to the laboratory. On the rst visit, they answered a questionnaire about training habits; afterwards, anthropometric data measurements and the cardiorespiratory maximum text were per-

Int. J. Environ. Res. Public Health2021,18, 11258 3 of 8 formed. On the second visit, the isokinetic strength test was performed. The two visits were performed 15–30 days before the marathon. The race times were provided by the organizing committee of the race. Before the marathon and 24, 48 and 72 h after the marathon, the athletes were asked about the subjective feeling of soreness. To avoid the invasive nature of muscle biopsies and plasma creatine kinase activity to assess muscle damage, muscle soreness was assessed using a pain scale. Pain Likert scales were also used in previous studies to assess the perceived soreness [5,27]. 2.3. Questionnaire about Training Habits The athletes answered a questionnaire about training habits with the following two open-ended questions: (1) How many years have you been practicing running?; (2) How many kilometers do you run a week? 2.4. Isokinetic Strength Test All the participants underwent a knee extensor muscles isokinetic evaluation for the dominant lower limb. Isokinetic strength tests were performed on a Biodex System 3 isoki- netic dynamometer (Biodex Medical System, Shirley, New York, NY, USA). A calibration procedure was performed prior to each test. The dominant lower limb was determined by asking the participant which limb they prefer to use to kick a ball. This procedure was used in previous studies [28,29]. Before the strength test, the participants warmed up for ve minutes on a cycle ergometer (Cybex Inc., Ronkonkoma, NY, USA). This cycle ergometer was set at a resistance of 25 Watts [29]. The warm-up was followed by low-intensity dynamic stretching exercises for the lower limbs [30]. Then, the participants were asked to sit with their hips exed at approximately 85 . Initially, the participants underwent three trials at submaximum effort with a gradually increasing load and then performed one set of ve repetitions at the maximum concentric contraction at angular speeds of 60 /s in the concentric mode. A coef cient of variance lower than 10% was considered valid for analysis. Standardized verbal encouragement was given to the participants during the entire test, always by the same experienced examiner. The peak

a gradually increasing load and then performed one set of ve repetitions at the maximum concentric contraction at angular speeds of 60 /s in the concentric mode. A coef cient of variance lower than 10% was considered valid for analysis. Standardized verbal encouragement was given to the participants during the entire test, always by the same experienced examiner. The peak torque in newton-meters (Nm) was assessed at 60 /s for the knee extensor muscles at concentric action and recorded for further analysis. 2.5. Cardiorespiratory Maximum Test on a Treadmill Cardiopulmonary exercise testing (CPET) was conducted on a motorized treadmill (Inbrasport, ATL, Porto Alegre, Brazil) using a computer-based metabolic analyzer (Quark, Cosmed, Italy). The calibration procedure was performed prior to each test. CPET was used to measure . VO2max . . VO2max was determined as stabilization of . VO2 (increase lower than 2.1 mL/min/kg) even after increasing the treadmill velocity during the last stage of the CPET [31]. All the participants reached the . VO2maxvalues. The test protocol consisted of a warm-up phase of 3 min at 9 km/h. After the warm- up period, the running velocity was increased by 1 km/h every minute until voluntary exhaustion [32]. The entire CPET lasted for 8–12 min and the treadmill grade was set at 1% to simulate the energy cost of outdoor running [33]. 2.6. Perceived Soreness Muscle soreness was assessed using a seven-point Likert scale (Table) for muscle pain individually immediately before and remotely (using Google Forms) 24, 48 and 72 h after the race. A study collaborator would call the participant to remind him to answer the questionnaire after the race.

Int. J. Environ. Res. Public Health2021,18, 11258 4 of 8 Table 1.Muscle pain assessment scale used in the study. Value Description 0 Painless 1 Mild pain when touching/vague pain 2 Moderate pain when touching/small persistent pain 3 Mild pain when walking up or up the stairs 4 Mild pain when walking on a at surface/sore 5 Moderate pain, stiffness or weakness when walking on a at surface/very sore 6 Severe pain that makes movement dif cult 2.7. Statistical Analysis The strength, . VO2max and race time values presented normal distribution and ho- mogeneous variance according to the Shapiro–Wilk and Levene's tests, respectively. An ordinal logistic regression model was tted to describe and explain the relationship be- tween the peak knee extensor torque value at 60 /s and . VO2max with the pain scale 24, 48 and 72 h after the race. The Akaike information criterion (AIC) identi es the model quality, but its meaningfulness depends on there being a good predictive model [34]. Statistical analysis was performed using SPSS v21.0 (Chicago, IL, USA) [35]. The signi cance level was set atp< 5%. The data are presented as the means standard deviation for the following data: . VO2max , race time, and the peak torque values, as well as the median and the interquartile range for pain values. 3. Results . VO2max and the total marathon race time in the group were 57.7 6.8 mL/min/kg and 4:09:36 0:42:36 (data presented as h:mm:ss), respectively. Before the race, the median and the interquartile range for the pain level reported by the participants (0(0)) were signi cantly lower than the values reported 24 h after the race (3(1)) (p< 0.001). The pain level reported 48 h after the race (2(2)) was signi cantly lower than 24 h after the race (p< 0.001). Similarly, the pain level reported 72 h after the race (1(1)) was also lower than 48 and 24 h after the race (p< 0.001); therefore, the peak of pain was reached 24 h after the race for the entire group (Figure).Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW

than 24 h after the race (p< 0.001). Similarly, the pain level reported 72 h after the race (1(1)) was also lower than 48 and 24 h after the race (p< 0.001); therefore, the peak of pain was reached 24 h after the race for the entire group (Figure).Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW 5 of 9 Figure 1. Boxplot for pain intensity before the race and 24, 48 and 72 h after the race (* p < 0.05—lower pain level than 24 h after the race). The level of association between the knee extensor strength and í µí±‰ 6í µí±‚ 6í µí±ší µí±Ží µí±¥ with the pain level reported 24, 48 and 72 h after the marathon race were also studied. The pain level 24 h after the marathon presented a significant association with the knee extensor muscles strength (x 2 (1) = 4.821, p = 0.028, ß = −0.023), with a reduction of 0.023 points on the pain scale (IC = −0.004/−0.002) per unit of increment in the peak extensor muscles torque at 60°/s. Conversely, there was no association with the í µí±‰ 6í µí±‚ 6í µí±ší µí±Ží µí±¥ level (x 2 (1) = 0.242, p = 0.623, ß = −0.025). For this model, the AIC was 96.780. On the other hand, the pain level 48 h after the marathon presented no association with the knee extensor muscles strength (x 2 (1) = 1.128, p = 0.288, ß = −0.010) and í µí±‰ 6í µí±‚ 6í µí±ší µí±Ží µí±¥ (x 2 (1) = 0.003, p = 0.958, ß = 0.003), and the AIC was 97.768. Similarly, the pain level 72 h after the marathon also presented no association with the knee extensor muscles strength (x 2 (1) = 0.662, p = 0.416, ß = −0.008) and í µí±‰ 6í µí±‚ 6í µí±ší µí±Ží µí±¥ (x 2 (1) = 0.013, p = 0.905, ß = −0.006), and the AIC was 98.096. 4. Discussion This study intended to investigate whether the pre-race muscle strength can predict muscle soreness 24, 48 and 72 h after

muscles strength (x 2 (1) = 0.662, p = 0.416, ß = −0.008) and í µí±‰ 6í µí±‚ 6í µí±ší µí±Ží µí±¥ (x 2 (1) = 0.013, p = 0.905, ß = −0.006), and the AIC was 98.096. 4. Discussion This study intended to investigate whether the pre-race muscle strength can predict muscle soreness 24, 48 and 72 h after a full marathon in men. The main findings of the study are that the knee extensor muscles strength was significantly associated with muscle soreness 24 h after the marathon race (the more muscle strength, the less muscle soreness), but this association was not present 48 and 72 h after the race. These findings confirm the initial hypothesis that the stronger athletes would present with less pain for at least 24 h after the race. The knowledge that muscle strength is associated with muscle soreness 24 h after the race indicates that stronger individuals recover faster from pain after the race, but does not indicate that they would be able to return to training faster. Previous research showed many mitochondria, erythrocytes, leukocytes and other phagocytic cells within the extracellular and extravascular spaces besides dilation and disruption of the T-tubule system after a marathon race, evidencing a process of muscle fiber necrosis and inflamma- tion, which are most prevalent at 1 and 3 days after a marathon [36,37]. Nonetheless even after this period and after muscle soreness has subsided, there is some level of cellular dam- age in muscles as late as 8 weeks after a race [36,38]. Considering this muscle recovery time after a marathon, it is understood that the return to sports practicing after the race should not be immediate; however, the research regarding the return to running following a mara- thon is scarce and there is no consensus about whether rest is indicated [37]. Sherman et al. (1984) compared two groups of marathoners for 6 days following a race [39]. One group Figure 1. Boxplot for pain intensity before the race and 24, 48 and 72 h after the race (*p< 0.05—lower pain level than 24 h after the

mara- thon is scarce and there is no consensus about whether rest is indicated [37]. Sherman et al. (1984) compared two groups of marathoners for 6 days following a race [39]. One group Figure 1. Boxplot for pain intensity before the race and 24, 48 and 72 h after the race (*p< 0.05—lower pain level than 24 h after the race).

This study investigates the relationship between muscle strength and soreness in marathon runners.