Internal mechanical work and maximum subtalar joint pronation in different gradients

Introduction: Some authors have described the importance of physiological intensity in the behavior of the biomechanical aspects of running (for example, subtalar pronation), but the complex relationships between these variables are not yet well understood. Objective: This study investigated the influence of positive gradients on internal mechanical work (Wint) and maximum subtalar pronation at a submaximal * KAL: undergrad, e-mail: karinalopes93@hotmail.com MMB: Master’s student, e-mail: mayamb2@hotmail.com LM: undergrad, e-mail: leticia_marttins@hotmail.com ALK: undergrad, e-mail: andrekiihn@gmail.com MRQ: PhD, e-mail: queirogamr@hotmail.com MPT: PhD, e-mail: mtartaruga@unicentro.br


Introduction
In recent decades, the study of the human gait has gained importance in sport and rehabilitation research centers [1].Numerous studies investigated the relationship between physical activity and injuries, particularly those related to running [2,3].Researches associating the behavior of the subtalar joint angle, specifically subtalar pronation, with the footwear used for running have significantly contributed to the comprehension of injuries involving the hip, knee, ankle and foot [4].
Subtalar pronation consists of an impactabsorbing mechanism, which acts combined with other body mechanisms to decrease the tension in some articular structures with an adequate level of impact and without provoking microtraumas.However, pronation becomes pathological when it exceeds its physiological articular range of motion, that is, when the maximum subtalar pronation exceeds approximately 12º.This state is known as hyperpronation [5].Maximum subtalar pronation is generally reached between 20% and 40% of the stance phase, and is mainly influenced by the linear speed of running, intensity of effort, muscle imbalance and/ or ligament laxity, and the running technique used by the runner [6].Maximum subtalar pronation during running contributes to running-related injuries.However, complex relationships between joint motion and running technique are not well understood [7].
Margaria [8], in the first study reporting the metabolic optimum walking gradient, found the energetic cost of running is minimized at a gradient of approximately -10% (Margaria et al. [9]).Margaria's technique for calculating the efficiency of locomotion linked the metabolic energy consumption to the estimated mechanical work and the running technique.Davies et al. [10] used similar methods.The authors measured the energetics of human running and estimated the mechanical work by considering only the work done to lift and lower the body's center of mass.
Traditionally, the human locomotion mechanics have been analyzed according to the mechanical work performed [11].The total locomotion mechanical work (W tot ) is conventionally considered the sum of the two separate aspects of mechanical work: external mechanical work (W ext ) and internal mechanical work (W int ) [12].W int represents the work required to accelerate the limbs reciprocally with the body's center of mass during human locomotion.It is computed using both segment movements and anthropometric parameters [13].In contrast, W ext represents the work required to lift and accelerate the body's center of mass within the environment.W ext has been investigated in various conditions, such as force platform and kinematic analysis, and across many different populations [12].For example, Buczek and Cavanagh [14] used a force platform installed along a 17 m downhill walkway to measure the power of the knee and ankle joints at a gradient of approximately -8%.However, Iversen and McMahon [15] first developed a model capable of predicting the pattern of motion of gradient running and demonstrated a probable relationship between these two variables.
The literature reveals two key mathematical models to determine the maximum subtalar pronation.The first model uses two reference points, both located in the subject's shoe: marker 1 (M1), located on the lower edge of the shoe above the sole, and marker 2 (M2), located at the center of the upper edge of the shoe, above the Achilles tendon.In this model, the maximum subtalar pronation can be determined by the maximum angle formed between the segment M1-M2 (S1) and the vertical axis y, or between the S1 and the axis parallel to the shoe sole (Ferrandis et al. [16]).The second model uses four reference points: markers M1 and M2 (as in the previous model), marker 3 (M3), located at the origin of the Achilles tendon (calcaneal tendon), and marker 4 (M4), located at the origin of the Gastrocnemius muscle.In this model, the maximum subtalar pronation is determined by the maximum angle formed between the segments S1 and S2 (M3-M4) (see Wit et al. [17]).
Although some studies have examined the influence of positive gradients on mechanical work and maximum subtalar pronation, a literature review has revealed that little research has investigated the effect of effort intensity on these dependent variables.This study intends to address this gap by investigating the influence of positive gradients on W int and maximum subtalar pronation at a submaximal running speed.

Methods
Subjects.Sixteen male, trained long-distance runners (age: 29 ± 7 yr; stature: 1.72 ± 0.07 m; body mass: 72.1 ± 10.6 kg), were recruited.The sample size was calculated according to a previous study by Williams and Cavanagh [18] investigating the relationship between distance running mechanics, running economy (RE) and performance.The sample size had a statistical power of 80% and significance of p ≤ 0.05.The mean maximal oxygen uptake of the subjects (VO 2max ) was 50.6 ± 4.9 mL .kg -1.min -1 .The subjects had a mean of 3.4 ± 1.4 yr of running practice, and their usual racing distance ranged from 10 km to 45 km.The experimental group typically ran 3-5 d .wk -1 with a mean weekly running distance of 40 ± 10 km .wk -1 during the month preceding the investigation.The subjects provided their informed consent to participate in the study.The study was conducted according to the Declaration of Helsinki.A local ethics committee for protection of individuals approved the project before its commencement (CAAE: 70903716.1.0000.0106).
Experimental design.Subjects underwent two laboratory sessions: (1) sample characterization; and (2) four submaximal treadmill tests (RE).Due to the influence of the environment on physiological processes that contribute to the regulation of metabolic rate and neuromuscular responses, the laboratory ambient temperature (± 25°C) and relative humidity (± 55%) were controlled according to ISO-8573-1 (international standards).Some restrictions were imposed on the subjects: (a) no food and drink at least 3 to 4 hrs before the tests; (b) no stimulants or intense physical activity 12 hrs before the evaluation; and (c) use of their own training shoes (with rubber soles and no cleats).Sports shoes and anti-pronation shoes were not allowed.
Session 1: Sample Characterization.Anthropometric parameters were recorded using scales and stadiometer (WELMY-110, Santa Bárbara d'Oeste, SP, Brazil) and a skinfold caliper (LANGE SKINFOLD CALIPER-C130, Porto Alegre, RS, Brazil).The body fat percentage was calculated using the Siri equation [19].Body density was calculated using the Jackson and Pollock method [20].A professional with experience in anthropometric evaluations performed all measurements.After the anthropometric measurements were taken, each subject performed a maximal test on a motorized treadmill (Movement-RT350, Pompeia, Brazil) to determine VO 2max , proposed by Ellestad et al. [21].
Session 2: Running Economy Tests.Initially, four reflective points were affixed to each leg.Two contrasting markers were placed on the midline of the heel counter of the shoe and two on the lower leg midline.See Figure 1 (cited by Wit et al. [17]).After the preparation phase, the treadmill was turned on, and the subjects completed a three-minute warm-up consisting of walking at a comfortable speed.Then, subjects increased the speed to their optimal running speed, corresponding to the intensity of lower energy expenditure and better performance in long-distance running.This was maintained for four minutes on the gradients used in this study (+1%, +5%, +10% and +15%), with a five-minute rest period between conditions.To quantify the maximum values of subtalar pronation, each running test was filmed at the posterior frontal plane at a sampling frequency of 240 Hz using a highspeed camera (Casio Exilim EX-FH25, Japan).The camera was mounted on a tripod, placed 2 m from the treadmill, and aligned so that the plane of the camera was parallel to the treadmill.Three consecutive steps were averaged during the last 15 seconds of each RE test.The kinematic records were scanned manually and automatically using DVIDEO software (UNICAMP, Campinas, SP, Brazil).Then these records were used to determine the W int and maximum values of subtalar mathematical models discussed by Tartaruga et al.
[2], using a fifth-order Band-Pass Butterworth filter with a cut-off frequency of 5 Hz; see Figure 2. pronation using two routines developed using the MATLAB software (R2017a, MathWork, Natick/ Massachusetts, United States) according to the two Maximum subtalar pronation and W int .The predicted W int was expressed as J/kg of body mass per unit distance travelled (m) and was associated with gait pattern modifications using the following formula [22]: ⋅q (1)   in which SF is the stride frequency (Hz), s is the average progression velocity (m/s), DF is the duty factor, and q is a compound dimensionless term accounting for the inertial properties of the limbs and the mass partitioned between the limbs and the rest of the body (= 0.10 at gradient gaits) [23].
Statistical analysis.Data are expressed as mean ± SD.The data normality was verified using the Shapiro-Wilk test.As the results showed symmetrical behaviors, the Student's T-test was applied to dependent samples to compare the mean values of the W int and the maximum subtalar pronation of both feet and in both mathematical conditions.One-way repeated-measures ANOVA was applied to compare the maximum values of subtalar pronation for each one of the gradients adopted.Significance at p ≤ 0.05 was adopted for all statistical tests, and the statistical package used was the Statistical Package for the Social Sciences (SPSS) version 20.0.

Results
Analysis of the maximum values of subtalar pronation of both feet found no significant differences between the values of each foot regardless of the mathematical method used.Similar results were reported by Wit et al. [17] and Tartaruga et al. [6].Consequently, the behavior of the right leg (dominant) of each subject was chosen for analysis.The mean mass of the shoe used in the sample was 210.2 grams, with a standard deviation of ± 86.1 grams.
Significant differences were found between W int values of each gradient.However, no significant differences were observed in the maximum values of subtalar pronation between gradients in both mathematical method adopted, see Table 1.

Discussion
This study investigated the influence of positive gradients on internal mechanical work and maximum subtalar pronation at a submaximal running speed.The findings show W int is impacted by gradient, but gradient does not influence the behavior of the subtalar joint during submaximal running irrespective of the mathematical model adopted.These results corroborate the studies by Minetti et al. [24] and Oliveira et al. [7].
According to Minetti et al. [24], W int is an important component of the total mechanical work of running.In this study, W int remained nearly constant at all downhill gradients, but increased at positive gradients.These changes in W int parallel the changes recorded in the stride frequency.The lack of change in W int at negative gradients suggests W int has little influence on the optimal gradient.In addition, W int is, by definition, formed from equal positive and negative components at all gradients [25].The reduced dependence of W int on speed during running compared with walking [26] is due to the flight time, which allows limbs to move more slowly in the swing phase in running during a progression run.In our study, the W int increased at positive gradients at a submaximal running speed.These findings corroborate those of Minetti et al. [24].The sum of W int and W ext [11,12] is the total mechanical work (W tot , in J .kg .-1m -1 ), and energy expenditure is reported at between 40% and 70% [27], with intraindividual variation between 3% and 11% [28].
However, no significant differences in the maximum values of subtalar pronation between gradients were observed despite the different values recorded according to the mathematical model used.These differences may be related to the movement at the segment S2, which is influenced by the rotation movements along the longitudinal axis and the translation movements of the tibia [2], in its turn influenced by internal tibial rotation as reflected in the second mathematical model, which uses four reference points (Wit et al. [17]).According to McClay and Manal [29], the internal rotation of the tibia is one of the main causes of subtalar pronation and contributes significantly to its absolute value.Likewise, the pronation action of the foot causes internal rotation of the tibia and of the femur, followed by the rotation of the entire leg [30].A tibial rotation of 11.1° might entail dorsiflexion of the posterior part of the foot of 18.7°, which poses a higher risk of injury to the hip, knee and ankle.According to Snook [31], when repeated excessively, the internal rotation of the tibia can result in hyperpronation of the subtalar joint and, therefore, several osteoarticular complications.However, scholars have noted that physical condition and professional experience are significant variables affecting good running technique and thus the likelihood of developing subtalar hyperpronation [32,33].In our study, hyperpronation values were not observed.
The causes of lower limb pathologies also appear to result from the impact forces that overburden the pronation mechanism, posing a risk to the articular structures.When we observe hyperpronation of the subtalar joint, it is very probably associated with a strong impact that occurs during the foot-ground contact phase given that pronation is a mechanism that attenuates the impact resulting from the foot's contact with the ground, and consequently offers osteoarticular protection [17].Study by Gottschall and Kram [34] confirms that impact forces are more influenced by variations in negative gradient than in positive gradient as locomotion in negative gradients requires greater use of elastic energy.In this study, the running speed was kept constant and at a comfortable rate, which was probably insufficient to cause changes in the impact force values and, consequently, changes in articular behavior.This result demonstrates the importance of running speed in the behavior of maximum subtalar pronation, as previously demonstrated by Oliveira et al. [7] (although Oliveira et al. [7] did not make mechanical evaluations (e.g.W int )).This study demonstrates that W int is influenced by gradient, but gradient does not influence the behavior of the subtalar joint during submaximal running irrespective of the mathematical model adopted .
Some authors described the importance of the intensity of effort in the behavior of the biomechanical aspects of locomotion.For example, the preference for prescribing moderate intensity exercise rather than vigorous exercise reflects a body of research reporting a greater number of injuries caused by running than by walking.The American College of Sports Medicine (ACSM, 2011) states that, "Walking and moderate-intensity physical activities are associated with a very low risk of musculoskeletal complications, whereas jogging, running, and competitive sports are associated with increased risk of injury" [35,36,37].However, an important distinction must be made.Walking and running differ in mode, not just in intensity.Running has a flight phase between steps, resulting in the runner striking the ground with greater force than a walker does [38].Swain et al. [38] propose that the aerobic intensity of running is not responsible for the increased risk of musculoskeletal injuries; rather, this increased risk is due to impact forces.Moreover, mode selection can separate aerobic intensity from impact forces, an important possibility to consider when interpreting our results.In this study, we adopted different positive gradients undertaken at the same running speed, e.g. each subject ran at a comfortable speed at all gradients.Despite the increase in effort intensity confirmed by the W int values, the maximum subtalar pronation values remained constant, regardless of the mathematical models adopted.Thus, this study recommends running on a treadmill on an inclined surface and at a constant speed as the ideal exercise choice.This approach does not affect maximum subtalar pronation and is, thus, unlikely to result in greater orthopedic stress when compared with running at high speeds on a horizontal plane.

Conclusion
The results of this study show that, applying any of the two mathematical models, gradient does not influence the maximum subtalar pronation during submaximal running, i. e., the maximum subtalar joint is not influenced by gradient but, probably, by physiological intensity.However, the W int of running and consequently the intensity of effort are impacted by positive gradients.Incline treadmill running at a constant speed has been demonstrated to be an excellent choice of exercise as it causes no changes to the maximum subtalar pronation and consequently is unlikely to cause greater orthopedic stresses than is found when running at high speeds on a horizontal plane.This finding indicates that this form of running is safe and effective in periodization training.In terms of further studies, it is suggested that additional investigation of the influence of W ext and the type of footwear on energy cost and of the maximum subtalar pronation in other conditions would be beneficial.

Figure 1 -
Figure 1 -Illustration of the markers at the rear part of the left leg and foot.

Figure 2 -
Figure 2 -Mathematical models of two and four points for calculation of subtalar pronation [2].

Table 1 -
Mean and standard deviation (SD) values of the variables internal mechanical work (W int ) and maximum subtalar pronation calculated with two and four anatomical reference points, at different gradients, of 16 trained male long-distance runners Note: Asterisks represent statistically significant differences between the mathematical methods (i.e., 2 and 4 points); letters represent statistically significant differences compared with 1% (a); 5% (b) and 10% (c) gradients.p < 0.05.