Influence of maximum-graded exercise test on maximal plantarflexion and dorsiflexion torque production in the seated and supine positions

Abstract

BACKGROUND:

There have been multiple studies focusing on the relationship between ankle muscle torque and fatigue with different body positions but have found conflicting results.

OBJECTIVE:

We investigated the effect of body position on maximum voluntary isometric contractions (MVIC) of ankle plantarflexors (PF) and dorsiflexors (DF) in the pre and post-fatigued conditions in healthy adults.

METHODS:

Twenty-five participants ran on a treadmill until volitional exhaustion by performing the Bruce protocol. The participants then performed three MVICs for both PF and DF before and after volitional exhaustion.

RESULTS:

Peak torques of PF ( $p<$ 0.01) and DF ( $p<$ 0.01) in the pre-fatigue condition were greater than in the post-fatigue condition regardless of the body position. Peak torques of PF ( $p<$ 0.01) and DF ( $p=$ 0.03) in the seated position were greater than in the supine position regardless of time. Variances of peak torque differences were not significantly different between the pre and post-fatigue conditions for the seated and supine positions ( $p=$ 0.09).

CONCLUSIONS:

The results of this study suggest that the body position affects ankle PF and DF torques but does not influence the magnitude of PF and DF strength declines elicited by a fatiguing protocol. Therefore, to obtain the most reliable MVIC measurements, the body position during MVICs should be consistent.

Keywords

Running Bruce protocol fatigue maximum voluntary isometric contraction (MVIC)isokinetic dynamometer

1. Introduction

Plantarflexors (PF) and dorsiflexors (DF) are essential components of a normal gait cycle and play large roles in maintaining stability [1]. Running performance relies on both the strength of the PF and DF, as the eccentric contractions of the DF produce the driving force for the concentric contractions of the PF during takeoff [2]. Measuring the peak torque of PF and DF could isolate muscular strengths and weaknesses in a fatigued state, which is when the ankle may be more prone to injury [3].

One of the most common graded exercise tests is the Bruce protocol. Multiple studies have examined the reliability of the Bruce protocol in obtaining accurate VO2 measurements and exhaustion in young men and older women. Studies by both Nordrehaug et al. and Fielding et al. have concluded that VO2 was accurately reproducible in their subject populations using the Bruce Protocol [4, 5]. It is important to accurately emulate the functional environment of a fatiguing run compared to using an isokinetic dynamometer to reach fatigue in order to determine its effects on ankle torque production. Thus, a number of studies have used fatigue protocols to examine the effect on ankle PF and DF in athletes but have displayed conflicting results in ankle fatigability. A study by Fourchet et al. investigated the effects of a 5-hour hilly run on ankle torque and fatigability. They conducted a fatiguing resistance test, which resulted in decreased maximum voluntary isometric contractions (MVIC) of PF, but DF was not significantly decreased [6].

In contrast to his previous findings, another study by Fourchet et al. demonstrated no significant changes of isokinetic peak torques between PF and DF in the pre and post-fatigue conditions [7]. This may have occurred because they used a high-intensity running protocol on PF fatigability, which was not consistent with their previous fatigue test that had used hill running to fatigue. Previous studies in ankle fatigue have used their own respective fatigue protocols, which may have created discrepancies in the results due to the use of fatigue protocols that have not been well established [6, 7]. Therefore, the Bruce protocol offers a more valid and reliable fatigue protocol compared to those that have not been tested and reviewed.

Previous studies have shown that body positions could affect muscle torque, but none have compared the MVIC of PF and DF contractions after a functional fatigue protocol. A study by Rochette et al. investigated the effect of a submaximal fatiguing contraction on knee extension in the seated and supine positions [8]. The MVIC in the pre-fatigue condition of the seated position was greater than in the supine position. However, in the post-fatigue condition, the seated position had a larger decrease in MVIC than the supine condition [8]. Maffiuletti and Lepers reached a similar conclusion that force production in the seated position was significantly greater than in the supine position [9]. The seated position may have had greater torque production due to the shortened length of the rectus femoris muscle [9]. Additionally, Turpin et al. also conducted that maximal PF torque in the seated was greater than in the supine positions [10]. These previous studies did not use a fatigue protocol, instead Rochette et al. used fatiguing isometric contractions of the knee extensor muscles for both body positions [8].

Unlike isokinetic contraction fatigue protocol, a functional running fatigue protocol such as the Bruce protocol will result in fatigue affecting several muscles in the lower extremities rather than just the knee extensors. Therefore, the Bruce Protocol may result in different torque production at several joints in the seated and supine positions. Body position and fatigue due to the Bruce protocol may alter functions of the lower extremities, which can eventually influence ankle torque production. Thus, in order to understand how different body positions influenced ankle torque in a fatigued condition induced by the Bruce protocol, it is important to investigate the effects of a functional fatigue protocol on ankle torque in different body positions.

The purpose of the study was to identify the effects of fatigue on maximal torque production in the PF and DF in the seated and supine positions. To the best of our knowledge, this is the first study to investigate the effect of functional fatigue induced by the Bruce protocol on the MVIC of PF and DF in the seated and supine body positions. The hypothesis was that the difference between the pre and post-fatigued conditions in the seated position would be greater than in the supine position. Additionally, the post-fatigued condition will have lower peak torques of PF and DF compared to the pre-fatigued condition.

2. Materials and methods

2.1 Participants

Twenty-five volunteers, twelve females and thirteen males (22.9 $\pm$ 1.2 yrs, 167.8 $\pm$ 9.2 cm, 63.9 $\pm$ 11.9 kg) reported no injuries affecting the lower extremities on an injury history questionnaire, which included ankle sprains. For inclusion criteria, the participants should be categorized as a low-risk population for cardiovascular disease according to the current American College of Sports Medicine (ACSM) Guidelines for Exercise Testing and Prescription. Additionally, all of the participants should have performed at least 1.5 hours of planned physical activity per week. Physical activity was defined as any intended exercise for the goal of improving and benefiting health such as bike riding, jogging, stair-stepping, walking, weight training, and yoga. Participants who volunteered but did not meet the inclusion criteria were excluded. All participants gave written informed consent approved by the University Institutional Review Board. Recruitment flyers were posted on advertising boards and all participants were recruited in the Richmond metro area in Virginia.

2.2 Bruce protocol

The guidelines for the Bruce Protocol set by ACSM were followed to determine volitional fatigue and the termination of activity prior to completion of the Bruce protocol [11]. The participants performed the protocol using a Trackmaster treadmill (Full Vision Inc., Newton, KS, USA). While running, the subject’s heart rate was monitored using a ParvoOneMax system (Parvo Medics, Salt Lake City, UT, USA) and a Polar HR sensor (Polar Electro Inc., New Success, NY, USA). The participants initially walked for 3 minutes at 0.8 m/s with 0% grade for a warm-up. Then the incline was elevated by 2% every 3 minutes with increases in speed to 1.1, 1.5, 1.9, 2.2, and 2.5 m/s until the participants reached volitional fatigue. The rate of perceived exertion (RPE) categorized the subject’s exhaustion and was taken every three minutes using a scale from 6–20 [12]. Verbal encouragement was provided throughout the fatiguing protocol. The test was terminated if the subject’s heart rate surpassed their age-associated maximum heart rate (220-age). Angina, dizziness, and nausea were additional test terminating criteria. The characteristics of the participants are shown in Table 1.

Table 1
The mean and standard deviations for participants’ max heart rate (HR ${}_{\text{max}}$ ) and heart rate (HR), duration of running and ratings of perceived exertion scale (RPE) at volitional exhaustion

HR ${}_{\text{max}}$	HR	Duration (minute)	RPE
195.9 $\pm$ 1.2	194.1 $\pm$ 7.8	12.8 $\pm$ 1.1	20 $\pm$ 0

Values are mean $\pm$ SD.

2.3 Procedure

Participation required a total of two visits with at least 48-hours between each visit. One visit was for the supine test position and the other visit was for the seated test position. The order of the positions and contractions were randomized and counterbalanced. For a single visit, the participants participated in a warm-up exercise by riding a stationary bike for five minutes. The participants were situated into an isokinetic dynamometer (BIODEX, INC, Shirley, NY, USA) with appropriate straps across their ankles, chest, thigh, and waist. With proper instruction, the participants performed a set of warm-up contractions at both 50% and 75% of their MVIC. After the warm-up set, the participants were given a ten-minute rest before testing. Verbal encouragement was provided during the MVIC. An MVIC in the PF direction was held for five seconds followed by an MVIC in the DF direction for five seconds. The participants were given a five-second rest between trials. Three trials of MVIC were performed in both directions. After completing the pre-fatigue trials, the participants underwent the Bruce protocol on a treadmill. The participants ran until they reached volitional exhaustion as previously described. The participants then performed the last three trials of MVIC as the post-fatigue trials in both directions as described above. There was a one-minute delay between the conclusion of the Bruce protocol and the post-fatigue test to properly position the subject for the MVIC.

2.4 Test positions

For both the seated and supine test positions, the subject’s ankle axis of rotation (dominant malleolus) was aligned with the dynamometer shaft while their knee was fully extended using a limb-support pad and appropriate straps. The subject’s ankle was set at 0 ${}^{\circ}$ of plantarflexion (neutral position). The seatback angle was set at 70 ${}^{\circ}$ for the seated position and was fully reclined for the supine position. While performing the MVIC, the subject’s arms were crossed on the chest to avoid additional torque that may be generated by holding the handles adjacent to the seat.

Table 2
Differences of peak torques of plantarflexors (PF) and dorsiflexors (DF) between the pre and post-fatigue condition in male and female

% Difference	Gender	Supine	Seating
PF	Male	25.1 $\pm$ 12.8	20.3 $\pm$ 10.1
Torque (%)	Female	21.2 $\pm$ 10.7	19.4 $\pm$ 8.2
DF	Male	25.1 $\pm$ 10.6	10.9 $\pm$ 6.4
Torque (%)	Female	23.3 $\pm$ 11.1	11.3 $\pm$ 6.6

Values are mean $\pm$ SD.

Table 3

Peak torques of plantarflexors (PF) and dorsiflexors (DF) in the pre and post-fatigue condition in the supine and seating positions

	Fatigue test	Supine		Seating		Mean
PF	Pre	94.5	$\pm$ 12.8	113.1	$\pm$ 16.3	103.8	$\pm$ 17.2 ${}^{*}$
Torque (Nm)	Post	75.0	$\pm$ 11.7	89.9	$\pm$ 13.2	82.4	$\pm$ 14.4
	Mean	84.7	$\pm$ 15.6	101.5	$\pm$ 18.8 $\Omega$
DF	Pre	19.9	$\pm$ 3.6	23.6	$\pm$ 5.4	21.7	$\pm$ 4.9 ${}^{*}$
Torque (Nm)	Post	15.9	$\pm$ 6.1	20.7	$\pm$ 5.6	18.3	$\pm$ 6.3
	Mean	17.9	$\pm$ 5.4	22.2	$\pm$ 5.6 $\Omega$

${}^{*}p$ -value $\leqslant$ 0.05: seating $>$ supine, $\Omega$ $p$ -value $\leqslant$ 0.05: pre $>$ post.

Table 4

Differences of peak torque of plantarflexors (PF) and dorsiflexors (DF) between the pre and post conditions in the supine and seating positions

	Fatigue test	Supine		Seating		Mean
PF	Pre-Post	19.5	$\pm$ 14.52	23.2	$\pm$ 15.3	21.4	$\pm$ 14.4
Torque (Nm)		20.0	$\pm$ 14.48%	20.51	$\pm$ 11.2%	20.26	$\pm$ 12.4%
DF	Pre-Post	4	$\pm$ 2.5	2.9	$\pm$ 4.4	3.45	$\pm$ 3.7
Torque (Nm)		20.1	$\pm$ 4.8%	12.28	$\pm$ 5.6%	16.19	$\pm$ 7.8%

2.5 Statistics

The means of the three trials for peak torques of PF and DF in the seated and supine positions were determined. Two-way (time $\times$ position) repeated measure analyses of variance (ANOVA) were used to assess the time effects (pre and post-fatigue) and the position effects (seated and supine positions) on the peak torque of PF and DF. Post-hoc comparisons using Fisher’s Least Significant Difference were performed to assess specific differences when there was a significant difference between the time and position effects. Differences of the peak torques between the pre and post-fatigue conditions in the seated and supine positions for PF and DF were calculated. Two paired $T$ -tests were performed to assess the position effect for PF and DF. Four independent $T$ -tests were performed to assess the gender effect for body positions for PF and DF. The level of significance was set at $\alpha=$ 0.05 for all comparisons. Based on previously published data utilizing similar variables to those in the current study, a priori power analysis ( $\alpha=$ 0.05, $\beta=$ 0.80) determined that an average of fifteen participants was necessary [13]. Effect sizes (eta-squared) of significant differences for the main effects were reported. IBM SPSS Statistics (SPSS Inc, Chicago, IL, USA) was used to perform statistical analyses.

3. Results

3.1 Gender

There were no significant differences between male and female ( $p\geqslant$ 0.05) for seating position with PF (t (22) $=$ 1.24, $p=$ 0.11) and DF (t (22) $=$ 2.03, $p=$ 0.13) and supine position with PF (t (22) $=$ 1.83, $p=$ 0.12) and DF (t (22) $=$ 1.54, $p=$ 0.11) (Table 2).

3.2 Plantarflexors

There was no significant interaction between time and position. (F ${}_{1,28}=$ 0.38, $p=$ 0.54). There were significant main effects for time (F ${}_{1,28}=$ 52.53, $p<$ 0.01) and position (F ${}_{1,28}=$ 17.72, $p<$ 0.01). Post-hoc comparisons using the Fisher’s Least Significant Difference indicated that the mean peak torque of PF in the pre-fatigue condition ( $p=$ 0.01 with 95% CI [98.35, 109.29]) was significantly higher than in the post-fatigue condition (95% CI [77.76, 87.10], partial eta squared $=$ 0.09) regardless of position. It also indicated that the mean peak torque of PF in the supine position ( $p<$ 0.01 with 95% CI [78.93, 90.50]) was significantly lower than in the seated position (95% CI [95.74, 107.32], partial eta squared $=$ 0.11) regardless of time (Table 3).

3.3 Dorsiflexors

There was no significant interaction between time and position. (F ${}_{1,28}=$ 0.71, $p=$ 0.41). There were significant main effects for time (F ${}_{1,28}=$ 25.33, $p<$ 0.01) and position (F ${}_{1,28}=$ 5.56, $p=$ 0.03, partial eta squared $=$ 0.08). Post-hoc comparisons using the Fisher’s Least Significant Difference indicated that the mean of peak torque of DF in the pre-fatigue condition ( $p<$ 0.01 with 95% CI [20.06, 23.47]) was significantly higher than in the post-fatigue condition (95% CI [16.11, 20.49], partial eta squared $=$ 0.14) regardless of position. It also indicated that the mean of peak torque of DF in the supine position ( $p=$ 0.03 with 95% CI [15.33, 20.52]) was significantly lower than in the seated position (95% CI [19.55, 24.74], partial eta squared $=$ 0.08) regardless of time (Table 3). There were no significant differences between the pre and post-fatigue peak torque differences for the supine and seated positions; t (14) $=$ ( $-$ 0.98), $p=$ 0.09 (Table 4).

4. Discussion

The main purpose of the study was to ascertain differences between different body positions during MVIC of PF and DF under pre and post-fatigue conditions. The main findings were (i) that the MVIC of PF and DF were greater in seated conditions for the pre and post-fatigue conditions than in supine positions and (ii) the ratio of percentage decrease between the pre and post-fatigue conditions were not significantly different for both body positions. The results did not support our hypothesis that the difference between the pre and post-fatigue conditions in the seated position would be greater than in the supine position.

The pre-fatigue condition demonstrated greater peak torques of PF and DF than the post-fatigue condition regardless of the testing position due to many possible factors such as changes in the motor unit recruitment [14]. The review conducted by Weir et al. mentioned that the definition of muscle fatigue is difficult to explain with one model because the mechanism of muscle fatigue is dependent on a task-specific movement [15]. According to one hypothesis about fatigue, the decrease in maximal force output, more specifically MVIC, is caused by the decreased rate of firing of motor neurons [16, 17]. According to Hill, muscle fatigue is also associated with a decrease in muscle contractile speed along with a decrease in force output [17]. Gandevia says that the loss in force occurs due to a “neural dilemma” which is caused when the motor unit firing rate does not match the behavior of the muscle [16]. It can be concluded that the force output of PF and DF for both body positions decreased after conducting the Bruce protocol because the subject’s ankle was fatigued.

Peak torques of PF were greater in the seated position compared to the supine position. In the seated position, the hip is flexed, which causes the knee extensors to shorten compared to the supine position [9]. A possible conclusion may be that the shortened muscle length accommodates a stronger neural activation [9, 18]. The increased neural activation for shortened muscle lengths may be due to the compensation for a mechanical disadvantage, which indicates that torque is decreased as the muscle is shortened [9, 18]. In the seated position, the neural activation will be stronger because of the shortened muscle, which may have increased the MVIC of the plantarflexion. Therefore, the ability of the knee extensors to produce torque may have directly influenced the torque output during plantarflexion. Turpin et al. measured the differences in isolated isometric PF contractions and multi-joint isometric PF contractions. Multi-joint contractions had higher torque in PF for both the seated and supine positions [10]. Turpin et al. concluded that the knee and hip extensors can still influence ankle torque measurements without crossing the ankle joint. Even though the accessory muscles do not cross the ankle joint, they still provide a neural activation influence on ankle torque production [10]. Thus, a possible explanation may be that the increased knee extensor activation in the seated position caused an increased torque production during a plantarflexion in the seated position compared to the supine position. Regardless of a compensation mechanism, it is still unclear to establish a relationship between ankle torque and hip position. According to our results, it is apparent that to standardize the torque testing procedure is crucial because of the effects of body position on ankle torque.

Contrary to our results, Turpin et al. observed greater PF torque in the supine position compared to the seated position [10]. One possible reason for the conflicting result may be because of the different knee positions. Turpin et al. used a hip and knee angle of 90 ${}^{\circ}$ in the seated position while the present study used a hip angle of 70 ${}^{\circ}$ with a fully extended knee [10]. With increasing flexion of the knee, the EMG root mean square decreased in the gastrocnemius while the soleus remained unchanged. The gastrocnemius in the supine position with the knee fully extended contributes a minimum of 40% to maximal PF torque production [19, 20]. Therefore in Turpin’s seated position, the gastrocnemius would have had a decreased influence on PF torque production, which may explain how their maximal PF torque values in the supine position, with the knee fully extended, were greater than in the seated position.

Peak torques of DF were greater in the seated position compared to the supine position. Studies by Andrade et al. and Mitchell et al. have indicated that the position of the hip influences the range of motion (ROM) at the ankle [21, 22]. Mitchell et al. stated that in a seated position with the hip flexed and knee extended, ankle ROM was significantly decreased compared to the supine position [21, 23]. Andrade et al. concluded that the changes in ankle ROM may be attributed to the underlying structures that cross the hip and ankle joints such as peripheral nerves and fasciae [22]. In the seated position, the tension developed by passive tissues may have increased due to the hip flexion at 90 ${}^{\circ}$ compared to the supine position with an extended hip [22]. Therefore, a possible explanation for the increased torque production in the seated position may be due to the increased neural tension in the sciatic nerve or muscle fasciae that may have influenced the force of dorsiflexion [24]. Similar to the results of our study, Turpin et al. also reported that joint torques were greatest in the seated position compared to the supine position [10].

Interestingly, the differences in peak torque between the pre and post-fatigue conditions in the supine position were not different than in the seated positions for PF and DF. Our results did not support our hypothesis. The difference in peak torque for the pre and post-fatigue conditions for the seated positions in PF is 23.1 and for DF is 2.9. For the supine positions, the difference in peak torque for the pre and post-fatigue conditions in PF is 19.5 and in DF is 4. A study done by Christina et al. used two fatiguing protocols which involved two different body positions for the DF and invertor muscles, but regardless there was a similar ratio of percentage decrease in peak torque MVIC for the pre and post-fatigue conditions (DF decreased 57.6 $\pm$ 10.6% and invertors decreased 71.4% $\pm$ 15.3% of the pre-fatigue maximum torque) [3]. We postulated that the seated position would see a greater decrease in MVIC between the pre and post-fatigue conditions because the fatigued knee extensors in the seated position would not be able to provide a large contribution to ankle torque. However, the Bruce protocol caused a similar level of fatigue of the PF and DF in both the seated and supine positions. Thus, it may be possible that the Bruce protocol did not induce sufficient fatigue of the upper leg muscle. Without measurement of the upper leg muscles after the Bruce protocol, it is difficult to fully understand that there was no difference in the ratio of percentage reduction between the two positions. This is considered a research limitation. Therefore, further study is needed to investigate the role of upper leg muscle fatigue on torque during PF and DF activity while in the seated and supine positions.

5. Limitations of this study

It has been suggested that gender would affect strength changes and fatigability [25, 26]. Therefore, this current study may complicate the interpretation of the results. However, some researchers include both men and women for their strength and fatigability studies [27, 28]. The main purpose of this study was to investigate the % change in the difference between pre and post fatigue protocols in the seated compared to supine positions regardless of gender. Therefore, gender was not considered a contributing factor in this study.

6. Conclusion

The present study reinforced the importance of body positioning during maximal torque measurements. The seated position may elicit a greater torque than the supine position regardless of pre or post-fatigue conditions based on our results. Therefore, for consistent strength measurements in a population using seated or supine body positions, one position must be selected and maintained throughout the study. However, for fatigability measurements, both the seated and supine position measurements can be used interchangeably since the ratio of decrease from the pre and post-fatigue conditions remained the same regardless of body position. Finally, examining PF and DF fatigabilities induced by running may help clinicians to prevent ankle fatigue by applying for a targeted strengthening program.

Footnotes

Acknowledgments

The authors would like to thank research assistants for their help with managing participants in this study.

Conflict of interest

There is no conflict of interest regarding this study.

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