Relationship Between Foot Flexibility and Leg Muscle Stiffness After Running: a Cross-sectional Study

doi:10.21203/rs.3.rs-49959/v1

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Relationship Between Foot Flexibility and Leg Muscle Stiffness After Running: a Cross-sectional Study

https://doi.org/10.21203/rs.3.rs-49959/v1

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Background

Deformation of the foot is related to the development of running injuries. The prevention of running injuries requires the management of changes in leg muscle stiffness after running. However, the relationship of muscle stiffness and the structure and flexibility of the foot arch is unclear. The purpose of this study was to investigate differences in muscle stiffness and flexibility of the arch before and after running.

Methods

Twenty lower limbs of 10 healthy volunteers were enrolled. All of the subjects performed the same running task on a treadmill set at an incline of 7%, running at a speed of 8 km/h for 60 min. The shear elastic modulus of the longitudinal axis of the medial and lateral gastrocnemius (MG, LG), flexor digitorum longus (FDL), and abductor hallucis muscles were measured both before and after running using ultrasound shear wave elastography. Arch height index (AHI) and arch height flexibility (AHF) were measured at 10, 50, and 90% of the body weight loaded position, respectively. The correlation of AHI, AHF, and alterations in each muscle stiffness before and after running was assessed using Spearman’s rank correlation coefficient.

Results

The FDL, LG, and MG were significantly harder after running than before running. The AHI and AHF had no significantly difference between before and after running. There were significant moderate correlations between AHF50 before running and stiffness of the FDL after running.

Conclusion

Increased stiffness of the FDL is related to medial tibial stress syndrome. Our results indicate that stiffness of the arch is associated with greater stiffness of the FDL, which restricts performance of the dynamic function of stretching the muscle and tendon complex of the toe flexor with weight loading on the foot.

Operations Research

Flexor digitorum longus

Running

medial longitudinal arch

stiffness

1. The stiffness of flexor digitroum longus is increased after running.
2. Arch flexibility is decreased after running, although arch height shows no change.
3. Less flexible arch show higher flexor digitroum longus stiffness after running.

The development of running injuries is multifactorial, with passive range of motion, muscle strength, biomechanics of the running, gender and body weight [1] [2, 3] [4]. During running, muscle stiffness due to malalignment and overuse increases mechanical stress at the insertion of the skeletal muscles to the bone. Several authors demonstrated that the flexor digitorum longus (FDL), and soleus muscles originated from the medial tibial border, and the medial tibial stress syndrome (MTSS) Increase in the stiffness of the flexor digitorum longus (FDL), and traction-induced injury, related to muscles of the superficial and deep posterior compartments, has been implicated as the cause of medial tibial stress syndrome (MTSS) with symptoms commonly occurring in the distal third of the posteromedial tibia. soleus muscles originated from the medial tibial border is related to medial tibial stress syndrome [5] [6, 7]. In addition, Achilles tendinopathy is related to stiffness of the medial and lateral heads of the gastrocnemius (MG, LG) [8]. During physical therapy, these muscles are treated by stretching and strength training[9]. However, in many cases, the symptoms recur with a return to activity. Therefore, during physical therapy for running injuries, it is important to control for changes in the stiffness of key muscles after running.

Malalignment of the foot is a well-known cause of running injuries[10–12]. In particular, flatfoot is reported to be a risk factor for patella-femoral pain syndrome[11] and low back pain[11, 12]. Many studies demonstrate the relationship between running injuries and the static foot posture, although arch flexibility plays a role in buffering loading stress by flattening during weight loading. Recently, Zifchock et al. [13]proposed that most flatfeet are very flexible, with only a small proportion being associated with stiffness. Therefore, it is important for the treatment of running injuries to understand the role of not only static foot posture, but also the flexibility of the arch. However, the relationship between running injuries and flexibility of the arch is unclear.

Long distance running tends to decrease the height of the medial longitudinal arch, and to reduce arch flexibility[14, 15]. Moreover, the stiffness of the dynamic stabilizers of the arch, such as the tibialis posterior and the FDL, is increased after running[16, 17]. However, the effects of the structure and flexibility of the arch on changes in muscle stiffness after running are unclear. The arch of the foot is maintained by both a static stabilizer and a dynamic stabilizer as extrinsic and intrinsic foot muscles. We hypothesize that patients with greater alteration of both structure and flexibility of the foot show an increase in stiffness of both the leg and foot muscles that maintain arch structure. Therefore, the purpose of this study was to investigate changes in muscle stiffness and the structure and the flexibility of the arch of the foot before and after running.

Participants

Twenty lower limbs of 10 healthy university students who habitually participated in recreational sports activity more than 2 days per week were enrolled in this study. Inclusion criteria were subjects without any history of pain in the leg and foot while running. Two of the subjects could not finish the running task and were excluded from the study. Thus, 16 lower limbs of the remaining 8 subjects (age, 21.4±0.5 years; height, 162.4±9.2 cm; body weight, 54.1±8.3 kg; 5 males) were analyzed. The study was approved by the Medical Ethics Committee of the authors' institution (2018–103), and all the subjects provided informed consent for study participation.

Procedure

All subjects performed the same running task on a treadmill (Adventure3, Johnson Health Tech, Tokyo, Japan) set at an incline of 7% and a running speed of 8 km/h for 60 min after 3 min of warm up. Warm up started with level walking (4 km/h) for 90 s, followed by level jogging (6 km/h) for 90 s. After the warm up period, the incline was set at 7% and the running task was commenced (8 km/h). The foot contact pattern of the runners was not restricted.

Muscle stiffness was assessed using ultrasound shear wave elastography (Aplio 300, Canon Medical Systems, Tokyo, Japan) and a 5–14 MHz linear probe. A higher shear elastic modulus indicates an increase in the stiffness of the tissue. The shear elastic modulus (kPa) of each muscle was calculated automatically from 3 circular regions of interest (ROI) in the color mapped area of elastographic images of each muscle. Assessment of the shear elastic modulus after running was completed within 10 min after the running task. The shear elastic modulus of the longitudinal axis of the MG, LG, FDL, and abductor hallucis (AH) muscles were measured both before and after running for 60 min.

The LG and MG were measured at the proximal 30% of the lower leg (from the popliteal crease to the lateral malleolus). The FDL was measured at the proximal 50% of the area between the cleavage line of the knee and the medial malleolus [16, 17]. The AH was measured at the medial border of the foot below the navicular bone. The FDL muscle was identified using a B-mode ultrasound image during passive motion of the toe. In addition, we marked the measurement site with cotton bandages so that measurements both before and after running could be recorded at the same site.

Ten lower limbs of 5 participants were included in a reliability study. Muscle stiffness was assessed by a single tester who had practiced ultrasound imaging for 2 h per week for 2 months before the study. The tester performed assessments 3 times as the first session, and repeated the evaluations 3 times on another day as the second session. Assessment of intra-tester reliability of the measurement of muscle stiffness was performed using the intra-tester correlation coefficient [ICC (1,k)], and the standard error of the mean (SEM) was calculated from the mean value of the first and second sessions. Minimum detectable change with 95% confidence intervals (MDC₉₅) was calculated using equation (1).

The structure and flexibility of the medial longitudinal arch was assessed using the modified arch height index (AHI) [18] and arch height flexibility (AHF) [13], respectively. Images of the medial side of the foot at 10%, 50%, and 90% body weight (BW) loading were captured by a digital camera (EOS Kiss X7i, Canon Inc., Tokyo, Japan) positioned at a constant distance (90 cm) from the foot. The dorsal arch height (DH) at 50% of the foot length divided into the truncated foot length in the 10%, 50%, and 90% body weight-loaded positions were calculated as AHI₁₀, AHI_50, and AHI₉₀, respectively. The differences between AHI₅₀ and AHI₁₀, and AHI₉₀ and AHI₁₀ were assessed as AHF₅₀ and AHF₉₀ by equations (2) and (3):

Difference in AHI and difference in AHF (DAHI, DAHF) were defined as the difference in each parameter before and after running. A higher DAHI indicated a decrease in arch height after running, and a higher DAHF indicated an increase in arch flexibility after running.

Analysis

Muscle stiffness, arch structure, and arch flexibility before and after running were compared using the Wlicoxon test, and the correlation of arch structure, arch flexibility, and the difference in each parameter with muscle stiffness before and after running were assessed using Spearman’s rank correlation coefficient. All statistical tests were performed using SPSS statistics version 25.0 (IBM Corp., Armonk, NY, USA), with p < 0.05 considered significant.

The shear elastic modulus of each muscle is shown in Table 1. ICCs (1,k) of all the muscles were considered to have high reliability (> 0.7).

Table 1

Reliability of the shear elastic modulus
	ICC (1,k)	SEM	MDC₉₅
LG	0.82 (0.41–0.94)	1.97 (1.40–3.34)	5.46
MG	0.73 (0.09–0.92)	3.25 (2.30–5.52)	9.01
FDL	0.97 (0.91–0.99)	0.76 (0.53–1.28)	2.11
AH	0.98 (0.93–0.99)	0.57 (0.40–0.97)	1.57
LG, lateral gastrocnemius; MG, medial gastrocnemius; FDL, flexor digitorum longus; AH: abductor hallucis

The shear elastic modulus of each muscle before and after running for 60 min is shown in Table 2. The FDL, LG, and MG were significantly harder after running than before running. The hardness of the AH was not significantly different between before and after running.

Table 2

Alteration of muscle stiffness after running
	Before running						After running						p-value
LG	20.2	(	15.6	-	25.1	)	27.2	(	23.1	-	44.7	)	0.001
MG	25.8	(	20.0	-	29.3	)	38.8	(	34.4	-	47.3	)	0.001
AH	19.3	(	16.5	-	24.3	)	20.8	(	14.8	-	24.4	)	0.756
FDL	19.6	(	14.7	-	22.0	)	21.8	(	18.3	-	27.1	)	0.013
LG, MG, and FDL stiffness after running was significantly higher than before running.
LG: lateral gastrocnemius, MG: medial gastrocnemius, FDL: flexor digitorum longus, AH: abductor hallucis

The structure and flexibility of the arch before and after running are shown in Table 3. The structure of the arch was not significantly different before and after running. In the assessment of arch flexibility, AHF₅₀ indicated a significant decrease in the flexibility of the arch after running.

Table 3

Difference in arch height and flexibility before and after running
	Before running						After running
AHI₁₀	0.4	(	0.4	-	0.4	)	0.4	(	0.4	-	0.4	)	0.877
AHI₅₀	0.4	(	0.4	-	0.4	)	0.4	(	0.3	-	0.4	)	0.098
AHI₉₀	0.4	(	0.3	-	0.4	)	0.4	(	0.3	-	0.4	)	0.148
AHF₅₀	2.7	(	1.9	-	3.8	)	3.7	(	2.5	-	4.5	)	0.017
AHF₉₀	2.1	(	1.4	-	2.3	)	2.0	(	1.8	-	2.6	)	0.278
AHF₅₀ after running is significantly higher than that before running.
AHI₁₀, _50, and ₉₀ is arch height index for the 10, 50, and 90% weight loading, respectively.
AHF₅₀ and ₉₀ is arch height flexibility for the 50 and 90% weight loading, respectively.

The correlation coefficients between AHI and AHF before running and the muscle stiffness after running are shown in Table 4. There were significant moderate correlations between AHF₅₀ before running and stiffness of the FDL after running. Thus, subjects with lesser flexibility of the arch before running demonstrated harder FDLs after running.

Table 4

Correlation coefficients between arch parameters before running and muscle stiffness after running
	LG	MG	AH	FDL
AHI₁₀	-0.26	-0.07	-0.01	-0.35
AHI₅₀	-0.19	-0.35	-0.16	-0.10
AHI₉₀	-0.32	-0.26	-0.17	-0.25
AHF₅₀	-0.21	0.43	0.23	-0.50	*
AHF₉₀	-0.07	0.21	0.25	-0.39
LG, lateral gastrocnemius; MG, medial gastrocnemius; FDL, flexor digitorum longus; AH, abductor hallucis. AHI₁₀, _50, and ₉₀ is the arch height index for the 10, 50, and 90% weight loading, respectively. AHF₅₀ and ₉₀ is the arch height flexibility for the 50 and 90% weight loading, respectively.

The purpose of this study was to investigate changes in muscle stiffness and the structure and the flexibility of the arch of the foot before and after running. As results, decreased shear elastic modulus of the FDL, MG, and LG was observed after 60 min of uphill running, but there was no affect on arch height. Furthermore, after running, there was an increase in arch flexibility with 50% weight loading. Subjects with lower flexibility of the arch after running demonstrated greater stiffness of both the LG and FDL after running. Moreover, subjects with lesser flexibility of the arch before running had a greater increase in stiffness of the FDL after running than those with greater flexibility of the arch. Swanson et al. reported that uphill running increased plantar flexion of the ankle during the propulsive phase[19]. Further, uphill running requires the generation of greater ankle power than that required during level and downhill running[20–22]. The resultant increased compartment pressure of the plantar flexor muscles by the repetitive overload stress during running leads to greater stiffness of both the gastrocnemius and FDL. Stiffness of the gastrocnemius reportedly has a strong correlation with plantar fasciitis[23]. Moreover, patients with a history of medial tibial stress syndrome had stiff FDLs[17] and increased stiffness of the FDL after running[16]. These results are similar to those of the our study, which show an increase in the stiffness of muscles related to running injuries. The arch height did not have any difference between before and after running, although, we hypothesize the lower arch is shown after running. Because, the long distance runners showed to decrease the arch height after half and full marathon [14] [15]. These differences of the influence the arch structure is due to the level of distance, therefore, it has a possibility to decrease the arch height after longer distance than current study. In the other hand, there was shown to decrease the arch flexibility after running. Despite the overwhelming focus on arch height as a predictor of overuse injury, there is evidence to suggest that arch stiffness might also be a key factor in predicting overuse injury[13] [24] [25] [26]. However, relationship arch flexibility and muscle stiffness after running remind uncleared. This is a first study, the subject with low flexible arch before running has been demonstrated greater stiffness of both the LG and FDL after uphill running.

The FDL inverts the ankle and elevates the arch of the foot. LG muscle fascicles are reported to have a twisted structure in the Achilles tendon[27], resulting in stretching of the MG, LG, and soleus when the subtalar joint is pronated, and shortening with supination[28]. Thus, subjects with greater stiffness of both the FDL and LG demonstrate decreased arch flexibility, because these muscles restrict pronation of the calcaneus.

Yamauchi et al[29] showed that toe flexor strength was related to arch flexibility in the weight-loaded position and that there is a greater increase in toe flexor strength when changing from the sitting to standing position in subjects with a flexible arch as compared to those with a stiff arch. Thus, a stiff arch restricts performance of the dynamic function of stretching of the muscle and tendon complex of the toe flexor when weight is loaded on the foot. This function is known as stretch shortening cycle, which demonstrates the higher efficiency of the skeletal muscle tension. Our study demonstrated that subjects with low flexible arch before running show greater stiffness of the FDL than those with high flexible arch after repetitive weight loading, as during running. The foot with low flexible arch has difficulty participating in the stretch shortening cycle of the FDL, which leads to overuse of the FDL.

There are three limitations to this study. First, although we assessed foot alignment before and after running, we did not assess kinematics during running. Thus, the effects of kinematics during running on arch height and muscle activity are unclear.

The Achilles tendon is a tough band of dense connective tissue that connects both the gastrocnemius and soleus muscles to the calcaneal tendon. Further, the tibialis posterior muscle plays a big role in maintenance of arch structure. However, in this study, these muscles were not tested because of their deep position, difficulty in assessment of the stiffness of deep muscles, and the presence of a hard aponeurosis superficial to the muscle. Further, muscle stiffness needs to be assessed less than 10 min after running for consideration of muscle fatigue.

the subjects in this study did not have any symptoms of overuse injury in the lower limbs. Further studies will need to assess the altered arch stiffness and muscle stiffness after running in patients with running injuries.

Muscle stiffness related to running injuries was increased after 60 min of uphill treadmill running (8 km/h, 7% incline). Further, although arch height did not change, arch flexibility was increased after running. Stiffness of the arch before running was associated with greater stiffness of the FDL after running, which restricted performance of the dynamic function of the stretching shortening cycle of the muscle and tendon complex of the toe flexor with weight loading on the foot. Further studies should assess the effect of muscle hardness on running injuries.

LG, lateral gastrocnemius; MG, medial gastrocnemius; FDL, flexor digitorum longus; AH, abductor hallucis; AHI, arch height index; AHF, arch height flexibility; DAHI, difference in AHI; DAHF, difference in AHF

Ethics approval and consent to participate

This study was approved by the ethics committee of Morinomiya University of Medical Sciences (2018–103), and all the subjects provided informed consent for study participation.

Consent for publication

Not applicable

The work presented herein is original, has not been previously published in whole or in part, and is not under consideration for publication in any other journal.

Availability of data and materials

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Competing interests

The authors declare that they have no competing interests.

Funding

This work was supported by JSPS KAKENHI Grant Number 19K19815

Authors' contributions

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Acknowledgements

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Relationship Between Foot Flexibility and Leg Muscle Stiffness After Running: a Cross-sectional Study

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