Accepted Manuscript Title: Superficial plantar cutaneous sensation does not trigger barefoot running adaptations Authors: M.A. Thompson, K.M. Hoffman PII: DOI: Reference:
S0966-6362(17)30492-7 http://dx.doi.org/doi:10.1016/j.gaitpost.2017.06.269 GAIPOS 5477
To appear in:
Gait & Posture
Received date: Revised date: Accepted date:
21-11-2016 13-6-2017 26-6-2017
Please cite this article as: Thompson MA, Hoffman K.M.Superficial plantar cutaneous sensation does not trigger barefoot running adaptations.Gait and Posture http://dx.doi.org/10.1016/j.gaitpost.2017.06.269 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
SUPERFICIAL PLANTAR CUTANEOUS SENSATION DOES NOT TRIGGER BAREFOOT RUNNING ADAPTATIONS M.A. Thompsona & K.M. Hoffmanb,c
aExercise
Science Department Fort Lewis College Durango, CO 81301 bDepartment
of Orthopedics Denver Health Medical Center Denver, CO 80204 cDepartment
of Vascular Surgery / Podiatry University of Colorado Medical School Denver, CO 80045
Address for correspondence: Melissa Thompson 138 Whalen Gym Exercise Science Department Fort Lewis College 1000 Rim Drive Durango, CO 81301
[email protected] (ph: 970-247-7580)
Highlights: Sensory feedback contributes to barefoot gait adaptations
Anesthetizing superficial skin of the plantar foot did not alter barefoot running
Deep/subcutaneous receptors likely cause barefoot running gait changes
ABSTRACT: It has long been proposed that the gait alterations associated with barefoot running are mediated by alterations in sensory feedback, yet there has been no data to support this claim. Thus, the purpose of this study was to examine the role of superficial plantar cutaneous feedback in barefoot and shod running. METHODS: 10 healthy active subjects (6 male, 4 female); mass: 65.2 + 9.7 kg; age: 27 + 7.1 years participated in this study. 10 over-ground running trials were completed in each of the following conditions: barefoot (BF), shod (SHOD), anesthetized barefoot (ANEST BF) and anesthetized shod (ANEST SHOD). For the anesthetized conditions 0.1-0.3 mL of 1% lidocaine was injected into the dermal layer of the plantar foot below the metatarsal heads, lateral column and heel. 3-dimensional motion analysis and ground reaction force (GRF) data were captured as subjects ran over a 20 m runway with a force plate at 12 m. Kinematic and kinetic differences were analyzed via two-way repeated measure ANOVAs. RESULTS: The differences in gait between the BF and SHOD conditions were consistent with previous research, with subjects exhibiting a significant decrease in stride length and changing from rearfoot strike when SHOD to fore/midfoot strike when BF. Additionally, BF running was associated with decreased impact peak magnitudes and peak vertical GRFs. Despite anesthetizing the plantar surface, there was no difference between the BF and ANEST BF conditions in terms of stride length, foot strike or GRFs. CONCLUSION: Superficial cutaneous sensory receptors are not primarily responsible for the gait changes associated with barefoot running.
Keywords: biomechanics; running; barefoot; sensory; mechanoreceptor
INTRODUCTION: Running requires complex integration of supraspinal input, centrally generated command signals and sensory feedback. Despite this complex neurological integration, humans run in a stereotypical manner due to central nervous system organizational networks, termed central pattern generators (CPGs) that control alternating flexion and extension movements associated with gait [ 1]. CPGs create rhythmic muscle activation seen in locomotion, but feedback from sensory receptors is essential for stereotypical locomotor patterns [ 2]. While sensory feedback is essential for CPG output, the role that specific sensory components play in human running has remained elusive because in vivo measurements are currently not possible.
Sensory sources that influence gait include energetic and mechanical feedback, which provide the individual with information about the environment and their physiological state. Mechanical feedback comes from a variety of sources including stretch receptors, joint receptors and cutaneous mechanoreceptors. It is clear that mechanical feedback plays a role in creating stereotyped gait patterns. However, it remains unknown how variations in these types of sensory feedback influence gait. The comparison of barefoot to shod running highlights gait changes in response to altered mechanical sensory feedback. Compared to barefoot running, shod running is thought to alter cutaneous feedback from the soles of the feet [ 3] and generally results in increases in stride length and adoption of a rearfoot strike pattern [ 4]. Additionally, the use of minimalist shoes highlights mechanical feedback mediated gait changes, with a greater level of minimalism leading toward barefoot-style running mechanics [ 5].
Several gait changes have been reported when individuals change from shod to barefoot running or when running in certain types of minimalist shoes, with the most consistent being decreased stride length and a fore/midfoot strike pattern. Specifically, when running barefoot most individuals decrease stride length by approximately 5.0-8.5% as compared to shod running [ 6, 7, 8]. Additionally, despite the fact that 72-89% of individuals exhibit a rearfoot strike pattern when wearing traditional shoes [ 9, 10], nearly all individuals adopt a fore/midfoot strike pattern when running barefoot or in less cushioned minimalist shoes [ 6, 9, 7, 11].
It has been proposed that the gait alterations associated with barefoot running are due to changes in sensory feedback from the sole of the foot. In a series of studies, Robbins and colleagues proposed that the loss of perception of pain and pressure from the skin in shod running leads to a failure to adopt impact attenuating protective gait adaptations (ground contact on the metatarsal heads and reduced stride length) that are observed when running barefoot [ 12, 13, 3]. The enhanced sensory feedback when running barefoot triggers gait alterations that are associated with reduced impact transmission through the musculoskeletal system, which may lower injury risk [ 14]. Further illustrating the role of sensory feedback are reports that shoes influence ankle joint position sense [ 7] and coordination [ 15]. Additionally, sensory feedback has been shown to influence pressure distribution, muscle activation, lowerlimb kinematics and gait dynamics of walking [ 16, 17]. While the theory of sensory mediated
gait adaptations associated with barefoot running certainly seems plausible, there has been no data to quantitatively support this claim.
Therefore, the purpose of this study was to examine the role of plantar cutaneous feedback in barefoot and shod running in order to substantiate the claim that sensory feedback triggers gait alterations seen in barefoot running. To do this we minimized cutaneous sensory feedback and examined how this reduction in plantar cutaneous sensation affected gait biomechanics during barefoot and shod running. Because in vivo measurements of sensory feedback are not possible, we used a novel anesthesia technique based on the protocol of Meyer & Oddsson [ 18] to anesthetize the end organs of plantar cutaneous receptors without affecting foot and ankle proprioception or intrinsic foot musculature. We hypothesized that with reduced plantar cutaneous sensation individuals would not exhibit gait adaptations (i.e. decreased stride length and fore/midfoot strike pattern) typically observed when switching from shod to barefoot running.
METHODS: Ten healthy, physically active, adults [6 males and 4 females; age: 27 ± 7.1 yr; height: 1.63 ± 0.13 m; mass: 65.2 ± 9.7 kg] participated in this study. Inclusion criteria consisted of rearfoot strike preference when running shod, performing at least 30 minutes of physical activity five days a week, no acute or chronic musculoskeletal injuries, and no history of adverse reaction to anesthetic. The Fort Lewis College Institutional Review Board approved the protocol for this study.
Subjects were tested under two sensory conditions: normal (NORM) and anesthetized (ANEST). Testing sessions for each sensory condition were separated by at least 24 h. For each sensory condition the subject’s gait was analyzed while running both barefoot (BF) and shod (SHOD). Sensory and shoe conditions were tested in a random order. For the SHOD conditions participants ran in their own footwear, however it was required that participants utilized traditional running shoes, defined as a minimum of a 15mm forefoot stack height, 25mm rearfoot stack height and 12mm heel-toe drop. Prior to each testing session, and following footwear changes (e.g. barefoot to shod), subjects ran for 5-10 min to warm-up and familiarize with the condition. In both testing sessions, subjects were instructed to run in their preferred manner (i.e., self-selected stride length and foot strike) but at a consistent velocity. Subjects performed 20 trials (10 BF and 10 SHOD) in each condition (NORM and ANEST). Five strides from 10 separate trials, in which the subject contacted the force plate, were used to calculate participant mean data for each condition. Within a given condition, trials in which velocity or stride length differed by more than 5% were excluded from analysis.
Anesthesia was achieved via intradermal injection of lidocaine based on the protocol of Meyer & Oddsson [ 18]. This involved standard skin preparation with alcohol, inducing brief topical anesthesia with ethyl chloride spray, followed by injection of 0.1-0.3 mL of 1% lidocaine into the dermal layer of skin. This procedure was repeated at five sites (plantar medial, central and lateral metatarsal heads; lateral column and heel) on the soles of both feet. Anesthesia was confirmed when the subject did not have sensation when a 10 g monofilament was pressed on
the foot sole with enough pressure to buckle. Vibratory sensation was evaluated with a 128 Hz tuning fork, following intradermal injections vibratory sensation remained intact in all participants. In order to ensure that only sensory nerves were blocked with the local anesthetic, prior to and during the anesthetization process, strength of the foot musculature was evaluated by having subjects perform simple foot and ankle movements, and by manual testing of intrinsic foot musculature.
Kinematics and Kinetics: 3-dimensional motion analysis and ground reaction force (GRF) data were captured as subjects ran over a 20 m runway with a force plate (AMTI, Waterton, MA) located at 12 m. To measure kinematic data, 16 retro-reflective markers were attached with tape to anatomical landmarks according to the Modified Helen Hayes Marker Set [ 19]. This marker set includes bilateral markers on the anterior superior iliac spines, mid-thigh, femoral epicondyle, mid-calf, malleolus, second metatarsal head and calcaneus. During the shod condition, foot markers were placed on the shoes overlying the anatomical landmarks. Threedimensional positions of each marker were captured at 250 Hz via a Vicon Bonita motion analysis system (Vicon, Oxford Metrics Ltd., UK). Marker trajectory data were filtered via a Woltring filtering routine with predicted mean square error of 4 mm 2. From marker trajectory data, transverse, frontal and sagittal plane joint angles were calculated for the ankle, knee and hip via Vicon Plug-In Gait. Stride length was measured as the horizontal distance between heel marker minima. Gait velocity was calculated as the average of the horizontal displacement of the anterior superior iliac spine markers through the capture volume divided by the
corresponding times. Foot strike was verified by motion analysis, with fore/midfoot strike defined as a foot strike angle < 0o and rearfoot strike defined as a foot strike angle > 0o [ 20].
The three orthogonal components [vertical (v), anterior-posterior (ap), medio-lateral (ml)] of the GRF data were captured at 1000 Hz from the force plate in synchrony with motion capture data. GRF data was low-pass filtered at 30 Hz using a 4th order Butterworth filter. Impact peak magnitude was determined as the first peak in the vGRF; no value was recorded if an impact peak was not present.
Statistics Differences in kinetic and kinematic parameters were analyzed using two-way repeated measure ANOVA tests. This allowed us to assess main effects of the sensory (NORM and ANEST) and shoe conditions (BF and SHOD), and the interaction of the shoe and sensory conditions. We performed Newman–Keuls post hoc tests to ascertain the differences between conditions. A Bonferroni correction was used to account for multiple tests. Significance was defined as p≤0.008 for kinematic variables and p≤0.02 for kinetic variables. All statistical tests were conducted in SPSS Version 23 (IBM, Armonk, NY).
RESULTS: In both the NORM and ANEST conditions participants exhibited a significant decrease in stride length when switching from SHOD to BF running (p<0.001, η2 = 0.256). In the NORM condition
subjects decreased stride length by 6.5% (p<0.001), and in the ANEST condition subjects experienced a 6.7% reduction (p<0.001) (Table 1). For each shoe condition (i.e., BF or SHOD) there was no significant difference in stride length between the NORM and ANEST conditions (p=0.177). There were no significant differences in velocity between any conditions (p=0.100, η2 = 0.033) (Table 1).
Kinematics: In both the NORM and ANEST conditions runners switched from a rearfoot strike when SHOD [NORM SHOD 7.5(3.8)o, ANEST SHOD 7.3(4.2)o] to a fore/midfoot strike when BF [NORM BF 5.5(5.1)o, ANEST BF -3.8(3.2)o] (p<0.001, η2 = 0.701). Correspondingly, in both the NORM and ANEST conditions participants adopted a dorsiflexed ankle angle at ground contact when SHOD and a plantarflexed ankle angle when BF. For a given shoe condition (i.e., BF or SHOD) there were no significant differences in foot strike or sagittal plane ankle angle between the NORM and ANEST conditions (p>0.05). In both the NORM and ANEST conditions participants exhibited greater peak hip flexion when SHOD [NORM SHOD: 43.1(10.1)o, ANEST SHOD: 42.9(9.4)o] as compared to BF [NORM BF: 35.6(11.2)o, ANEST BF: 37.8(11.5)o] (p =0.008, η2 = 0.104).
Kinetics: Kinetic differences were observed between shoe conditions, but for a given shoe condition there were no differences between the NORM and ANEST conditions for any kinetic variables (Figure 1). Both the NORM and ANEST SHOD conditions exhibited a pronounced impact peak, whereas impact peaks were significantly reduced or absent in the BF conditions (NORM SHOD
vs. NORM BF: p=0.016 and ANEST SHOD vs. ANEST BF: p=0.004, η2 = 0.302) (Table 3). In both the NORM and ANEST conditions there was a significant decrease in peak vGRF when switching from SHOD to BF running (p<0.001, η2 = 0.186) (Table 3). Additionally, there was a significant difference in peak apGRF between BF and SHOD running in both the NORM and ANEST conditions (p=0.002, η2 = 0.161) (Table 3). There were no significant differences in mlGRF between any conditions.
DISCUSSION: Consistent with previous research comparing barefoot and shod running, we found that when running barefoot individuals decreased their stride length and adopted a fore/midfoot strike [ 4]. Based on the theory that these observed changes are triggered by diminished sensory feedback when shod, we expected that with the surface of the plantar feet anesthetized individuals would run similar to the shod condition even when barefoot. However, contrary to this hypothesis we observed little effect of anesthetizing the surface of the plantar foot on the examined kinematic and kinetic variables.
To the best of our knowledge this is the first study to use the experimental technique of intradermal local anesthetic injections to examine the role of sensory feedback during running. However, several previous studies have utilized similar techniques to examine the role of sensory feedback in walking and our finding that plantar surface anesthetization did not influence running kinematics or kinetics is in agreement with these results. Following intradermal injections of anesthetic to minimize cutaneous sensory feedback from the plantar
surface of the foot, Höhne et al. [ 21] did not find differences in pressure distribution, force variables or contact times during walking. Similarly, Höhne et al. [ 22] found that intradermal injections of anesthetic to the plantar foot did not affect dynamic stability while walking. Höhne et al. [ 16] did observe kinematic and kinetic alterations and corresponding changes in muscle activation during walking following anesthetization via intradermal injection. However, these observed differences occurred during the phase from foot flat to mid-stance and at push-off, which differs from the periods of the gait cycle where alterations associated with barefoot running occur (e.g. ground contact). Further, Nurse and Nigg [ 17] used ice immersion to minimize sensory feedback from the plantar surface of the foot and quantified the corresponding gait changes during walking. They found that attenuated sensory input lead to altered pressure distribution and muscle activation. However, anesthetization via ice immersion is extremely transient and potentially alters skin and muscle mechanical properties, thus it is possible that these results differ from the present study due to methodological differences.
The intradermal injections of anesthetic used in the present study effectively reduced plantar cutaneous feedback with the anesthetization lasting throughout the duration of the study, but this level of anesthesia was not found to alter gait changes associated with barefoot running. It is possible that failure to observe any effect of plantar surface anesthetization on gait is due to the depth of anesthesia. The anesthesia method was chosen because it specifically targeted the end organs of cutaneous mechanoreceptors without affecting intrinsic foot musculature or ankle proprioception [ 23]. However, this procedure leaves deep sensory receptors intact, which was evidenced by vibratory sensation remaining intact. It is possible that sensory
receptors responsible for the gait changes observed in barefoot running are located deep in the dermal layer and subcutaneous tissue, and/or consist of free nerve endings located in joints and the calcaneal fat pad. Further, slowly adapting type II (SAII) mechanoreceptors respond to higher forces and would be primarily responsible for the sensation of impact [ 24]. Thus, it is likely that SAII mechanoreceptors would be less active when running in traditional shoes because the cushioning attenuates impact. Without being able to rely on the cushioned heel, barefoot runners likely adopt the fore/midfoot strike pattern to reduce impact [ 3]. The present results indicate that this gait change is likely triggered by activation of impact sensing mechanoreceptors rather than activation of more superficial cutaneous receptors. However, this notion is not supported by the findings of Fiolokowski et al. [ 25] who found that leg stiffness during hopping (a proxy for running) decreased following a tibial nerve block. The tibial nerve block eliminates all sensory feedback below the level of the ankle, thus one might expect that this technique would result in greater stiffness, as there is no sensation of the need to reduce impact. However, hopping is not perfectly analogous to running, thus future research could utilize the tibial nerve block technique to further elucidate the role of sensory feedback during running.
The present results indicate that superficial cutaneous sensory receptors are not primarily responsible for gait changes associated with barefoot running, suggesting that deep cutaneous and/or subcutaneous sensory receptors more likely play a dominant role, but it is plausible that energetic and/or other sources of mechanical feedback are responsible for or contribute to the observed gait changes. Metabolic feedback has been shown to be a primary determinant of gait
parameters, with individuals generally adopting gait patterns that minimize metabolic cost [ 26]. However, when gait parameters are constrained, running behavior can differ substantially from what is predicted to reduce metabolic cost [ 27, 28, 29], indicating other sources of sensory feedback influence gait. Additionally, whole body metabolic feedback takes considerably longer to be sensed than mechanical sensory feedback. Yet, gait changes observed when switching to barefoot running are immediate, indicating that plantar mechanical feedback is a determinant of barefoot gait changes. The present study focused on shod and barefoot conditions, but different levels of cushioning in the midsole of running shoes likely influences the amount of sensory feedback transmitted to the plantar surface of the feet. In this regard, Squadrone et al. examined different running shoes models and found that the level of minimalism influences gait [ 5]. Future studies should examine the effect of different types of running shoes on plantar sensory feedback during running.
It is important to acknowledge limitations of the current study. First, was the small sample size. Due to the invasive nature of the anesthesia procedure we were only able to recruit ten participants. All attempts were made to recruit a homogenous sample, but individual differences, such as the amount of keratinization of the plantar surface of the foot, could limit statistical power. Additionally, although all participants ran in traditional running shoes, footwear did vary across participants. Further, to limit pain associated with injections we only anesthetized five locations on the plantar foot. This covered a large area, but did not achieve anesthesia of the entire plantar surface. The plantar central arch and plantar digits were not anesthetized as they have minimal ground contact, but it is possible that sensory feedback from
these areas influences gait. Additionally, minimal amounts of local anesthetic (0.1-0.3 mL) were administered in a circumferential pattern from the site of injection, but it is plausible that the mass effect of the local anesthetic in the plantar fat pad may have influenced gait.
In conclusion, our findings suggest that minimizing superficial cutaneous sensory feedback via intradermal injections of anesthetic does not alter kinematics or kinetics of barefoot or shod running. This finding suggests that sensory receptors responsible for observed differences in barefoot and shod running are located deep in the dermal layer and subcutaneous tissue, or consist of free nerve endings located in joints and the calcaneal fat pad. Future research should be aimed at utilizing deeper levels of anesthesia in order to elucidate the role of sensory feedback during barefoot and shod running.
Conflict of interest statement The authors report no conflict of interest.
Acknowledgements: We would like to thank the following undergraduate students for their assistance with the data collection for this study: Manuel Chavarria, Dusty Dasugo & Nicole DeSouchet.
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Figure 1. Representative example of vGRF and apGRF for the four running conditions.
Table 1. Stride length and velocity for BF and SHOD running in the NORM and ANEST conditions. NORM
ANEST
BF
SHOD
BF
SHOD
Stride Length (m)
2.07 (0.24)*
2.21 (0.24)*
-2.01 (0.27)*
2.15 (0.29)*
Velocity (m/s)
3.23 (0.34)
3.51 (0.37)
3.12 (0.30)
3.33 (0.37)
Mean (SD) values for preferred stride length and velocity for BF and SHOD running in the NORM and ANEST conditions. *Indicates significant difference between BF and SHOD conditions for a given sensory condition (p≤0.05). ^ Indicates significant difference between sensory conditions NORM & ANEST for a given shoe condition (p≤0.05).
Table 2 Lower extremity joint angles at ground contact and peak values. NORM
Ankle Dorsiflexion (o)
Ankle Adduction (o)
Ankle Int. Rotation (o)
Knee Flexion (o)
Knee Varus (o)
Knee Int. Rotation (o)
Hip Flexion (o)
Hip Adduction (o)
Hip Int. Rotation (o)
ANEST
BF
SHOD
BF
SHOD
Contact
-5.5 (5.1)*
7.5 (3.8)*
-3.8 (3.2)*
7.3 (4.2)*
Peak
29.9 (6.9)
28.9 (7.1)
29.1 (7.0)
30.2 (6.7)
Contact
2.2 (7.1)
-1.3 (8.0)
1.5 (8.2)
-0.9 (6.7)
Peak
7.5 (5.4)
8.4 (6.9)
8.6 (5.9)
8.0 (5.7)
Contact
-8.6 (11.5)
-9.2 (10.7)
-5.6 (10.9)
-6.8 (11.1)
Peak
4.4 (9.8)
3.1 (10.5)
6.1 (10.4)
5.8 (9.9)
Contact
6.8 (4.9)
4.1 (7.8)
5.9 (6.2)
4.8 (6.3)
Peak
35.9 (5.8)
36.1 (5.3)
33.9 (7.0)
34.8 (6.1)
Contact
6.2 (4.5)
6.1 (7.5)
5.4 (7.7)
6.1 (6.3)
Peak
18.7 (10.1)
21.3 (12.9)
19.9 (9.3)
20.7 (11.2)
Contact
-27.1 (14.5)
-29.0 (16.5)
-28.4 (12.4)
-27.9 (13.6)
Peak
2.4 (6.3)
3.9 (9.2)
4.1 (8.8)
3.4 (9.7)
Contact
34.5 (10.6)
33.9 (11.0)
35.7 (10.9)
36.1 (11.2)
Peak
35.6 (11.2)*
43.1 (10.1)*
37.8 (11.5)*
42.9 (9.4)*
Contact
6.0 (5.4)
6.1 (6.6)
5.9 (5.7)
6.0 (6.2)
Peak
13.1 (9.1)
12.6 (7.9)
13.7 (8.0)
12.8 (6.4)
Contact
21.9 (18.1)
24.6 (17.2)
25.4 (16.8)
Peak
29.4 (14.9)
33.2 (13.9)
32.4 (10.5)
Mean (SD) values for lower extremity joint angles at ground contact and peak values for BF and SHOD running in the NORM and ANEST conditions. Significant differences are indicated in bold (p≤0.05). *Indicates a significant difference between BF and SHOD conditions for a given sensory condition. ^ Indicates a significant difference between sensory conditions NORM & ANEST for a given shoe condition.
Table 3. GRFs for the BF and SHOD running in the NORM and ANEST conditions. NORM
ANEST
BF
SHOD
BF
SHOD
Impact peak (BW)
1.65 (0.22)
1.89 (0.26)
1.59 (0.25)
1.83 (0.22)
vGRF (BW)
2.19 (0.24)*
2.32 (0.19)*
2.15 (0.28)*
2.28 (0.23)*
apGRF (BW)
0.34 (0.09)
0.39 (0.08)
0.31 (0.07)
0.36 (0.09)
mlGRF (BW)
0.09 (0.07)
0.07 (0.08)
0.08 (0.09)
0.09 (0.07)
Mean (SD) values for the vGRF impact peak and peak values of the three orthogonal components of the GRF (v=vertical, ap=anterior posterior, ml=medio-lateral) for BF and SHOD running in the NORM and ANEST conditions. *Indicates significant difference between BF and SHOD conditions for a given sensory condition (p<0.05). ^ Indicates significant difference between sensory conditions NORM & ANEST for a given shoe condition (p<0.05).