Because footwear alters sensory perception, research examining the role of cutaneous feedback in barefoot running may provide important insight related to some of the gait changes that occur in patients with diabetes and others who suffer from distal symmetric peripheral neuropathy.
By Melissa Thompson, PhD, and Kristine Hoffman, DPM, FACFAS
Shod running and peripheral neuropathy are two research topics that may seem unrelated, but they do have a key element in common—sensory feedback. Several studies have indicated footwear blocks sensory feedback, resulting in gait changes in runners.1-4 Similarly, peripheral neuropathy by definition alters sensory feedback, leading to gait changes in that patient population. Emerging research on how footwear affects the gait of runners may have implications for addressing gait changes in patients with diabetes and others who suffer from peripheral neuropathy.
Peripheral neuropathy is a common disorder affecting up to 7% of the US population.5 Peripheral neuropathy can result in numerous morbidities, including severe neuropathic pain, loss of sensation, foot ulceration, Charcot neuroarthropathy, amputation, falls, fracture, increased mortality, and impaired quality of life.6 Distal symmetric polyperipheral neuropathy (DSPN) presents as numbness, paresthesias, and/or pain that typically begins at the toes and spreads proximally. DSPN can be progressive and can eventually take on a stocking-and-glove distribution. Neuropathies are the most chronic complication of diabetes, with DSPN accounting for approximately 75% of cases of diabetic neuropathy.7,8 Other etiologies of DSPN include chronic alcohol abuse, nutritional deficiency, toxins including medications and chemotherapy, genetic disorders, inflammatory conditions, other metabolic disorders, chronic infections, neoplasms, and idiopathic causes. Given its high prevalence, diabetic neuropathy is the most frequently studied type of DSPN.
The pathogenesis of developing DSPN can be multifactorial. Numerous risk factors contribute to the development of DSPN in patients with diabetes, including genetic predisposition, hyperglycemia, hyperlipidemia, hypertension, increased height, smoking, and exposure to other neurotoxic agents.9-11 The exact mechanism for development of diabetic DSPN is unknown, but several biochemical mechanisms, including the polyol pathway, advanced glycation end products, and oxidative stress, are thought to contribute. Small fiber sensory neurons are damaged first in diabetic DSPN, affecting the modalities of light touch, pain, and temperature. With prolonged hyperglycemia, further damage occurs to the large sensory nerve fibers, affecting the modalities of limb proprioception, vibration, and deep pressure. Clinically, DSPN most commonly results in loss of vibratory sensation and loss of pressure sensation, as measured with a 5.07-g monofilament.12
Neuropathy and gait
Numerous gait changes are associated with diabetic neuropathy. General gait changes seen in patients with diabetic neuropathy include reduced walking speed, reduced cadence, decreased step length, and altered acceleration patterns.13,14 With respect to walking speed, patients with diabetic peripheral neuropathy walk more slowly than healthy controls of the same age.13,15 Menz et al and Dingwell et al found that patients with loss of plantar cutaneous sensation secondary to diabetic DSPN tended to have a slower preferred walking speed.13,14
Diabetic neuropathy is associated with altered gait kinematics, reduced ankle dorsiflexion and plantar flexion, as well as reduced knee flexion and extension, seen in patients with diabetic neuropathy compared with controls.16,17 Gait kinetics are also altered in patients with diabetic peripheral neuropathy, who exhibit smaller peak plantar flexion moments than controls.18-20
Additionally, decreases in strength, as well as muscle mass, are seen in individuals with diabetic neuropathy. Specifically, reductions in ankle plantar flexion strength and knee maximal isokinetic strength have been identified in individuals with diabetic neuropathy.21,22 Muscular atrophy, beginning with the intrinsic foot muscles and progressing proximally, is thought to23 produce the muscle weakness seen in patients with diabetic neuropathy. Atrophy of the intrinsic foot musculature, in addition to compensation for sensory loss, contributes to increases in peak plantar pressure in the forefoot and midfoot seen in individuals with diabetic neuropathy.16,17,22 These increases in peak plantar pressures are a primary contributor to diabetic foot ulceration.
Similar to the gait adaptations that occur subsequent to sensory loss associated with peripheral neuropathy, sensory feedback is thought to trigger the gait alterations associated with running barefoot versus shod. Thus, barefoot running creates an interesting opportunity for further understanding the role of plantar sensory feedback in gait, as there are consistently reported gait changes that occur with barefoot running that have long been thought to be triggered by sensory feedback from the feet. Specifically, barefoot running is typically found to result in a shorter stride length than shod running, along with more frequent use of a forefoot or midfoot strike pattern rather than the rearfoot strike pattern that is common among shod runners.24 Along with these changes, we also see a reduction in peak ground reaction forces (GRFs) and vertical impact peak magnitudes, which have been proposed to have implications for injury risk.24
Footwear and sensory feedback
Robbins and colleagues were the first to address the role of plantar sensory feedback in running. In a series of studies,1-4 they analyzed the effects of footwear on plantar loading and impact-attenuating gait alterations, concluding footwear blocks sensory feedback, resulting in a failure to adopt gait modifications that limit injurious loading.
Specifically, Robbins and Hanna1 evaluated the adaptive pattern of the medial longitudinal arch following four months of barefoot weightbearing activity in habitually shod recreational runners, finding positive changes that consisted of shortening of the medial arch and load redistribution to the digits, which they associated with improved activation of the intrinsic foot musculature. Further, they speculated that cutaneous plantar sensory feedback was largely responsible for the altered activation of the foot musculature and that shoes create a “pseudo-neuropathic” condition that blocks this sensory feedback, potentially leading to running-related injury.
Further, Robbins and Gouw4 assessed plantar discomfort associated with loading that simulated locomotion, and found shoes block the discomfort associated with potentially injurious plantar loading, which subsequently results in inadequate impact-moderating behaviors and consequent injury. Similarly, Robbins, Gouw, and Hanna3 examined pain thresholds at various locations of the plantar surface of the foot, and Robbins, Hanna, and Gouw2 assessed the avoidance behaviors associated with painful loading of the plantar foot, providing evidence that sensory feedback from loading of the plantar surface likely induces mechanical alterations associated with intrinsic foot shock absorption. Although these studies provided evidence that suggested a relationship between sensory feedback and impact-attenuating gait alterations (eg, decreased stride length and change in foot strike pattern), this relationship was not systematically addressed.
Altering sensation in the lab
Currently, in vivo measurement of sensory feedback from cutaneous receptors is quite limited and not possible to assess during dynamic activities such as walking and running. An alternative approach has been to reduce or eliminate sensory feedback and examine the corresponding gait changes. Nurse and Nigg25 conducted one of the first studies to use such an approach to evaluate the role of plantar sensory feedback, using an ice immersion protocol to reduce sensation in healthy individuals. This study found minimizing sensory feedback from select areas of the foot resulted in altered plantar pressures and muscle activation patterns during walking, suggesting cutaneous sensory feedback is a key parameter in gait modification.
Although this was one of the first studies to use an anesthetization technique to evaluate the role of cutaneous sensory feedback in gait, this approach is limited in that the resulting anesthesia may not be complete, and associated cooling may potentially influence skin and muscle properties. Subsequently, researchers used intradermal anesthetization to eliminate sensory feedback and examined corresponding gait alterations.
Hohne et al26 examined the effect of plantar cutaneous sensation on plantar pressure distribution by applying intradermal anesthetic injections to the plantar foot surface in healthy individuals. They found no changes in plantar pressure distribution during walking following the reduction in plantar cutaneous sensation, which led them to suggest that peripheral sensory neuropathy, at least at a superficial level, may be not a decisive factor for altering plantar pressures. Further, a second study by Hohne et al27 examined the role of cutaneous sensory feedback on dynamic stability during walking by applying intradermal anesthetic injections to the plantar surface, finding that impaired plantar cutaneous afferent feedback does not inhibit adaptive dynamic stability alterations during walking or diminish dynamic stability following perturbation.
Additionally, a third study by Hohne et al28 reduced plantar-afferent feedback via intradermal injections and examined the corresponding alterations in gait dynamics, lower-limb kinematics, and muscle activity during walking. The results showed loss of plantar cutaneous sensation did not influence spatiotemporal variables of gait dynamics, but did lead to altered lower limb muscle activation patterns and lower limb kinematics, suggesting altered gait associated with DSPN is due to superficial sensory changes, even if those sensory changes do not affect plantar pressures or dynamic stability.
Intradermal anesthetic injections have the benefit of not affecting intrinsic foot musculature; with this methodology, only sensory feedback from peripheral sensory receptors is eliminated. However, it is possible that other sources of plantar sensory feedback influence gait, and that sensory feedback from deep cutaneous and subcutaneous sensory receptors remains intact following intradermal injections. To address this, Fiolkowski et al29 used a tibial nerve block to eliminate all sensory feedback from the feet of healthy volunteers and analyzed the corresponding changes in peak force and leg stiffness during a hopping task (a proxy for running). The tibial nerve block technique eliminated tactile sensation, as well as deep pressure sensation, and resulted in a significant decrease in leg stiffness during hopping, indicating deep plantar sensation does play a role in regulating leg mechanics during running.
In a series of recent studies,30,31 we addressed the claims that shoes block sensory receptors and that this leads to a failure to adopt the barefoot gait adaptations of decreased stride length and a forefoot or midfoot strike pattern. Specifically, we minimized sensory feedback by anesthetizing the feet to further understand the role of plantar sensory feedback during running. We did this in two studies using anesthetization techniques similar to Hohne et al26 and Fiolkowski et al.29
In the first study, we used intradermal anesthetic injections, which eliminated most of the superficial cutaneous sensory feedback from the soles of the feet. In the second, we used a tibial nerve block intervention, which eliminated all sensory feedback from the feet. We then compared participants’ barefoot gait adaptations relative to the shod condition under these anesthetized conditions. We hypothesized, based on the idea that shoes are thought to limit sensory feedback from the feet, that with the absence of sensory feedback individuals would run similar to the shod condition even when barefoot.
In our initial study30 we used intradermal injections of lidocaine to the plantar medial, central, and lateral metatarsal heads, lateral column, and heel to anesthetize the superficial plantar surface of the foot. Anesthesia was confirmed as the absence of sensation when a 10-g monofilament was pressed on the foot sole with enough pressure to buckle. Vibratory sensation (an indicator of deep sensory feedback) was evaluated with a 128-Hz tuning fork, and remained intact in all participants. In this study 10 healthy, physically active individuals completed 10 successful trials of overground running in which kinematics and kinetics were measured for each of four conditions: shod running, barefoot running, anesthetized shod running, and anesthetized barefoot running. The results showed the classic changes of decreased stride length and adoption of a forefoot or midfoot strike position at ground contact associated with barefoot running, but we did not observe any effect of anesthesia on gait. This finding indicates superficial sensory feedback from the plantar surface of the foot is not responsible for the gait alterations associated with barefoot running.
In the second study,31 11 healthy, active participants completed the same combination of normal and anesthetized barefoot/shod overground running trials as in our first study, during which kinematics and kinetics were measured. Anesthesia was confirmed as the absence of both protective sensation (evaluated by 10-g monofilament) and vibratory sensation (evaluated with the 128-Hz tuning fork). In this study, which utilized the tibial nerve block, we did see a significant effect of anesthesia, with participants maintaining a longer stride length and a rearfoot strike pattern in the anesthetized barefoot condition. Together with our findings regarding superficial sensory feedback, this indicates deep cutaneous and subcutaneous sensory receptors are responsible for the gait changes associated with barefoot running.
These insights gained from examining the role of cutaneous feedback in barefoot running may provide important insight into addressing some of the gait changes that occur in patients with DSPN. To evaluate this further, an initial aim of our future research is to examine the role of cutaneous feedback in walking instead of running. Second, we plan to examine the role of cutaneous sensory feedback in patients with DSPN by making comparisons with sensory-based alterations observed with the use of anesthetic techniques in healthy controls. Finally, we will examine the role shoes play in affecting cutaneous feedback in patients with DSPN.
Shoe gear that blocks sensory feedback from the feet and results in gait changes may be a modifiable parameter in patients with DSPN. It is clear that abnormal mechanical loading of the foot, which may be due to gait alterations, can lead to ulceration in DSPN patients.23 Loss of protective sensation puts patients with DSPN at a higher risk of ulceration, so shoe gear remains important for protecting the feet; however, modification of shoe gear and/or inserts to enhance sensation may help to improve gait in patients with DSPN. Bartold et al, for example, found modifying shoes to enhance plantar sensory feedback in the midfoot reduced plantar foot pronation compared with a neutral shoe.32 Similar shoe gear modifications may be an option to alter plantar sensory feedback and reduce injury risk in patients with DSPN.
Decreasing the gait changes associated with DSPN will lessen the morbidities associated with neuropathic gait changes, including the risk of foot ulceration and amputation.
Missy Thompson, PhD, is an assistant professor of exercise science at Fort Lewis College in Durango, CO. Kristine Hoffman, DPM, FACFAS, is an attending physician in the Department of Orthopedics at Denver Health Medical Center and an assistant professor in the Department of Orthopedics at the University of Colorado School of Medicine in Denver.
- Robbins SE, Hanna AM. Running-related injury prevention through barefoot adaptations. Med Sci Sports Exerc 1987;19(2):148-156.
- Robbins SE, Hanna AM, Gouw GJ. Overload protection: avoidance response to heavy plantar surface loading. Med Sci Sports Exerc 1988;20(1):85-92.
- Robbins SE, Gouw GJ, Hanna AM. Running-related injury prevention through innate impact-moderating behavior. Med Sci Sports Exerc 1989;21(2):130-139.
- Robbins SE, Gouw GJ. Athletic footwear: unsafe due to perceptual illusions. Med Sci Sports Exerc 1991;23(2):217-224.
- Callaghan BC, Price RS, Feldman EL. Distal symmetric polyneuropathy: a review. JAMA 2015;314(20):2172-2181.
- Ziegler D. Treatment of diabetic neuropathy and neuropathic pain: how far have we come? Diabetes care 2008;31(Suppl 2):S255-S261.
- Dyck PJ, Albers JW, Andersen H, et al. Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev 2011;27(7):620-628.
- Albers JW, Pop-Busui R. Diabetic neuropathy: mechanisms, emerging treatments, and subtypes. Curr Neurol Neurosci Rep 2014;14(8):473.
- Papanas N, Ziegler D. Risk factors and comorbidities in diabetic neuropathy: an update 2015. Rev Diabet Stud 2015;12(1-2):48-62.
- Smith AG, Singleton JR. Obesity and hyperlipidemia are risk factors for early diabetic neuropathy. J Diabet Compl 2013;27(5):436-442.
- Tavakkoly-Bazzaz J, Amoli MM, Pravica V, et al. VEGF gene polymorphism association with diabetic neuropathy. Mol Biol Rep 2010;37(7):3625-3630.
- Kanji JN, Anglin RE, Hunt DL, Panju A. Does this patient with diabetes have large-fiber peripheral neuropathy? JAMA 2010;303(15):1526-1532.
- Menz HB, Lord SR, St George R, Fitzpatrick RC. Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. Arch Phys Med Rehabil 2004;85(2):245-252.
- Dingwell JB, Cusumano JP, Sternad D, Cavanagh PR. Slower speeds in patients with diabetic neuropathy lead to improved local dynamic stability of continuous overground walking. J Biomech 2000;33(10):1269-1277.
- Dingwell JB, Cavanagh PR. Increased variability of continuous overground walking in neuropathic patients is only indirectly related to sensory loss. Gait Posture 2001;14(1):1-10.
- Hazari A, Maiya AG, Shivashankara KN, et al. Kinetics and kinematics of diabetic foot in type 2 diabetes mellitus with and without peripheral neuropathy: a systematic review and meta-analysis. Springerplus 2016;5(1):1819.
- Fernando M, Crowther R, Lazzarini P, et al. Biomechanical characteristics of peripheral diabetic neuropathy: A systematic review and meta-analysis of findings from the gait cycle, muscle activity and dynamic barefoot plantar pressure. Clin Biomech 2013;28(8):831-845.
- Yavuzer G, Yetkin I, Toruner FB, et al. Gait deviations of patients with diabetes mellitus: looking beyond peripheral neuropathy. Eura Medicophys 2006;42(2):127-133.
- Savelberg HH, Schaper NC, Willems PJ, et al. Redistribution of joint moments is associated with changed plantar pressure in diabetic polyneuropathy. BMC Musculoskelet Disord 2009;10:16.
- Sacco IC, Picon AP, Macedo DO, et al. Alterations in the lower limb joint moments precede the peripheral neuropathy diagnosis in diabetes patients. Diabetes Technol Ther 2015;17(6):405-412.
- Mueller MJ, Minor SD, Sahrmann SA, et al. Differences in the gait characteristics of patients with diabetes and peripheral neuropathy compared with age-matched controls. Phys Ther 1994;74(4):299-308.
- Andersen H. Motor dysfunction in diabetes. Diabetes Metab Res Rev 2012;28(Suppl 1):89-92.
- van Schie CH. A review of the biomechanics of the diabetic foot. Int J Low Extrem Wounds 2005;4(3):160-170.
- Altman AR, Davis IS. Barefoot running: biomechanics and implications for running injuries. Curr Sports Med Rep 2012;11(5):244-250.
- Nurse MA, Nigg BM. The effect of changes in foot sensation on plantar pressure and muscle activity. Clin Biomech 2001;16(9):719-727.
- Hohne A, Stark C, Bruggemann GP. Plantar pressure distribution in gait is not affected by targeted reduced plantar cutaneous sensation. Clin Biomech 2009;24(3):308-313.
- Hohne A, Stark C, Bruggemann GP, Arampatzis A. Effects of reduced plantar cutaneous afferent feedback on locomotor adjustments in dynamic stability during perturbed walking. J Biomech 2011;44(12):2194-2200.
- Hohne A, Ali S, Stark C, Bruggemann GP. Reduced plantar cutaneous sensation modifies gait dynamics, lower-limb kinematics and muscle activity during walking. Eur J Appl Physiol 2012;112(11):3829-3838.
- Fiolkowski P, Bishop M, Brunt D, Williams B. Plantar feedback contributes to the regulation of leg stiffness. Clin Biomech 2005;20(9):952-958.
- Thompson MA, Hoffman KM. Superficial plantar cutaneous sensation does not trigger barefoot running adaptations. Gait Posture 2017;57:305-309.
- Thompson M.; Hoffman K. Cutaneous sensory feedback is a primary determinant of gait changes observed in barefoot running. Presented at American Society of Biomechanics Annual Meeting; August 2-5, 2016, Raleigh, NC.
- Bartold S, Bryant A, Clark R, et al. Acute effects of a shoe with enhanced plantar sensory feed back on midfoot kinematics whilst walking. J Footwear Science 2011;3(Suppl 1):S7-S8.