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Diabetes Special Issue |
MJ Mueller, PT, PhD, FAPTA, is Associate Professor, Program in Physical Therapy and Department of Radiology, Washington University School of Medicine, Campus Box 8502, 4444 Forest Park Blvd, St Louis, MO 63108 (USA).
D Zou, DSc, is Assistant Professor, Program in Physical Therapy and Department of Radiology, Washington University School of Medicine.
KL Bohnert, MS, CDT, is Research Patient Coordinator, Program in Physical Therapy, Washington University School of Medicine.
LJ Tuttle, PT, is a doctoral student, Movement Science Program, Program in Physical Therapy, Washington University School of Medicine.
DR Sinacore, PT, PhD, FAPTA, is Associate Professor, Department of Medicine and Program in Physical Therapy, and Director, Applied Kinesiology Laboratory, Washington University School of Medicine.
Address all correspondence to Dr Mueller at: muellerm{at}wustl.edu
Submitted January 10, 2008;
Accepted March 28, 2008
 | Abstract |
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Subjects: Twenty-four subjects participated: 12 with diabetes mellitus, peripheral neuropathy, and a plantar ulcer (DM+PN group) and 12 with no history of diabetes mellitus or peripheral neuropathy (control group). The subjects (11 men, 13 women) had a mean age (±SD) of 54±8 years.
Methods: Plantar pressures were measured during barefoot walking using a pressure platform. Stress variables were estimated at the forefoot and the rear foot for all subjects.
Results: All stress variables were higher (127%–871%) in the forefoot than in the rear foot, and the peak pressure gradient showed the greatest difference (538%–871%). All stress variables were higher in the forefoot in the DM+PN group compared with the control group (34%–85%), and the peak pressure gradient showed the greatest difference (85%). The depth (
±SD) of peak maximum subsurface shear stress in the forefoot in the DM+PN group was half that in the control group (3.8±2.0 versus 8.0±4.3 mm, respectively).
Discussion and Conclusions: These results indicate that stresses are relatively higher and located closer to the skin surface in locations where skin breakdown is most likely to occur. These stress variables may have additional value in predicting skin injury over the traditionally measured peak plantar pressure, but prospective studies using these variables to predict ulcer risk are needed to test this hypothesis.
| Introduction |
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 TopAbstract Introduction MethodResultsDiscussionConclusionReferences |
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Even if the perspective is narrowed to physical stresses alone, there are several characteristics of physical stresses that could contribute to skin injury and breakdown. Using the Physical Stress Theory as a theoretical background,6 the key stress variables that contribute to skin injury on the plantar surface of the foot would include the magnitude, time, and direction of stresses. The magnitude of stress is characterized as the peak plantar pressure (PPP) during barefoot and shod walking and has been studied extensively in this population.2,7–9 Time factors include the duration of the pressure applications (pressure-time impulse10–12), the number of pressure applications (often characterized as the number of steps taken12,13) and the rate of pressure application (not well studied). The primary directions of stress application generally are thought of as perpendicular or parallel to the skin surface. Stresses applied perpendicular to the skin are measured using a number of commercially available sensors, but stresses measured parallel to the skin surface (shear stresses) are challenging to measure14 and devices providing established and credible measures are not yet commercially available. Given the number of variables and activities that can influence the skin (eg, walking, stair climbing, footwear); these stresses could combine in an almost infinite number of ways to cause skin injury. Because of the number of mechanical and physiological factors that can combine to cause skin injury and despite a clear association between PPP and location of skin breakdown, a specific threshold of any given stress variable that predicts skin breakdown with good sensitivity and specificity has not been identified.15 Additional research is needed to identify the optimal stress characteristics to predict and understand skin injury.
Surface skin pressures generate shear stresses inside the soft tissue of the plantar surface of the foot that contribute to tissue damage. These subsurface shear stresses are caused, in part, by the uneven distribution of stresses across the skin surface. They can be caused by uneven perpendicular forces and are different from traditionally recognized shear stresses that are generated by parallel forces along the surface of the skin. The magnitude and depth of these subsurface shear stresses can be estimated using mechanical laws and theories.16 We have used the pressure distribution on the surface of the skin to estimate the peak maximum shear stress (PMSS) and the depth of the PMSS (D_PMSS) using the potential functions H(x, y, z) and H1(x, y, z) (harmonic functions satisfying Laplace's equation) by Hook's law assuming small-strain, small-deformation theory of elasticity at any point within the body.16 First, the maximum shear stress is estimated for every level (millimeter) of subsurface tissue within the region of interest. Then, the magnitude of the maximum shear stress is compared among the various levels of tissue. The greatest magnitude of the maximum shear stress compared across all levels is considered the PMSS.16
The spatial change in pressure across the surface of the skin appears to be an important component of predicting these subsurface shear stresses. We previously defined the peak pressure gradient (PPG) as the greatest spatial change in plantar pressure around the PPP location.17 The location of PPP is identified, and then the spatial change in plantar pressure is determined for every direction around the PPP location. The greatest spatial change in plantar pressure (ie, the greatest slope of the pressure distribution) is the PPG. Based on mechanical theories,18 we believe pressures that change substantially across the surface of skin (ie, high PPG) are more damaging than high pressures distributed equally across the skin surface. For example, the hydrostatic pressures experienced by the skin of deep-sea divers may be very high, but divers do not experience skin breakdown because these high pressures are distributed evenly across the surface of the skin (ie, they have a very low PPG). The relationship among various magnitudes of PPG and the resultant calculated PMSS is illustrated in Figure 1 using methods previously reported.16 In this theoretical illustration, PMSS increases as the PPG increases.
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The primary purpose of this study was to determine the differences in indicators of skin breakdown (PPP, PPG, PMSS, and D_PMSS) between the forefoot and the rear foot in subjects with and without diabetes mellitus, peripheral neuropathy, and a plantar ulcer measured during barefoot walking. A secondary purpose was to determine the correlations among these variables. We hypothesized that values would be greater in the forefoot than in the rear foot and greater in the subjects with diabetes mellitus, peripheral neuropathy, and a plantar ulcer than in the comparison group. Furthermore, we speculated, based on mechanical failure theory, that the subjects with skin breakdown would show high values of PMSS that were located close to the skin surface (low D_PMSS values) compared with those without skin breakdown.
| Method |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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The control group was selected from a sample of convenience. The control group was matched on age, weight, and sex with the DM+PN group. All subjects signed a consent form approved by the Human Research Protection Office of Washington University School of Medicine. Subject characteristics are shown in Table 1.
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±SD) was 68.4±20.7 m/min for the control group and 57.1±17.7 m/min for the DM+PN group (no significant difference, P>.05). Each walking trial yielded a single plantar map (step). The 3-dimensional stress components, the principal stresses, and shear stresses in the subsurface tissues were calculated from the measured pressure at the PPP time frame of each gait cycle for the forefoot and the rear foot.16 Each plantar map was divided (ie, masked) into forefoot and rear foot regions at 50% of the length of the foot. After masking the plantar map, the magnitude of the PPP was averaged over 3 trial steps in each mask and summarized using Groupmask evaluation software.* The PPG, PMSS, and D_PMSS for each area of interest also were calculated from pressure data averaged over 3 steps during walking.24,25
Custom-written software used the pressure distribution data collected by the EMED system to estimate the PMSS and D_PMSS and to calculate PPG on the forefoot and rear foot of one foot of each subject. The PPG was defined as the maximal spatial change (ie, greatest slope) in surface pressure located around the PPP.17 The PPG at the location of the PPP was calculated after a bicubic polynomial spline smoothing of the pressure data. The PPG was determined in a defined area (3x3 sensor pixels, 450 mm2) on nodes (spacing equal to half the length of the sensor pixel), which were generated using the bicubic polynomial spline function. The PPG around the PPP was calculated as the highest change in pressure (pressure gradient) from one node (half pixel apart) to the next node according to rows and to columns and by diagonal.17
The PMSS and D_PMSS were estimated using potential functions and by Hook's law assuming small strain and small deformation theory of elasticity.16 The maximum shear stress was estimated for every level (millimeter) of tissue within the region of interest. Then, the magnitude of the maximum shear stress was compared among all levels of tissue. The greatest magnitude of the maximum shear stress compared across all subsurface levels was considered the PMSS. The D_PMSS was the depth below the skin surface of this value.16
Data Analysis
A group (DM+PN versus control) x location (forefoot versus rear foot) analysis of variance (ANOVA) was performed for each of the dependent variables (PPP, PPG, PMSS, and D_PMSS). Individual post hoc t tests were performed on each of the significant group and location comparisons. In addition, PMSS was plotted on the vertical axis and D_PMSS was plotted on the horizontal axis of a graph for all subjects to help determine whether particular values were associated with skin breakdown. Pearson product moment correlations with a Bonferroni correction were used to determine simple correlations among variables for all subjects.
| Results |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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±SD) were closer to the skin surface in the forefoot (3.8±2.0–8.0±4.3 mm) than the rear foot (12.5±3.3 mm), but especially in the DM+PN group (3.8±2.0 mm, significant group x location interaction, P<.05).
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Figure 2 presents the PMSS values plotted against the D_PMSS values for the forefoot and rear foot of both groups. The PMSS values generally were higher and located much closer to the surface of the skin in the feet with a plantar ulcer in the DM+PN group compared with all other locations. The forefeet of the subjects without skin breakdown had relatively low PMSS values (75–250 kPa) and a wide range of D_PMSS values (3–14 mm). Conversely, those subjects with skin breakdown had relatively high values of PMSS (150–325 kPa) that were concentrated in low soft tissue depths (3–4 mm). Rear foot values tended to group in the lower right-hand corner of the graph, where PMSS values were relatively low (25–125 kPa) and D_PMSS values were relatively high (9–18 mm).
Correlations among the stress variables were high in the forefoot (r= –.73 to .96, P<.05, Tab. 2). The highest correlation was between PMSS and PPP values (r=.96). There were high, inverse correlations among PPP, PPG, PMSS, and D_PMSS values (r=–.73 to –.87), indicating that high values of stress variables were associated with low values of D_PMSS (ie, high stress values were located close to the skin surface). All correlations among variables were lower in the rear foot compared with the forefoot (Tab. 2).
| Discussion |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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High stress values occur in the rear foot and forefoot at heel-strike and push-off, respectively, because body-weight forces are focused on a relatively small area of the foot compared with forces during mid-stance, when the entire foot is in contact with the ground. The forefoot-to-rear foot comparison is important because most neuropathic ulcers in people with diabetes occur in the forefoot, despite both areas experiencing relatively high stresses.20,21 In our study, all stress variables were higher in the forefoot than in the rear foot (Tab. 2). The PPP values were 2.3 to 2.6 times greater in the forefoot than in the rear foot, which is essentially identical to the results reported by Caselli et al21 (PPP values [±SD] were 2.3±2.4 times higher in the forefoot than in the rear foot in a group of subjects with diabetes mellitus and peripheral neuropathy). In our study, forefoot-to-rear foot pressure gradient comparisons were more dramatic than other comparisons; the PPG values were 6.4 to 8.7 times greater in the forefoot than in the rear foot (Tab. 2).
There are a number of reasons why the forefoot may experience higher stress values than the rear foot. First, soft tissue thickness is about 36% to 48% greater in the rear foot than in the forefoot.26 Soft tissue clearly plays an important role in stress distribution, and the thicker tissue under the rear foot compared with the forefoot may help to distribute stresses evenly to the underlying bony structures. A second reason that stresses may be less in the rear foot compared with the forefoot is the relatively large, rounded surface beneath the calcaneus compared with the smaller circumference of the metatarsal heads in the forefoot (Fig. 3). It appears that the thicker soft tissue envelope is better able to distribute stresses to the broader area beneath the calcaneus compared with the thinner soft tissue and small area beneath the metatarsal heads in the forefoot. People without diabetes mellitus and peripheral neuropathy experience high forefoot stresses; however, they do not experience plantar skin breakdown. The baseline pathophysiological impairment that allows skin breakdown is peripheral neuropathy.1 People with intact sensation are able to sense high pressures and pain and to adjust their weight-bearing activities accordingly to avoid continued trauma and injury.
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Figure 3 illustrates part of the reason why forefoot stresses were higher in the DM+PN group than in the control group. As illustrated in the figure, people with diabetes mellitus and peripheral neuropathy have a high incidence of hammer-toe deformity (hyperextension of the metatarsophalangeal joint) that is associated with high plantar pressures27–29 and skin breakdown.30,31 Hammer-toe deformity reduces the ability of the toes to share weight-bearing stresses during walking and increases stresses under the metatarsal head, where most ulcers are located. Although the precise reason for the hammer-toe deformity is not known, weakness and atrophy in the intrinsic muscles of the foot from peripheral neuropathy are thought to contribute.32 For further discussion of the muscle and bone changes secondary to peripheral neuropathy, see the articles by Hilton et al33 and Sinacore et al34 in this issue. Other factors besides intrinsic muscle weakness must contribute to the hammer-toe deformity, however, because not all people with intrinsic muscle weakness develop hammer toe deformity.35 Soft tissue thickness is known to be inversely correlated with plantar pressures under the metatarsal heads.28,36 Although some people with diabetes mellitus and peripheral neuropathy may have reduced soft tissue thickness,26 these changes may be subtle and are not universally seen across all people in this group.32
All of the stress variables reported in this article were highly correlated (r=.73–.96), and it is not yet explicitly clear what additional value PPG, PMSS, or D_PMSS have over the traditionally used PPP to predict tissue injury. Because of the larger group differences and because the PPG is linked to subsurface shear stresses (Fig. 1) and intuitively linked to injury, we believe the PPG may be a more sensitive indicator of injury risk than the PPP. Additional prospective studies, similar to that conducted by Armstrong et al,15 need to be conducted to determine whether these stress variables are more sensitive and specific to predicting skin breakdown than PPP alone.
The results reported in this article are consistent with results from previous recent studies (Tab. 3),16,19 despite using a different pressure testing method (EMED versus F-Scan In-shoe Pressure System,
which have different numbers and spatial resolution of sensors) and different footwear conditions (barefoot versus shod). Data consistently show that people with diabetes mellitus and peripheral neuropathy have higher PPP, PPG, and PMSS values that are closer to the surface of the skin compared with control subjects. However, all of these stress variables in the forefoot were at least double in the barefoot condition in our study compared with previous reports that included data collected only in a shod condition (Tab. 3). This difference provides support for the importance of footwear to mitigate stress factors that may lead to skin breakdown in this population. People with diabetes mellitus and peripheral neuropathy are encouraged to wear shoes at all times, even during household ambulation, to protect their feet from unnoticed injury.37 See the related article in this issue by LeMaster et al,38 who conducted a randomized controlled clinical trial to determine whether people with diabetes mellitus and peripheral neuropathy can increase their walking tolerance without an increased incidence of skin breakdown.
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Another limitation of this study was that we did not include groups with only diabetes mellitus, only peripheral neuropathy, or diabetes mellitus and peripheral neuropathy but no history of a neuropathic ulcer. Therefore, we do not know for certain the individual contributions from diabetes mellitus or peripheral neuropathy. We included only the group with diabetes mellitus and peripheral neuropathy and a history of a plantar ulcer, however, because our previous work did not find substantial differences between subjects with diabetes mellitus and peripheral neuropathy and subjects without disease.19 In addition, it was not the purpose of the current study to attribute changes in stress values to each of these specific pathologies.
Finally, weight (±SD) was greater (105±24 versus 92±12 kg) and walking speed (±SD) was lower (57±18 versus 68±21 m/min) in the DM+PN group compared with the control group. We do not believe, however, that these differences had a substantial impact on the results because the differences were not statistically significant (P>.05) and, although the greater weight may have driven the stress values up in the DM+PN group, the slower walking speed would have tended to drive the stress values down compared with the control group.40
Despite the limitations noted above, there are several important implications for clinical practice from this work. We believe the most important implication of this work, and of other studies showing similar connections between high stresses and skin breakdown,1–3 is the need for appropriate footwear and orthotic devices to minimize excessively high stresses for people who are at risk for skin breakdown. The American Diabetes Association currently recommends that people with diabetes mellitus and peripheral neuropathy and "with evidence of increased plantar pressure (eg, erythema, warmth, callus, measured pressure) should use footwear that cushions and redistributes the pressure."37
As shown by the results in Table 3, therapeutic shoes alone can dramatically reduce plantar pressures compared with walking barefoot. Athletic shoes or good walking shoes provide comparable stress reductions41 and often are more cosmetically acceptable to patients than traditional therapeutic shoes. Several studies have shown that viscoelastic insoles41 or total-contact inserts 42–44 provide additional pressure reduction compared with footwear alone. Metatarsal pads can reduce pressures even beyond a total-contact insert, but pad size, material properties, and placement make accurate management with metatarsal pads challenging.42 Finite element analysis is a promising technology that is being used to help design orthotic devices to evenly distribute plantar pressures.39,45,46 Clearly, the integumentary system (ie, the skin) provides an outstanding soft tissue envelope around the foot to help distribute excessive plantar stresses. In the presence of impairments such as insensitivity, foot deformity, or reduced soft tissue thickness, extrinsic devices such as shoes and orthotic devices can be used to compensate for these impairments and help distribute excessive plantar stresses. Additional research is needed to develop and test footwear and orthotic algorithms that will help prevent skin breakdown in this population at high risk for skin breakdown and subsequent infection and amputation.
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| Footnotes |
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This study was approved by the Human Research Protection Office of Washington University School of Medicine.
The authors acknowledge funding from the National Institutes of Health National Center for Medical Rehabilitation Research (grants RO1 HD36895 and T32 HD007434 to Dr Mueller) and National Institute of Diabetes and Digestive and Kidney Diseases (grant RO1 DK 59224 to Dr Sinacore) and a Foundation for Physical Therapy Promotion of Doctoral Studies I grant to Ms Tuttle. The authors thank Paul Commean for generating Figure 3 used in this study.
A poster presentation of this work was given at the Combined Sections Meeting of the American Physical Association; February 6–9, 2008; Nashville, Tenn.
* Novel Electronics Inc, 964 Grand Ave, St Paul, MN 55105. 
Tekscan Inc, 307 W First St, South Boston, MA 02127.
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