The current study reports a simple objective method to characterize asymmetry in plantar temperature as a function of graduated walking activity. This technique characterizes the PT hot spot (95th percentile) at each plantar region instead of manual comparison of plantar temperature between two feet.
We found that all participants experienced initial temperature decrease in both feet after 50 steps. But the slope of PT cooling to baseline was significantly slower in the affected foot. Consequently, the temperature difference between CN affected and contralateral foot is magnified after walking 50 steps (d = 1.20 and r = 0.52 at baseline versusd = 1.94 and r = 0.70 at 50 steps).
The initial drop in plantar temperature in early-walking steps may be due to regulation of microvascular flow in response to cyclic loading and relaxation. Silver-Thorn [26
] by applying a cyclic loading and unloading to human healthy tissue demonstrated that skin perfusion is initially increased in response to early loading and dropped with further increases in pressure or prolong loading till reaching to a steady-state level (first pulse response). Then, again it is increased followed by decreasing to the initial value in response to unloading (second pulse response or hyperemia response), whereas little to no tissue reperfusion was observed during prolong relaxation period without cyclic stress. Therefore, cyclic activities like walking may actually increase the cumulative plantar skin perfusion as a function of time (or time integral) compared to prolong relaxing (e.g., sitting, lying, and offloading) or prolong loading (e.g., standing) conditions. Thus, this skin perfusion regulation in response to cyclic stress may explain the initial drop in plantar temperature in early steps compared to baseline (relaxation) for healthy skin when other factors contributing to increase in skin temperature (e.g., friction, metabolic cost, etc.) are still negligible. Considering that the most of walking episodes are short (often less than 50 steps per episode) [27
], this regulation mechanism is of key importance in regulating foot temperature during activity of daily living. A failure in the above-explained skin perfusion regulation in response to cyclic plantar stress may explain the lack of drop in temperature in the CN-affected foot.
In non-CN, the temperature remained the same after continued activity from 50 steps up to 200 steps, but temperature was lower relative to the temperature at baseline. In CN, there was, however, a significant increase in temperature at 200 steps compared to 50, significantly higher than temperature difference between 50 and 200 steps in non-CN. These interesting findings merit further study as a potential stress test for prediction of unilateral or bilateral CN and subsequent ulcer development.
The sharp increase in plantar temperature in CN group after continued activity beyond 50 steps could be explained by a complex interplay between local metabolic status [28
], propensity for an ill-defined inflammatory overreaction [5
], perfusion status [30
], the physical state of plantar tissue, and limited joint mobility which may increase skin friction or metabolic cost. There could be an empiric support for these findings from Johnson, who reported a sharp increase in plantar temperature in Charcot patients and postulated that it could be explained by hyperemia in Charcot foot [31
]. According to Boulton et al., “It has been theorized that the site of pathology was within the arteriovenous shunts, which normally are under control of the sympathetic system. Loss of this function will result in blood being routed rapidly to the venous side of the capillary bed, increasing the local pO2, thereby decreasing the distal perfusion to the cells” [32
]. These results also support that modulating duration of continuous steps and/or prolong standing during daily activity could be helpful for reducing the trauma in patients with CN or DFU [27
The temperature differences in our study differ from others at baseline [15
]. This could be due to the duration of acclimatization, use of a thermal imager as opposed to an infrared dermal thermometer, and aggregation of temperature into regions of the foot as opposed to manual point testing. Additionally, we have eliminated any bias towards absolute temperature measurements by using the 95th percentile values.
This study has few limitations. First, we were not able to control the stage of Charcot foot development. It is likely that some patients were in a coalescence phase. The magnitude of the differences between groups merit further investigation in stages 0 and 1 patients. It is entirely plausible that these patients are likely to have a higher thermal gradient. Second, we did not standardize the offloading footwear and, while our population was easily robust enough to assess temperature gradient, it was not sufficiently powered to perform a stratified analysis by stage and offloading footwear type. Third, due to limitations in technology, a short delay was required for assessing plantar temperature after each walking path. However, since the change in plantar temperature is not rapid, we assumed that the effect of this delay (approximately 30 seconds) for assessing change in plantar temperature as a function of walking is negligible. Another study should be addressed to validate this hypothesis.
The observed differential thermal response to walking initiation between Charcot and non-Charcot feet warrants future investigation to provide further insight into the correlation between activity dosing and thermal response. It may also lend valuable insight into identifying an “inflammatory trigger” that may ultimately provide an early-warning sign [36
] or increased sensitivity for subsequent unilateral or bilateral CN development or clinical expression of foot ulcer. The importance of improved sensitivity and earlier diagnoses of CN was recently described by Wukich and colleagues. In their retrospective review of 22 CN patients, they emphasized the importance of identifying and aggressively treating stage 0 patients [6
]. This was defined as patients with diabetes-related sensory neuropathy presenting following foot and ankle insult with local swelling, redness, and warmth and radiographic signs absent for fracture and normal alignment [37
]. The group that was identified and treated for 4 weeks developed significantly less complications (14%) versus the group that was identified and treated after 8 weeks (67%) [6
In conclusion, the variability in thermal response to the initiation of walking between Charcot and non-Charcot feet warrants future investigation to potentially provide further insight into the correlation between thermal response and ulcer/Charcot development.