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Relationship Between Changes in Activity and Plantar Ulcer Recurrence in a Patient With Diabetes Mellitus

DJ Lott, PT, MSPT, CSCS, is Doctoral Candidate, Movement Science Program, Washington University, St Louis, Mo
KS Maluf, PT, PhD, is Post-Doctoral Research Associate, Department of Integrative Physiology, University of Colorado, Boulder, Colo
DR Sinacore, PT, PhD, is Associate Professor, Program in Physical Therapy and Department of Internal Medicine, Washington University School of Medicine, St Louis, Mo
MJ Mueller, PT, PhD, FAPTA, is Associate Professor, Program in Physical Therapy, Washington University School of Medicine
Dr Maluf and Dr Mueller provided concept/idea/project design. All authors provided writing. Dr Maluf and Dr Sinacore provided data collection, and Dr Maluf provided data analysis. Dr Sinacore provided the patient. Dr Mueller provided facilities/equipment. Dr Maluf, Dr Sinacore, and Dr Mueller provided consultation (including review of manuscript before submission)

Address all correspondence to Mr Lott at Program in Physical Therapy, Washington University, Campus Box 8502, 4444 Forest Park Blvd, St Louis, MO 63108-2212 (USA) (Djlott{at}artsci.wustl.edu)

Submitted April 6, 2004; Accepted October 12, 2004

	Abstract

 
Background and Purpose. Although pressure-reducing interventions have been effective in the healing of neuropathic foot ulcers, these ulcers frequently recur in people with diabetes mellitus (DM). This case report illustrates how sudden changes in weight-bearing activity may have affected ulcer recurrence in a patient with DM and how the physical stress theory (PST) relates to ulcer recurrence for this patient. Case Description. The patient was a 66-year-old man with a history of DM, peripheral neuropathy, and recurrent plantar ulcers. His plantar ulcer healed after total contact casting. Outcome. Despite relatively low peak plantar pressure (9.3 N/cm²), the patient's ulcer recurred within 4 weeks of healing. Plantar pressure assessment and activity monitoring suggested that a rapid and sudden increase in weight-bearing activity (steps per day) contributed to cumulative plantar tissue stress that was 3.3 times higher on the day of ulcer recurrence than his average value. Although his cumulative plantar stress was high compared with his usual value, the cumulative value was similar to the amount of daily stress of individuals without a history of recurrent ulcers. Discussion. Within the context of the PST, rapid change in activity level may have an effect on cumulative stress and the risk of ulcer recurrence.

Key Words: Diabetes mellitus • Foot • Stress • Ulcer

	Introduction

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Foot complications of diabetes account for 20% of all hospital admissions of people with diabetes mellitus (DM),¹ and they have 15 times greater risk of lower-extremity amputation than people without DM.² Diabetes mellitus is the leading cause of nontraumatic lower-extremity amputations in the United States,³ and the American Diabetes Association has estimated that up to 85% of these amputations can be prevented.⁴ Fifteen percent of people with DM will develop at least one foot ulcer during their lifetime,¹ and 24% of people with a foot ulcer will require an amputation.³ Although current interventions have been effective in healing foot ulcers, most plantar ulcers recur within 6 months of initial healing, with the greatest risk of injury in the first 3 to 4 weeks.⁵ Ulcer recurrence rates after healing are 34%, 61%, and 70% after 1, 3, and 5 years, respectively,^6,7 We believe that current strategies for managing plantar ulcers focus on reducing peak pressure, with little consideration given to other factors (eg, weight-bearing activity) that impose stress on the foot and may contribute to ulcer recurrence.

The physical stress theory (PST) considers multiple factors that contribute to tissue stress and is based on fundamental principles that appear to govern the adaptive response of biological tissues to stress.⁸ Physical therapists can apply this theory to guide patient care, education, and research, and it focuses on the tissues of the organ systems identified as most relevant to physical therapists in the Guide to Physical Therapist Practice (ie, cardiovascular/pulmonary, integumentary, musculoskeletal, and neuromuscular systems).⁹

The basic premise for the PST is that changes in the relative level of physical stress cause a predictable adaptive response in all biological tissue.⁸ Each of these adaptive responses is predicted to occur within a defined range along a continuum of stress levels. Specific thresholds define the upper and lower stress levels for each characteristic tissue response. The 5 qualitative responses to physical stress are decreased stress tolerance (eg, atrophy), maintenance (no apparent tissue change), increased stress tolerance (eg, hypertrophy), injury, and death. The PST recognizes that the stress thresholds required to achieve a given tissue response may vary among individuals depending on the presence or absence of several factors, and it includes consideration of these factors for managing patients and for understanding mechanisms of injury to biological tissue. The 4 main categories of these factors that affect the level of physical stress on injured tissue are: physiological factors, psychosocial factors, movement and alignment factors, and extrinsic factors. Once a clinician identifies these factors, he or she can decide on an appropriate intervention to modify these factors to decrease the stress on the injured tissue to enable the tissue to heal.

The purposes of this case report are: (1) to describe how rapid and sudden changes in weight-bearing activity may have contributed to excessive physical stress and ulcer recurrence in a patient with DM, (2) to suggest that activity monitoring to estimate cumulative stress may be a useful adjunct to existing methods for intervention and prevention of plantar ulcers in patients with DM, and (3) to describe how the PST relates to the ulcer recurrence in a patient with DM with a history of recurrent plantar ulcers.

	Case Description

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Patient Description

The patient was a 66-year-old Caucasian man with a history of DM for 16 years who had been referred for physical therapy by his orthopedic surgeon. His height was 1.80 m, and his weight was 121.5 kg. The patient reported that the current plantar ulcer had been present for 18 months. The patient had a history of 2 previous foot ulcers in the past 4 years, both located in the same region of the left midfoot, which had been successfully managed with total contact casting (TCC). The patient's self-reported medical history included DM, hypertension, and a history of recurrent foot ulcers. He reported walking barefoot only when taking a shower and said that his wife inspected his feet on a daily basis. Physiological factors that affected the level of physical stress to the plantar foot of this patient were his age (66 years), systemic pathology (eg, DM, hypertension, peripheral neuropathy), and obesity (body mass index=37.5 kg/m²).⁸

The patient's main complaint was the presence of the ulcer, and his goal was to heal the ulcer. He also reported having a desire to return to work as quickly as possible and to be able to return to his hobby of attending fairs. The patient's occupation was part-time bus driver for the local public school district. His desire to return to his work and to participate in community activities (eg, attending fairs) was identified as a psychosocial factor. The patient described his overall activity level as low, and he stated that he was fairly sedentary and often used a motorized scooter for mobility instead of walking. His low activity level was identified as a movement factor.

Examination

The patient had mild edema in the distal lower extremities. To determine the size of the wound, the physical therapist placed a sterilized clear plastic film¹⁰ on the plantar aspect of the foot covering the wound. Information on the reliability of data for measures used in this case is contained in the Table.^11–18 The therapist traced on the plastic film along the outer edge of the wound. This wound tracing measured 35 mm long x 21 mm wide x 4 mm deep (Fig. 1). After sharp debridement of necrotic tissue, the wound bed showed good granulation.

View larger version (106K): [in this window] [in a new window]   Figure 1. Initial plantar ulcer at left midfoot area measuring 35 mm long x 21 mm wide x 4 mm deep.

Regarding vascular testing, the dorsalis pedis artery pulse was palpable bilaterally; however, the posterior tibial pulse could not be palpated on either foot. The patient's ankle-brachial index (ABI) was assessed with a Doppler probe to measure the systolic blood pressure in the brachial and dorsalis pedis arteries while he was in a supine position. His ABI was 0.87, indicating a mild impairment in lower-extremity circulation.²⁰ The patient's glycosylated hemoglobin was 5.6%, indicating good control of his blood glucose level.

Inspection of the left foot revealed callus formation at the lateral midfoot, nail mycosis, absent hair growth, and an absent toenail at the second digit. Foot deformities included a plantar-flexed first ray and hammertoe deformity of the second through fourth digits bilaterally. Additional deformities present on the left foot included a bunion, hallux valgus, and a prominent bulge at the medial midfoot (Fig. 1). This prominence was hard and bony to touch. The plantar surface of the left foot was convex in appearance (Fig. 2). Goniometric measurements demonstrated that range of motion (ROM) for the distal lower extremities was not impaired except for limited (<30°) great toe extension on the left and the aforementioned deformed toes.

View larger version (100K): [in this window] [in a new window]   Figure 2. Medial view of patient's left foot demonstrating convexity of plantar surface.

View larger version (114K): [in this window] [in a new window]   Figure 3. Patient's custom-made, clamshell, polypropylene ankle-foot orthosis lined with 1.27 cm (0.5 in) of no. 1 Plastazote for pressure relief.

	Intervention

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According to the PST, the primary 2 questions to ask in an evaluation and the management of a patient with tissue injury are: (1) What factors appear to be contributing to excessive stress on the injured tissue? and (2) How can these contributing factors be modified to reduce stress in the tissue and allow the tissue to heal? Using the results of the patient examination to answer these 2 questions, we decided to use TCC to decrease the amount of excessive stress to the plantar surface of the foot that presumably caused the foot ulcer. Total contact casting is described in detail elsewhere.^21,22 In brief, TCC consisted of a series of casts applied to the distal lower extremity. The ulcer was covered with a thin layer of gauze. A stockinette was then applied from the knee to the toes, and small (0.32-cm) felt pads were placed at the malleoli and the anterior aspect of the tibia. A foam pad also was placed about the toes. Then a total contact plaster shell was molded around the lower leg. A walking heel was attached to the plantar surface, and the shell was reinforced with plaster splints. The patient was instructed to not bear any weight through the involved lower extremity for the first 24 hours of TCC. The patient was told that he could walk after the first 24 hours without any weight-bearing restrictions.

To quantify the number of repetitions of stress exposure to the plantar surface of the foot from walking, the patient wore an activity monitor (Step Activity Monitor [SAM] for 2 weeks during intervention with TCC. The SAM is an accelerometer that assesses activity level by recording the number of strides (heel-strike of one foot to heel-strike of the same foot for the next successive step) taken per 24 hours for up to 15 consecutive days. The SAM weighs 65 g and has dimensions of 6.5 x 5.0 cm. Unlike waist-worn pedometers, the SAM is worn just superior to the ankle and is attached by 2 straps to the distal lower leg. Studies investigating the accuracy of the SAM have demonstrated this device to have a mean absolute error of only 0.5% for individuals with obesity¹⁶ and 0.31% for individuals with DM or lower-limb amputation.²³ More recent work has shown the SAM to yield reliable data for subjects with TCC¹⁷ (Table). The patient was asked to wear the SAM during all waking hours.

The patient returned to our clinic every 7 to 14 days to have the cast removed and reapplied. After 56 days of TCC, the patient's ulcer decreased in size to 10 mm long x 4 mm wide x 4 mm deep. After 63 days of TCC, the ulcer had full epithelization and no drainage (Fig. 4). We then decided to discontinue the use of TCC due to the tissue healing at the site of ulceration. The patient was instructed to ambulate using his clamshell AFO to avoid excessive stress on the newly healed tissues of the plantar surface of the foot while awaiting insurance authorization for therapeutic footwear. This prescribed footwear also included custom-made total contact inserts.

View larger version (92K): [in this window] [in a new window]   Figure 4. Healed left midfoot after 63 days of total contact casting.

Following pressure testing, the patient agreed to wear the SAM as he had previously done during TCC. This second monitoring of the patient's activity would enable us to assess changes in the amount of weight-bearing activity after TCC relative to the SAM data recorded during TCC.

Activity monitoring during TCC indicated that the patient had been relatively inactive while wearing the cast (1,387±649 strides per day averaged over 14 days of activity monitoring). Approximately 3 weeks after the wound had healed and TCC had been discontinued, the patient had a recurrence of his midfoot ulcer while wearing the SAM (Fig. 5). The patient reported that he had been more active than usual on the day of ulceration because he attended a county fair, but he stated that he had worn his AFO to reduce the amount of pressure on his feet while walking. The patient stated that he became aware of the tissue breakdown that evening when he noticed blood on his sock.

View larger version (111K): [in this window] [in a new window]   Figure 5. Reulceration of left midfoot area approximately 3 weeks after ulcer healing had occurred.

Intensity of weight-bearing activity (the number of strides the patient took per minute) also was determined for the second period of activity monitoring. Custom-made software was written to calculate the number of minutes per 24-hour period that the patient spent at different intensities of weight-bearing activity.²⁴ The average amount of time spent performing activities of increasing intensity was plotted for days 1, 2, 4, 5, and 6, and the best exponential fit of these data (R=.90) was used to characterize the patient's baseline activity (solid curves in Fig. 6). The solid circles in Figure 6 represent the actual time spent at each intensity level on the day of interest (days 1–6). Figure 6 illustrates that the increase in activity was primarily due to the patient performing a greater amount of high-intensity activity (36–47 strides per minute) on the day of ulceration (day 3) relative to the other 5 days of this period of activity monitoring.

View larger version (22K): [in this window] [in a new window]   Figure 6. Variations in activity over 6 consecutive days. Number of minutes per day spent at different intensities of physical activity monitored during 6 consecutive days. Curves represent best least-squares fit for baseline activity (days 1, 2, 4, 5, and 6). Solid circles represent the actual time spent at each intensity level on that particular day (days 1–6). Note the substantial change in the patient performing more high-intensity activity on the day of ulcer recurrence (day 3) relative to the other days that activity was monitored (days 1, 2, 4, 5, and 6).

View larger version (37K): [in this window] [in a new window]   Figure 7. Daily cumulative plantar tissue stress levels (which are the products of the pressure-time integral and the mean daily strides from activity monitor) for: subjects without diabetes (CON)25; subjects with diabetes, peripheral neuropathy, and no history of plantar ulcers (DMPN)25; subjects with diabetes, peripheral neuropathy, and a history of plantar ulcers (DMPN+U)25; and the patient of this case report on 6 consecutive days monitored after initial ulcer healing. On the day of ulcer recurrence (day 3), daily cumulative stress for the patient was 2.5 to 5 times higher than on days 1, 2, 4, 5, and 6, yet was similar to the amount of daily stress accumulated by subjects with and without diabetes and a history of ulceration.

	Discussion

Top Abstract Introduction Case Description Intervention Discussion References

Few studies have examined the effect of activity level on cumulative plantar tissue stress or ulcer recurrence in people with DM. Studies have shown that people with DM take fewer steps (2 steps=one stride) per day (4,548–7,816 steps per day^25–28) than people without DM (7,370–10,074 steps per day^25,28). Our patient was relatively inactive during TCC (1,387±649 strides per day or 2,774 steps per day) and after ulcer healing (1,909±504 strides per day or 3,818 steps per day on days 1, 2, 4, 5, and 6). According to principles of the PST, reduced weight-bearing activity in patients with DM may contribute to decreased cumulative stress on plantar tissues, resulting in tissue atrophy and a lower threshold for subsequent tissue adaptation and injury compared with the plantar tissues of active individuals (Fig. 8).⁸ This plantar tissue atrophy and subsequent lowering of thresholds in people with DM may make plantar soft tissues more susceptible to injury when exposed to the same stress levels that are routinely tolerated without injury by individuals with an average or high level of activity.⁸ The findings of LeMaster et al,²⁹ who studied the relationship between reported activity and ulcer recurrence in people with DM and a prior foot ulcer, are consistent with this principle. They reported that their most active participants were at 80% less risk for foot ulcer than the least active participants (95% confidence interval=13%–96%). Therefore, we speculate that the stress contributing to tissue injury may not be the number of steps, but the rapid change in the number of steps.

View larger version (31K): [in this window] [in a new window]   Figure 8. Effect of prolonged low stress lowers thresholds for subsequent adaptation and injury. Prolonged physical stress levels that are lower than the maintenance range result in decreased tolerance of tissues to subsequent stresses (eg, atrophy). Although relative thresholds remain the same, the absolute magnitude of physical stress is lower for each threshold. Injury (and all other adaptations) occurs at a lower level of physical stress than required previously. Reprinted with permission from the American Physical Therapy Association from Mueller MJ, Maluf KS. Tissue adaptation to physical stress: a proposed "physical stress theory" to guide physical therapist practice, education, and research. Phys Ther. 2002;82:383–403.

These observations suggest that tissue injury may result from sudden changes in activity and the routine loading of plantar tissues, rather than an absolute value of peak plantar pressure or step count. This conclusion is consistent with the principles of the PST that extreme deviations from the maintenance stress range that exceed the adaptive capacity of tissue result in tissue injury, which in this case was a recurrence of the patient's ulcer.⁸ Other researchers have suggested that sudden variability in activity may contribute to the development of plantar ulcers. Armstrong et al³⁰ recently evaluated the activity level of a group of individuals similar to the patient in this case report (people with DM, loss of protective sensation, no peripheral vascular disease, and a history of a plantar ulcer). These authors concluded that the subjects who developed plantar ulcers during their study demonstrated "periods of inactivity punctuated by relatively sudden pulses of activity taken over a short time frame."^30(p1982) We speculate that sudden changes greater than 2 standard deviations from a person's mean level of activity would place the person at high risk for skin breakdown, but additional research is needed to test this speculation.

It might be argued the recurrence of this patient's ulcer was due to the TCC being discontinued prematurely (before the ulcer had completely healed). We thought discontinuing the TCC was appropriate because skin coverage over the wound was complete. We observed no drainage from the ulcer site after completion of intervention with TCC. Although the newly healed tissues at the ulcer site likely were fragile, they were able to withstand the exposure to physical stress through the patient's regular amount of weight-bearing activity for more than 3 weeks without injury. Tissue injury occurred only when the patient's activity level increased substantially. Therefore, we believe that the decision to discontinue the TCC when we did was appropriate and that the sudden increase in activity level (increase in both amount and intensity) was the major contributing factor to the patient's ulcer recurrence.

This case highlights the potential contribution of changes in weight-bearing activity to plantar tissue stress and tissue adaptation. The case also supports the recommendation frequently given to patients that a graded return to activity following a period of immobilization with TCC could reduce the incidence of ulcer recurrence. Advocates of the PST contend that exposure to physical stress levels that exceed the maintenance range (ie, overload) result in increased tolerance of tissues to subsequent stresses, but adequate recovery between exposures of increased stress is necessary for hypertrophy to occur without injury.⁸ Gradual and progressive activity may promote tissue hypertrophy at the plantar surface of the foot and raise the tolerance for plantar tissue stress after prolonged immobilization with TCC. This improved tolerance to stress may enable the plantar surfaces of the feet to be loaded at gradually higher levels of stress with decreased risk of tissue injury. Additional research is needed to test this hypothesis generated by the PST.

The use of pedometers or activity monitoring devices may assist patients in monitoring their gradual increase in activity during the initial weeks after wound healing when the risk of tissue injury is highest.^5,30 A limitation to this approach may be poor adherence to activity guidelines. Our current research is investigating how to monitor other factors that may contribute to physical stress at the plantar surface of the foot. We have developed an in-shoe multisensory data acquisition system to monitor temperature, pressure, and humidity.^31,32 Future research on the quantification of these contributing factors and activity level may enable researchers and clinicians to identify and avoid the thresholds for injury. Further research, we believe, should focus on the development of guidelines for appropriate progression of activity to complement the physical therapist management of patients with DM after healing of a plantar ulcer. This case suggests that activity monitoring in conjunction with existing intervention approaches may help decrease the risk of plantar ulcer recurrence in individuals with DM. Additional research is needed to clarify the relationship between activity and ulcer recurrence rates.

	Footnotes

 
This worked was supported, in part, by a PODS 1 scholarship (DJL) and a PODS 2 scholarship (KSM) from the Foundation for Physical Therapy. This work also was supported, in part, by a NIDDK grant (DK 59224-03) awarded to Dr Sinacore.

Some of the data and figures in this article were presented at the VIII EMED Scientific Meeting in Kananaskis, Alberta, Canada, on July 31–August 3, 2002.

^* Bio Medical Instrument Co, 15764 Munn Rd, Newbury, OH 44065.

Professional Protective Technology, 21 E Industry Ct, Deer Park, NY 11729.

Bakelite Xylonite Ltd, London, United Kingdom, distributed in the United States by Alimed Inc, 297 High St, Dedham, MA 02026.

Prosthetics Research Study, 675 S Lane St, Suite 100, Seattle, WA 98104.

^|| Novel Electronics Inc, 964 Grand Ave, St Paul, MN 55105.

	References

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