PHYS THER
Vol. 88, No. 11, November 2008, pp. 1385-1398
DOI: 10.2522/ptj.20080019

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Correction (v89,p1103)
Right arrow All Versions of this Article:
ptj.20080019v1
88/11/1385    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when Rapid Responses are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by LeMaster, J. W
Right arrow Articles by Conn, V. S
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by LeMaster, J. W
Right arrow Articles by Conn, V. S
Related Collections
Right arrow Skin Abnormalities and Diseases
Right arrow Therapeutic Exercise
Right arrow Randomized Controlled Trials
Right arrow Diabetes
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

Diabetes Special Issue

Effect of Weight-Bearing Activity on Foot Ulcer Incidence in People With Diabetic Peripheral Neuropathy: Feet First Randomized Controlled Trial

Joseph W LeMaster, Michael J Mueller, Gayle E Reiber, David R Mehr, Richard W Madsen and Vicki S Conn

JW LeMaster, MD, MPH, is Assistant Professor, Department of Family and Community Medicine, School of Medicine, University of Missouri, MA306-K Medical Science Building, DC032.00, Columbia, MO 65212 (USA)
MJ Mueller, PT, PhD, FAPTA, is Associate Professor, Program in Physical Therapy and Department of Radiology, Washington University School of Medicine, St Louis, Missouri
GE Reiber, MPH, PhD, is Professor, Department of Health Services and Epidemiology, School of Public Health and Community Medicine, University of Washington, and VA Puget Sound Health Care System, Seattle, Washington
DR Mehr, MD, MS, is Professor, Department of Family and Community Medicine, School of Medicine, University of Missouri
RW Madsen, PhD, is Emeritus Professor, Department of Statistics, University of Missouri
VS Conn, PhD, RN, FAAN, is Professor, Sinclair School of Nursing, University of Missouri

Address all correspondence to Dr LeMaster at: lemasterj{at}health.missouri.edu


Submitted January 16, 2008; Accepted May 8, 2008


arrow
Abstract
 
Background: Weight-bearing exercise has been contraindicated among people with diabetic peripheral neuropathy (DM+PN). However, recent cohort studies have suggested that daily weight-bearing activity is associated with lower risk for foot ulceration.

Objective: The objective of this study was to determine the effect of a lower-extremity exercise and walking intervention program on weight-bearing activity and foot ulcer incidence in people with DM+PN.

Design: This was an observer-blinded, 12-month randomized controlled trial.

Setting: The settings were physical therapy offices in part 1 of the intervention and the community in part 2 of the intervention.

Participants: The participants were 79 individuals with DM+PN who were randomly assigned either to a control group (n=38) or an intervention group (n=41) group.

Intervention: Intervention components included leg strengthening and balance exercises; a graduated, self-monitored walking program (part 1); and motivational telephone calls every 2 weeks (part 2). Both groups received diabetic foot care education, regular foot care, and 8 sessions with a physical therapist.

Measurements: Total and exercise bout–related daily steps at baseline and at 3, 6, and 12 months were measured by accelerometers. Foot lesions/ulcers were photographed and classified by an independent panel of dermatologists. Use of adequate footwear was monitored.

Results: At 6 months, bout-related daily steps increased 14% from baseline in the intervention group and decreased 6% from baseline in the control group. Although the groups did not differ statistically in the change in total daily steps, at 12 months steps had decreased by 13% in the control group. Foot ulcer rates did not differ significantly between groups.

Conclusion: Promoting weight-bearing activity did not lead to significant increases in foot ulcers. Weight-bearing activity can be considered following adequate assessment and counseling of patients with DM+PN.


arrow
Introduction
 
In 2000–2002, approximately 60% of lower-extremity amputations in the United States were diabetes-related, and the majority were preceded by a foot ulcer.1 During their lifetimes, 40% of the estimated 20.8 million US adults with diabetes mellitus will experience loss of foot sensation.2,3 Almost all diabetic foot ulcers occur in those with insensate feet due to diabetic peripheral neuropathy (DM+PN).4,5

The role of weight-bearing physical activity in the development of diabetic foot ulcers remains poorly understood. Regular participation in moderately intense physical activity (eg, brisk walking) improves glycemic control.6 Eight-year cardiovascular mortality is 34% lower among people with diabetes who walk 2 hours per week compared with nonwalkers.7 Therefore, the American Diabetes Association (ADA) recommends at least 30 minutes of daily moderately intense physical activity.8 However, the ADA recommends that people with DM+PN should limit weight-bearing physical activity because of concerns that it could increase the risk of foot ulcers and amputation.8,9 Recent descriptive studies, however, suggest that patients with insensate feet who participate in daily weight-bearing activity are at decreased risk of foot ulceration compared with those who are less active,10,11 especially if there is minimal variation in their day-to-day activity pattern.11,12 A progressive walking program may preserve lower-extremity muscles and make plantar tissue more tolerant to stress and less likely to ulcerate.1315 To date, no randomized controlled trial has tested the effect of promoting weight-bearing physical activity on the risk for foot ulceration among people with DM+PN.

As a prelude to further large-scale clinical trials, investigators must develop an effective, safe strategy to increase physical activity among patients with DM+PN. Prior intervention studies have demonstrated that behavioral change programs individually tailored to patients’ physical limitations, activity preferences, and readiness to change substantially increase moderately intense activity in older adults.16,17 However, until now, no one has studied whether interventions of this sort are effective among patients with diabetic complications (such as DM+PN). People with diabetes and insensate feet are one third less active than those with diabetes but intact sensation.18,19 To investigate these issues, we conducted a randomized controlled trial among adults aged 50 years and older with diabetes mellitus and insensate feet, the "Feet First" study. We hypothesized that the intervention would increase weight-bearing activity significantly more among participants who receive the intervention compared with controls and that this change in activity would not result in increased foot ulcer rates.


arrow
Method
 
Design Overview

Feet First was an observer-blinded, randomized controlled trial of an individually adapted, behavioral change physical activity intervention. Seventy-nine patients with DM+PN were recruited over 18 months and randomly allocated to either an intervention group (n=41) or a control group (n=38). Physical activity, foot function, and foot-related self-care were measured at baseline prior to enrollment and after 3, 6, and 12 months of participation. Foot lesion detection was ongoing throughout the study. In an intention-to-treat analysis, we compared the change in weight-bearing activity from baseline to 3, 6, and 12 months and foot ulcer risk for participants in the intervention and control groups.

Setting and Participants

Patients aged 50 years and over who received diabetes or foot care at primary care, endocrinology, or podiatry practices in central Missouri were invited to join the study. Eligible participants were inactive (did not engage in moderately intense activity more than twice per week for more than 20 minutes per session),20 had diagnosed type 1 or 2 diabetes mellitus, had absent sensation to 5.07 Semmes-Weinstein monofilament sensation on at least one point at any of 10 sites on each foot,21 and had loss of vibratory sensation as measured by a biothesiometer (unable to sense <25 V at the great toe).22 We excluded individuals who lacked telephone access or had medical conditions that might contraindicate exercise.8 Figure 1 shows contacts, excluded and randomized participants, and those completing the study. Of the 79 participants who were recruited, 1 died of causes unrelated to the study and 2 withdrew early.


Figure 1
View larger version (47K):
[in this window]
[in a new window]

 
Figure 1. CONSORT study diagram: recruitment, randomization, and participation. All participants were analyzed as per their allocated group. Participants who withdrew did not provide activity data at or after indicated period of participation. All randomized participants were followed until withdrawal or study completion for foot outcomes. SBP=systolic blood pressure. DBP=diastolic blood pressure.

Randomization and Intervention

After providing written informed consent, eligible participants who completed baseline measures were randomly allocated to intervention and control groups. Because treatment strategies for early foot lesions could differ among types of clinical sites, randomization was by type of clinical site (specifically, university-affiliated family medicine, university-affiliated endocrinology, VA-affiliated foot clinic, local family medicine and internal medicine practices not affiliated with the university, and out-of-county unaffiliated family medicine and internal medicine practices). Study groups were balanced within each type of site by using randomization blocks of various sizes.23 Participants returned for a "randomization visit" 2 weeks after their initial visit for baseline measurements and informed consent. Allocation to study groups was concealed by opaque envelopes, which were opened by the study nurse at the randomization visit. Prior to and during this visit, the nurse had no access to information collected from participants at the baseline measurement visit.

The overall aim of the intervention was to encourage participants to gradually increase total daily weight-bearing steps. Based on the predictions of Mueller and Maluf's Physical Stress Theory, we hypothesized that the slow increase in activity would allow foot tissues to adapt to the physical stresses and make them relatively more resistant to ulceration.14,15 The intervention incorporated components from prior studies that increased activity in older adults.20,2428 It was delivered in 2 parts. During months 1 to 3 (part 1), a physical therapist worked with participants individually via 8 sessions focused on exercises to strengthen lower-extremity muscles and promote balance. These exercises (Appendix) were successful in prior fall-reduction interventions for frail older adults2527 and in improving balance in people with peripheral neuropathy.24 In 3 at-home sessions each week, participants were asked to perform progressively more difficult exercises over 1 hour. After the eighth supervised session, the therapist and study nurse helped each participant to develop a walking plan tailored to his or her personal stage of readiness to change, physical limitations, activity preferences, and social or environmental constraints. The therapist and nurse encouraged participants to increase activity slowly, at minimum adding 100 steps to their daily activities every 2 weeks, using their baseline average activity as the starting point.8,29 Participants self-monitored their walking using an inexpensive, waist-worn pedometer (Accusplit Eagle 170*) and recorded each day's total steps on an activity log. (This information was used by participants for self-motivation only, not as study data). Participants in the control group received an identical number of visits (n=8) with the therapist at which their feet were examined, but they were not taught leg strengthening or balance exercises or guided to undertake a walking program.

Part 2 (months 4–12) of the intervention was modeled after the Second Community Healthy Activities Model Program for Seniors (CHAMPS II) intervention, which increased moderately intense activity by 50% over 12 months among community-dwelling adults ≥65 years of age.20 The CHAMPS II intervention was based on social cognitive theory and used motivational techniques that enhanced self-efficacy and readiness to change to promote changes in physical activity via regular telephone calls and workshops.28,3032 In the Feet First trial, the project nurse called participants every other week (for a minimum of 10 minutes) to prompt participants to follow their walking plan and assist them in solving related barriers. The nurse received 1 week of intensive training in motivational interviewing techniques from CHAMPS II study staff consultants, with monthly follow-up contact to discuss issues in applying motivational interviewing techniques to specific participants. Control group participants did not have contact with the intervention study nurse after the randomization visit.

All participants were taught foot-related self-care skills, including daily foot examination. They received usual medical care from their own health care providers. Because wearing poorly fitting shoes is a frequent pivotal event preceding a foot ulcer,5 project staff referred all participants to local orthotists or podiatrists to obtain therapeutic footwear at enrollment. Participants were asked to wear this footwear when standing, walking, or being more active inside and outside their homes.

Outcomes and Follow-up

Observer blinding.
Research staff engaged in collecting physical measurements or questionnaire data from participants or tracking other outcomes (ie, foot lesions) were blinded to participants’ study group identity (intervention vs. control). These staff did not take part in intervention activities.

Physical activity.
At baseline and at 3, 6, and 12 months, each participant was fitted with a StepWatch water-resistant, computerized accelerometer.{dagger} Worn on the ankle, the StepWatch reliably counts steps of any intensity every minute without providing feedback to the wearer.33 It has been validated for people with DM+PN.14,34 Participants wore the StepWatch continuously when awake (except while bathing) and returned the StepWatch after 14 days. We documented changes in StepWatch-based total daily steps, steps taken in 30-minute exercise bouts, and minutes per week of weight-bearing activity. We defined a "combined physical activity increase" as an increase from baseline in both total daily steps and an increase in bout-related steps. Using the validated Summary of Diabetes Self-Care Activities Scale,35 participants also reported the number of days per week that they participated in any exercise program at baseline and at 6 and 12 months. Participants also completed a 6-minute walk test at baseline and at 6 and 12 months, which is a safe and valid measure of endurance for moderately intense activities.3641 Participants were instructed to walk as fast as they were able for 6 minutes; the distance walked (in feet) constituted the result.

Foot lesions and ulcers.
At each study visit (including the 8 initial visits with a physical therapist), study staff examined all surfaces of each participant's feet, including interdigital areas, to identify unreported and occult foot lesions. Therapists also taught participants to inspect their own feet every morning for any evidence of skin breakdown (eg, blisters, abrasions, other skin disruptions). We asked participants to call a dedicated hotline immediately if any of these lesions developed and at least weekly to report the presence or absence of any foot lesions. If a lesion was reported, study staff contacted the participant within 24 hours and arranged to examine and photograph the lesion.4244 An independent panel of dermatologists who were not otherwise involved in the conduct of the study reviewed the photographs to classify those meeting predetermined criteria for foot lesions and ulcers. Final classification was determined by consensus of panel members. Foot lesions were defined as any disruption of the skin surface (eg, abrasions, lacerations, blisters, macerations) at or below the malleolus; foot ulcers were defined as the subset of these lesions with full-thickness disruption.45 Any partial-thickness lesion that subsequently became a full-thickness lesion was counted as both a lesion and an ulcer. All lesions or ulcers that occurred at the same time on the same foot were categorized as a single episode. Whenever a foot ulcer or other lesion developed, participants were instructed to limit weight-bearing activity until healing, and study staff helped them make an appointment with a foot care provider.

Other foot-related characteristics measured at baseline included ankle brachial blood pressure index, which was the ratio of supine blood pressure at the brachial artery to that at the dorsalis pedis or posterior tibialis artery, measured using a Koven BiDop-3 doppler stethoscope{ddagger}; a self-reported foot-related disability score46; and history of prior foot ulcers in the year preceding enrollment. Staff inspected the inner and outer surfaces of the participants’ shoes for adequacy and wear at each post-enrollment study visit. Thinning (to less than half the thickness of unworn area) or rupture of the insole, outsole, or inner or outer surface of the shoe upper surface indicated excessive wear. Adequate footwear included prescribed or over-the-counter therapeutic footwear and walking or athletic shoes with double-density foam inserts.47 Study staff advised all participants wearing inadequate footwear at any study visit to consult a local orthotist or podiatrist to obtain adequate footwear.

Demographic and health characteristics included age, sex, current marital status, education, ethnicity, smoking status, type and duration of diabetes mellitus, number of comorbid illnesses, and availability of health insurance. Depressive symptoms were assessed at baseline using the Center for Epidemiologic Studies Depression Scale.48 Body mass index was calculated as weight (in kilograms)/height squared (in meters squared).

Data Analysis

Intention-to-treat analyses compared the intervention and control groups, regardless of their level of protocol adherence and study participation. Comparisons were 2-sided, and a P value of <.05 was considered significant. All analyses were conducted using either SAS version 9.0§ or Stata version 10.0.||

Physical activity.
Primary analyses used a "mixed-effects," repeated-measures regression to investigate changes in weight-bearing activity at 3, 6, and 12 months; activity at baseline was a covariate. This method allows inclusion of participants with some missing data (due to dropout or missed visits).49 The initial model (model 1) estimated the intervention's effect over the entire study after randomization (between-group effect), whether there was a change in activity within each group from baseline to 3, 6, or 12 months (within-group effect) or whether the change in activity from baseline to 3, 6, or 12 months differed between groups (interaction between groups and months). Because 2 distinct intervention components were delivered by different health care professionals (physical therapists in part 1 and a registered nurse in part 2), model 2 repeated this analysis for outcomes after completion of part 1 only (3 and 6 months). Some participants provided less than 14 days of StepWatch monitoring (eg, if the StepWatch was worn upside-down, it did not register steps). Because estimates of mean steps or minutes based on a larger number of measured days are more precise than those based on a smaller number of days, we weighted mean activity outcome values by the number of days of StepWatch data provided during each monitoring period. We tested whether seasonality at study entry and on subsequent study visits influenced results by including season in regression models; however, it was never significant and did not change outcome estimates by more than 10%. Therefore, season was excluded from final models.

To determine whether adherence to study protocol may have influenced our results, we defined "protocol completers" as participants who: (1) attended more than 50% of the required physical therapy sessions within the required 12-week time period, (2) attended the 3-, 6-, and 12-month study visits within 1 month of the anticipated date, and (3) completed at least 50% of the weekly telephone calls to report lesion outcomes.

Foot outcomes.
Incidence rate (IR) of foot lesions and ulcers (each was considered separately) equaled the total number of lesions or ulcers observed for all participants divided by total exposure time in the study for those participants. We estimated incidence rate ratios (IRintervention/IRcontrol) and 95% confidence intervals (CIs) to determine whether either study group was at significantly increased risk. We used the GENMOD procedure in SAS to perform Poisson regression with categorical predictor variables (eg, group) as well as with continuous covariates (eg, time enrolled). We tested these regression models for departure from the Poisson distribution (which assumes that each foot ulcer outcome occurred independent of any prior ulcers). Analyses consider foot lesions, total ulcers, and weight-bearing ulcers for the first 6 months and for the full 12-month study. These outcomes were monitored by a Data Safety and Monitoring Board, which was responsible for halting the study if the incidence rate of foot ulcers in one group significantly exceeded that in the other group.

Sample size.
Taking advantage of other prior work,14,19,50 sample size computations were based on the anticipated change in the number of steps per day (hereafter referred to as "daily steps"). Maluf and Mueller14 found that people with diabetes and insensate feet, on average, took 3,908 daily steps (SD=1,487). We assumed that participants in our control group would take a similar number of daily steps at baseline and that the standard deviation of the change in total daily steps would be similar to that in the study by Maluf and Mueller. The study had 96% power to detect a 25% difference between groups in the change in total daily steps between baseline and 3, 6, or 12 months (a change of 977 daily steps, half the change in activity achieved in the original CHAMPS II study, proportionally).20 The study also had 80% power to detect a doubling of the incidence rate of foot lesions comparing the intervention and control groups after 12 months of participation. This assumed an incidence rate equal to 0.75 lesions per person-year in the control group (the rate observed in a randomized trial in a similar population).5

Role of the Funding Source

The study was funded by the Robert Wood Johnson Foundation, which approved the study design but did not direct the study team regarding conduct or analysis of the study.


arrow
Results
 
Table 1 presents baseline characteristics for the 79 participants. The groups did not differ at baseline with respect to demographic, health or foot-related characteristics, or weight-bearing activity. The average age of participants was 66 years, 51% were women, and participants had an average of 15 years of education. Mean diabetes duration exceeded 11 years, and 93% of the participants had one or more serious comorbidities.


View this table:
[in this window]
[in a new window]

 
Table 1. Baseline Characteristics by Groupa

Table 2 presents estimated weight-bearing activity based on StepWatch measurements. In both the pooled analysis including all data collection points (model 1) and the analysis after part 1 of the intervention only (model 2), the change in total daily steps did not differ significantly between study groups; however, total steps decreased by 13% over the 12-month study within the control group.


View this table:
[in this window]
[in a new window]

 
Table 2. Estimated Weight-Bearing Physical Activity, by Months in Study (Based on Stepwatch3 Computerized Pedometer) (Weighted by Number of Days of Data Provided per Period)

Steps taken during 30-minute exercise bouts increased 14% from baseline to 6 months in the intervention group, whereas they decreased 6% in the control group. There was a difference between groups in this outcome at both 6 and 12 months (model 1) and in the change between baseline and completion of part 1 of the intervention (model 2). There was no difference between groups in the change (in minutes) of ambulatory activity per week from baseline to 3, 6, or 12 months (model 1 or 2), although it decreased by 15% between baseline and 12 months within the control group. There was no difference in the change in 6-minute walk test distances between baseline and 6 or 12 months (model 1 or 2), either between groups or within either group. The change in the number of exercise days per week from baseline to 6 months differed significantly between groups. Reported number of days participating in structured exercise programs increased from 0 days per week in both groups at baseline to 3 days per week in the intervention group and 1.5 days in the control group by 6 months; however, by 12 months, the number of exercise days per week no longer differed between groups (Tab. 2).

The range of increase in total daily steps for participants with a "combined physical activity increase" (an increase in both total steps and bout-related steps between baseline and 6 months) was 96 (minimum) to 3,610 (maximum) steps daily, with a median increase of 898 total steps daily (25th percentile=513, 75th percentile=1,762). These same participants had an increase in bout-related steps ranging from 10 to 1,027 steps during the most active 30 minutes of the day, with a median increase of 73 steps (25th percentile=39, 75th percentile=332 steps). The "combined physical activity increase" occurred more often among intervention group participants (n=16, 39%) than among control group participants (n=7, 18%) after 6 months of participation (odds ratio [OR]=2.83, 95% CI=1.01–7.96), although this did not hold true by 12 months (intervention group: n=13 [32%], control group: n=10 [26%], OR=1.3, 95% CI=0.48–3.48). This outcome was not associated with any other demographic, health, or foot-related baseline characteristic.

Mean follow-up was 392 days (SD=92) in the intervention group and 403 days (SD=68) in the control group but did not differ between groups. With respect to protocol adherence, at 6 months, only 18 (45%) participants in the intervention group and 13 participants (35%) in the control group qualified as "completers" through timely achievement of more than 50% of all study protocol elements ({chi}2=0.78, P=.38). By 12 months, this number had fallen to 7 (18%) participants in the intervention and 9 (24%) in the control group ({chi}2=0.45, P=.50). Nonetheless, when we excluded from the analysis participants who were not fully adherent, none of the regression estimates for any activity outcome varied from the intent-to-treat analysis by more than 10%. Figure 2 shows changes in mean activity for the intervention and control groups, with 95% CIs comparing all participants with completers at baseline and at 3, 6 and 12 months.


Figure 2
View larger version (24K):
[in this window]
[in a new window]

 
Figure 2. Step activity monitor findings for intervention and control groups and study completers: means with 95% confidence limits (actual values).

A total of 57 foot lesions were detected during the 12-month study. Nine lesions resulted from self-inflicted trauma during self-care (eg, cutting a toe while attempting to cut a toenail) and were excluded from further analysis. Of the remaining 48 lesions, 18 were full-thickness ulcers (9 in each study group, overall incidence=17%). Given that 58% of the sample had no history of foot ulcers (predicted annual incidence=4.5%) and that 42% had a history of foot ulcers (predicted annual incidence=31.7%), the predicted annual incidence of foot ulcers in this sample was 15.9%.51 Ulcers were generally small: only 1 ulcer in the intervention group and 4 ulcers in the control group were greater than 1 cm2 in surface area ({chi}2=2.62, P=.10). All ulcers healed except one on the foot of a participant who died due to causes unrelated to the study. Ulcer duration was 74 days (SD=49) in the intervention group and 51.5 days (SD=43) in the control group (one-way F test=1.25, df=1, P=.27). None of the ulcers required hospitalization for infection, and none led to amputation or Charcot arthropathy. Total foot ulcer and foot lesion incidence rates did not differ significantly between groups after 6 or 12 months of participation (Tab. 3). Ulcer rates on plantar weight-bearing areas did not differ significantly between the intervention and control groups at any point during the study. Plantar weight-bearing ulcer rates were the same during the first 6 months of follow-up (both groups=0.05 ulcers/person-year-at-risk). For the full 12-month study, the rate of weight-bearing ulcers was 0.02 ulcers/person-year-at-risk in the intervention group and 0.12 ulcers/person-year-at-risk in the control group. Shoe adequacy and wear did not differ between groups at any point in the study (data not shown in the tables).


View this table:
[in this window]
[in a new window]

 
Table 3. Foot Ulcer and Lesion Analysis

There was one nonulcerative adverse event possibly related to a specific component of the intervention. One participant in the intervention group with previously undiagnosed osteoporosis sustained a proximal phalangeal great toe fracture attributed to a leg strengthening exercise in part 1 of the intervention (raising up on toes). To avoid the possibility that this fracture could become neuropathic (Charcot), the participant was excused from further exercises of this sort, but still undertook a limited walking program after the fracture healed.


arrow
Discussion
 
In this randomized controlled trial, we found that the intervention increased weight-bearing, bout-related physical activity. This type of activity increased most notably between baseline and 6 months, after participants had completed part 1 of the intervention (physical therapist visits). Although there was no difference between groups in the change in total daily steps from baseline to any subsequent point in the study, participants in the control group decreased total steps by 13% over 12 months. Participants in the intervention group were about 3 times more likely to increase both total steps and bout-related steps by 6 months compared with participants in the control group. Participation in structured exercise sessions also increased more among participants in the intervention group (from 0 to 3 days per week) compared with those in the control group (0 to 1.5 days per week) by 6 months. These changes regressed toward baseline during the last 6 months of study participation.

Consistent with our hypothesis, we found that foot lesion and plantar foot ulcer rates did not differ significantly between study groups at any point in the study. Because participants were closely supervised and quickly referred to foot care providers upon ulceration, no ulcer progressed to infection, amputation, or Charcot arthropathy. These findings suggest that an intervention promoting weight-bearing activity such as the Feet First intervention is not harmful to the feet of people with DM+PN. The overall incidence of ulceration (17%) was similar to that predicted in prior studies among similar patients with similar characteristics and comorbidities.51,52

Participants in this study achieved only modest increases in activity. Recent meta-analyses of interventions promoting physical activity in people with chronic illnesses, including diabetes, showed that behavioral strategies such as giving participants daily step prescriptions, asking participants to monitor their daily steps, and using personal trainers to supervise them carefully as they increased activity produced larger effect sizes than studies without these components; however, cognitive interventions (such as the motivational strategies used in part 2 of our intervention) were less effective at increasing activity.17,53 Future interventions investigating the effect of weight-bearing activity among people with DM+PN should provide a more intense program that provides patients with specific daily step goals and closely supervises their increase in activity.

The Feet First intervention also helped participants in the intervention group to maintain their baseline number of total daily steps, whereas in the control group, participants’ total steps decreased consistently over the data collection period, declining 13% over 1 year. Given the dose-response increase in all-cause and cardiovascular mortality in people with diabetes associated with progressively greater inactivity,54,55 preventing a decline in physical activity of this magnitude is an important achievement in this population apart from the effect of the intervention on foot ulcer risk. Although we did not find that the Feet First intervention increased total daily steps, it did help participants increase steps taken in bouts. In a recent randomized trial of participants with type 2 diabetes who were sedentary, Richardson and colleagues56 found that providing participants with a targeted number of daily steps was more effective than providing a targeted number of minutes of activity per day in increasing total daily steps.

Although Stewart and colleagues20 found a 50% increase in exercise behavior in the original CHAMPS II study, the basis for part 2 of our intervention, only 7% of their sample had diabetes. Comorbidity in our sample was much higher than among the CHAMPS II study participants. In the current study, comorbidity was equally distributed between the intervention and control groups, so any exercise limitations arising from comorbidity probably affected both groups similarly.

ADA recommendations that people with DM+PN should limit weight-bearing activity are based on research on the effect of weight-bearing activity on insensate feet that was first conducted by Brand and colleagues, who found that repetitive mechanical stimulation of anesthetized rats’ footpads led to skin ulceration. In those experiments, footpads that received 10,000 daily repetitions ulcerated within 10 days; however, footpads that received slightly less daily stimulation (8,000 steps per day) for 5 days per week never ulcerated.57 A number of cohort studies subsequently demonstrated an association between high plantar foot pressures and increased diabetic foot ulcer risk.5861 Together, these studies led to the belief that repetitive stimulation to areas of increased pressure on an insensate foot during walking would further increase foot ulcer risk.9 (Also see the related article by Mueller et al62 investigating the physical stresses contributing to neuropathic ulcers in this issue.)

Surprisingly, Maluf and Mueller14 recently found that people with DM+PN and a history of foot ulcers took 46% fewer daily steps and had 41% less cumulative daily forefoot tissue stress (plantar pressure multiplied by daily steps) than people without ulcers, suggesting that those who ulcerate are less tolerant of daily stress and that a progressive increase in weight-bearing activity may lead to plantar tissue hypertrophy and reduced ulcer risk. LeMaster and colleagues10 also found that among people with prior diabetic foot ulcers, those who participated in weight-bearing activity at least 7.5 hours per day were at 80% less risk of reulceration compared with those who were weight bearing less than 4.5 hours per day. Similarly, Armstrong and colleagues11 found that among people with DM+PN monitored continuously for 25 weeks, those who ulcerated were significantly less active than those who did not, although variability in activity was higher among those who ulcerated. Although the current study did not show evidence that weight-bearing activity reduced foot ulcer risk, neither did it show evidence that foot ulcer risk increased. Additional studies using interventions with higher intensity are needed to help determine whether neuropathic skin and feet can adapt positively to increasing stress levels.

This study had a number of potential limitations. First, the study was designed primarily to detect differences in physical activity between groups rather than differences in foot ulcer incidence. We did this realizing that any inferences regarding the effect of physical activity on foot ulcer risk are dependent on the change in weight-bearing physical activity. The incidence rate ratio we observed for the full 12-month study for full-thickness ulcers and ulcer episodes was essentially equal to 1, indicating no significant or clinically important differences between groups; however, CIs were wide. Wide CIs indicate that a clinically important difference cannot be excluded with high probability. Subsequent studies should be designed to detect differences in important but rarer outcomes, such as the incidence of foot ulcers on weight-bearing areas of the foot.

Second, the Step Watch accelerometer measures only minutes of activity taken during stepping. Time spent standing immobile is not recorded; however, we did not observe any significant differences between groups in time spent inactive.

Third, participants in the control group did not receive motivational calls from the study nurse and may not have been as engaged in the study as participants in the intervention group. This could have led to reduced reporting of minor foot lesions by controls; however, we did not find any significant difference in protocol adherence between groups.

Fourth, the high level of close participant follow-up in the study helped us to detect foot lesions at an earlier stage than would likely have been possible during routine clinical care. This may have reduced the power of the study to detect a difference between groups in foot ulcer risk because lesions were treated successfully before they developed into full-thickness skin ulcers.

Finally, to reduce participant burden, we did not monitor participants’ physical activity or cumulative plantar tissue stress continuously throughout the study. This may have allowed us to miss key changes in activity that occurred just prior to the development of foot lesions. Future studies should consider continuously monitoring participants’ activity or foot stress (and the relationship between activity patterns and foot lesions) throughout study participation.


arrow
Conclusion
 
This study showed that participants in the Feet First intervention group achieved a modest increase in activity, with no increase in foot lesions, compared with those in the control group. We recommend additional research to further investigate current guidelines and close supervision for people with DM+PN as they attempt to increase their weight-bearing activity and make changes in this important self-management behavior.


arrow
Appendix.
 


Figure 1
View larger version (27K):
[in this window]
[in a new window]

 
Appendix. Intervention Program Part 1: Leg Strengthening and Balance Exercisea

aThe number of repetitions represents the goal for each exercise at the indicated stage. Participants started with one set and progressed no faster than 1 level per week for any given exercise. "Both hands" means holding a stable object with both hands (eg, a wall, an assistant's hand) while performing the maneuver; "one hand" means holding on with only one hand. "Both feet" means performing the maneuver while standing on both feet; "one foot" means performing the maneuver while standing on one foot. All participants practiced the "both hands" version of each exercise prior to attempting the maneuver without holding a steady object. All maneuvers were practiced initially under the supervision of the physical therapist, prior to practicing the maneuver at home. The above maneuvers are drawn from the referenced intervention studies.


arrow
Footnotes
 
All authors provided concept/idea/research design, writing, and fund procurement. Dr LeMaster, Dr Reiber, and Dr Madsen provided data analysis. Dr LeMaster provided project management and subjects. Dr Reiber provided Seattle-based facilities/equipment and institutional liaisons. Dr Mueller, Dr Reiber, Dr Mehr, Dr Madsen, and Dr Conn provided consultation (including review of manuscript before submission).

The authors acknowledge the contributions of the Feet First study participants and staff. Shari Schubert and Diana Stout were the study coordinators. Melba Hall, ANP, was the study nurse. Mary Gaub, PT, and Gwenna Peters, PT, were the intervention physical therapists. Evan Prost, PT, Jamie Thomas, Aaron Leppin, Jared Coberly, Matthew Simmons, Amanda Fink, and Dermond Henry were the study observers. Jeffrey Rodenbaugh was the study programmer/data manager. Anita Stewart, PhD, (University of California–San Francisco, Principal Investigator of CHAMPS II) provided advice, and Dawn Gillis, MS, and Barbara McLellan, MPH, (CHAMPS II study staff) provided training and ongoing support concerning this study's use of the CHAMPS II methods and approach.

The study was approved by the University of Missouri–Columbia Health Sciences and University of Washington institutional review boards and by the research and development committees at the Harry S Truman Memorial Veterans’ Hospital in Columbia, Missouri, and the VA Puget Sound Health Care System in Seattle, Washington.

Oral presentations of the results of this study will be given at the 68th Annual Meeting of the American Diabetes Association; June 6–10, 2008; San Francisco, California; and at the meeting of the North American Primary Care Research Group; November 15–19, 2008; Puerto Rico.

This study was funded by the Robert Wood Johnson Foundation Generalist Physician Faculty Scholars program. This material is the result of work supported with resources and the use of facilities at the University of Missouri Health Care System, the Harry S Truman Memorial Veterans’ Hospital, and the VA Puget Sound Health Care System.

* Accusplit, 6120 Stoneridge Mall Rd, Suite 210, Pleasanton, CA 94566. Back

{dagger} OrthoCare Innovations, 700 12th St NW, Suite 700, Washington, DC 20005. Back

{ddagger} Koven Technology Inc, 12125 Woodcrest Executive Dr, Suite 320, St. Louis, MO 63141. Back

§ SAS Institute. PO Box 8000, Cary, NC 27513. Back

|| Stata LP, 4905 Lakeway Dr, College Station, TX 77845. Back


arrow
References
 
  1. Centers for Disease Control and Prevention. History of foot ulcer among persons with diabetes—United States, 2000–2002. MMWR. 2003;52:1098–1102.[Medline]
  2. Narayan KM, Boyle JP, Geiss LS, et al. Impact of recent increase in incidence on future diabetes burden: U.S., 2005–2050. Diabetes Care. 2006;29:2114–2116.[Free Full Text]
  3. Palumbo PJ, Melton LJ III. Peripheral vascular disease and diabetes. In: National Diabetes Data Group, National Institute of Diabetes and Digestive and Kidney Diseases, eds. Diabetes in America. 2nd ed. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases; 1995:401–408.
  4. Pham H, Armstrong DG, Harvey C, et al. Screening techniques to identify people at high risk for diabetic foot ulceration: a prospective multicenter trial. Diabetes Care. 2000;23:606–611.[Abstract/Free Full Text]
  5. Reiber GE, Smith DG, Wallace C, et al. Effect of therapeutic footwear on foot reulceration in patients with diabetes: a randomized controlled trial. JAMA. 2002;287:2552–2558.[Abstract/Free Full Text]
  6. Boule NG, Haddad E, Kenny GP, et al. Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled clinical trials. JAMA. 2001;286:1218–1227.[Abstract/Free Full Text]
  7. Gregg EW, Gerzoff RB, Caspersen CJ, et al. Relationship of walking to mortality among US adults with diabetes. Arch Intern Med. 2003;163:1440–1447.[Abstract/Free Full Text]
  8. Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C. Physical activity/exercise and type 2 diabetes. Diabetes Care. 2004;27:2518–2539.[Free Full Text]
  9. Uccioli L. Footwear in the prevention of diabetic foot problems. In: Veves A, Giurini JM, LoGerfo FW, eds. Diabetic Foot: Medical and Surgical Management. Totowa, NJ: Humana Press; 2002:445–461.
  10. LeMaster JW, Reiber GE, Smith DG, et al. Daily weight-bearing activity does not increase the risk of diabetic foot ulcers. Med Sci Sports Exerc. 2003;35:1093–1099.[CrossRef][Web of Science][Medline]
  11. Armstrong DG, Lavery LA, Holtz-Neiderer K, et al. Variability in activity may precede diabetic foot ulceration. Diabetes Care. 2004;27:1980–1984.[Abstract/Free Full Text]
  12. Lott DJ, Maluf KS, Sinacore DR, Mueller MJ. Relationship between changes in activity and plantar ulcer recurrence in a patient with diabetes mellitus. Phys Ther. 2005;85:579–588.[Abstract/Free Full Text]
  13. England JD, Ferguson MA, Hiatt WR, Regensteiner JG. Progression of neuropathy in peripheral arterial disease. Muscle Nerve. 1995;18:380–387.[CrossRef][Web of Science][Medline]
  14. Maluf KS, Mueller MJ. Novel Award 2002. Comparison of physical activity and cumulative plantar tissue stress among subjects with and without diabetes mellitus and a history of recurrent plantar ulcers.Clin Biomech (Bristol, Avon). 2003;18:567–575.[CrossRef]
  15. 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.[Abstract/Free Full Text]
  16. Task Force on Community Preventive Services. Recommendations to increase physical activity in communities. Am J Prev Med. 2002;22:67–72.[CrossRef][Web of Science][Medline]
  17. Conn VS, Hafdahl AR, Brown SA, Brown LM. Meta-analysis of patient education interventions to increase physical activity among chronically ill adults. Patient Educ Couns. 2008;70:157–172. Epub 2007 Nov 26.[CrossRef][Web of Science][Medline]
  18. Tudor-Locke CE, Bell RC, Myers AM, et al. Pedometer-determined ambulatory activity in individuals with type 2 diabetes. Diabetes Res Clin Pract. 2002;55:191–199.[CrossRef][Web of Science][Medline]
  19. Armstrong DG, Abu-Rumman PL, Nixon BP, Boulton AJ. Continuous activity monitoring in persons at high risk for diabetes-related lower-extremity amputation. J Am Podiatr Med Assoc. 2001;91:451–455.[Abstract/Free Full Text]
  20. Stewart AL, Verboncoeur CJ, McLellan BY, et al. Physical activity outcomes of CHAMPS II: a physical activity promotion program for older adults. J Gerontol A Biol Sci Med Sci. 2001;56:M465–M470.[Abstract/Free Full Text]
  21. Abbott CA, Carrington AL, Ashe H, et al. The North-West Diabetes Foot Care Study: incidence of, and risk factors for, new diabetic foot ulceration in a community-based patient cohort. Diabet Med. 2002;19:377–384.[CrossRef][Web of Science][Medline]
  22. Boulton AJ, Malik RA, Arezzo JC, Sosenko JM. Diabetic somatic neuropathies. Diabetes Care. 2004;27:1458–1486.[Free Full Text]
  23. Meinert CL. Randomization and the mechanics of treatment masking. Clinical Trials: Design, Conduct, and Analysis. Oxford, United Kingdom: Oxford University Press; 1986:90–112.
  24. Richardson JK, Sandman D, Vela S. A focused exercise regimen improves clinical measures of balance in patients with peripheral neuropathy. Arch Phys Med Rehabil. 2001;82:205–209.[CrossRef][Web of Science][Medline]
  25. Binder EF, Schechtman KB, Ehsani AA, et al. Effects of exercise training on frailty in community-dwelling older adults: results of a randomized, controlled trial. J Am Geriatr Soc. 2002;50:1921–1928.[CrossRef][Web of Science][Medline]
  26. Buchner DM, Hornbrook MC, Kutner NG, et al. Development of the common data base for the FICSIT trials. J Am Geriatr Soc. 1993;41:297–308.[Web of Science][Medline]
  27. Gardner MM, Buchner DM, Robertson MC, Campbell AJ. Practical implementation of an exercise-based falls prevention programme. Age Ageing. 2001;30:77–83.[Abstract/Free Full Text]
  28. Stewart AL, Mills KM, Sepsis PG, et al. Evaluation of CHAMPS, a physical activity promotion program for older adults. Ann Behav Med. 1998;19:353–361.[CrossRef][Web of Science]
  29. Lindberg R. Active living: on the road with the 10,000 Steps program. J Am Diet Assoc. 2000;100:878–879.[CrossRef][Web of Science][Medline]
  30. Rollnick S, Mason P, Butler C. Health Behavior Change. Edinburgh, Scotland: Churchill-Livingstone; 2000.
  31. Bandura A. Social cognitive theory: an agentic perspective. Annu Rev Psychol. 2001;52:1–26.[CrossRef][Web of Science][Medline]
  32. Prochaska JO, DiClemente CC. Stages and processes of self-change of smoking: toward an integrative model of change. J Consult Clin Psychol. 1983;51:390–395.[CrossRef][Web of Science][Medline]
  33. Coleman KL, Smith DG, Boone DA, et al. Step Activity Monitor: long-term, continuous recording of ambulatory function. J Rehabil Res Dev. 1999;36:8–18.[Web of Science][Medline]
  34. Resnick B, Nahm ES, Orwig D, et al. Measurement of activity in older adults: reliability and validity of the Step Activity Monitor. J Nurs Meas. 2001;9:275–290.[Medline]
  35. Toobert DJ, Hampson SE, Glasgow RE. The summary of diabetes self-care activities measure: results from 7 studies and a revised scale. Diabetes Care. 2000;23:943–950.[Abstract]
  36. Kervio G, Ville NS, Leclercq C, et al. Intensity and daily reliability of the six-minute walk test in moderate chronic heart failure patients. Arch Phys Med Rehabil. 2004;85:1513–1518.[CrossRef][Web of Science][Medline]
  37. Pankoff BA, Overend TJ, Lucy SD, White KP. Reliability of the six-minute walk test in people with fibromyalgia. Arthritis Care Res. 2000;13:291–295.[CrossRef][Web of Science][Medline]
  38. Kervio G, Carre F, Ville NS. Reliability and intensity of the six-minute walk test in healthy elderly subjects. Med Sci Sports Exerc. 2003;35:169–174.[Web of Science][Medline]
  39. Wright DJ, Khan KM, Gossage EM, Saltissi S. Assessment of a low-intensity cardiac rehabilitation programme using the six-minute walk test. Clin Rehabil. 2001;15:119–124.[Abstract/Free Full Text]
  40. Montgomery PS, Gardner AW. The clinical utility of a six-minute walk test in peripheral arterial occlusive disease patients. J Am Geriatr Soc. 1998;46:706–711.[Web of Science][Medline]
  41. Redelmeier DA, Bayoumi AM, Goldstein RS, Guyatt GH. Interpreting small differences in functional status: the Six-Minute Walk Test in chronic lung disease patients. Am J Respir Crit Care Med. 1997;155:1278–1282.[Abstract]
  42. Williams C. The Verge Videometer wound measurement package. Br J Nurs. 2000;9:237–239.[Medline]
  43. Roa L, Gomez-Cia T, Acha B, Serrano C. Digital imaging in remote diagnosis of burns. Burns. 1999;25:617–623.[CrossRef][Web of Science][Medline]
  44. Langemo DK, Melland H, Hanson D, et al. Two-dimensional wound measurement: comparison of 4 techniques. Adv Wound Care. 1998;11:337–343.[Medline]
  45. Jeffcoate WJ, Chipchase SY, Ince P, Game FL. Assessing the outcome of the management of diabetic foot ulcers using ulcer-related and person-related measures. Diabetes Care. 2006;29:1784–1787.[Abstract/Free Full Text]
  46. Budiman-Mak E, Conrad KJ, Roach KE. The Foot Function Index: a measure of foot pain and disability. J Clin Epidemiol. 1991;44:561–570.[CrossRef][Web of Science][Medline]
  47. Reiber GE, Smith DG, Heagerty PJ, et al. Therapeutic footwear in patients with diabetes. JAMA. 2002;288:1231–1233.[Free Full Text]
  48. Radloff LS. The CES-D Scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385–401.[CrossRef]
  49. Cnaan A, Laird NM, Slasor P. Using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Stat Med. 1997;16:2349–2380.[CrossRef][Web of Science][Medline]
  50. del Aguila MA. Assessment of Physical Activity in Patients With Diabetes (Lower Extremities, DPAQ, Test Reliablity) [PhD dissertation]. Seattle, WA: University of Washington–Seattle; 1998.
  51. Lavery LA, Peters EJ, Williams JR, et al. Reevaluating the way we classify the diabetic foot: restructuring the diabetic foot risk classification system of the International Working Group on the Diabetic Foot. Diabetes Care. 2008;31:154–156.[Abstract/Free Full Text]
  52. Crawford F, Inkster M, Kleijnen J, Fahey T. Predicting foot ulcers in patients with diabetes: a systematic review and meta-analysis. QJM. 2007;100:65-–86.[Abstract/Free Full Text]
  53. Bravata DM, Smith-Spangler C, Sundaram V, et al. Using pedometers to increase physical activity and improve health: a systematic review. JAMA. 2007;298:2296–2304.[Abstract/Free Full Text]
  54. Khaw KT, Jakes R, Bingham S, et al. Work and leisure time physical activity assessed using a simple, pragmatic, validated questionnaire and incident cardiovascular disease and all-cause mortality in men and women: the European Prospective Investigation Into Cancer in Norfolk prospective population study. Int J Epidemiol. 2006;35:1034–1043.[Abstract/Free Full Text]
  55. Tanasescu M, Leitzmann MF, Rimm EB, Hu FB. Physical activity in relation to cardiovascular disease and total mortality among men with type 2 diabetes. Circulation. 2003;107:2435–2439.[Abstract/Free Full Text]
  56. Richardson C, Mehari K, McIntyre L, et al. A randomized trial comparing structures and lifestyle goals in an Internet-mediated walking program for people with type 2 diabetes. Int J Behav Nutr Phys Act. 2007;4:59.[CrossRef][Medline]
  57. Brand PW. Repetitive Stress on Insensitive Feet: The Pathology and Management of Plantar Ulceration in Neuropathic Feet. Carville, LA: US Department of Health, Education, and Welfare; 1975.
  58. Armstrong DG, Peters EJ, Athanasiou KA, Lavery LA. Is there a critical level of plantar foot pressure to identify patients at risk for neuropathic foot ulceration? J Foot Ankle Surg. 1998;37:303–307.[Medline]
  59. Kastenbauer T, Sauseng S, Sokol G, et al. A prospective study of predictors for foot ulceration in type 2 diabetes. J Am Podiatr Med Assoc. 2001;91:343–350.[Abstract/Free Full Text]
  60. Frykberg RG, Lavery LA, Pham H, et al. Role of neuropathy and high foot pressures in diabetic foot ulceration. Diabetes Care. 1998;21:1714–1719.[Abstract]
  61. Veves A, Murray HJ, Young MJ, Boulton AJ. The risk of foot ulceration in diabetic patients with high foot pressure: a prospective study. Diabetologia. 1992;35:660–663.[CrossRef][Web of Science][Medline]
  62. Mueller MJ, Zou D, Bohnert KL, et al. Plantar stresses on the neuropathic foot during barefoot walking. Phys Ther. 2008;88:1375–1384.[Abstract/Free Full Text]

Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?


This article has been cited by other articles:


Home page
ptjournalHome page
W T. Cade
Diabetes-Related Microvascular and Macrovascular Diseases in the Physical Therapy Setting
Physical Therapy, November 1, 2008; 88(11): 1322 - 1335.
[Abstract] [Full Text] [PDF]


Home page
ptjournalHome page
M. J Mueller, D. Zou, K. L Bohnert, L. J Tuttle, and D. R Sinacore
Plantar Stresses on the Neuropathic Foot During Barefoot Walking
Physical Therapy, November 1, 2008; 88(11): 1375 - 1384.
[Abstract] [Full Text] [PDF]


Home page
ptjournalHome page
J. S Brach, J. B Talkowski, E. S Strotmeyer, and A. B Newman
Diabetes Mellitus and Gait Dysfunction: Possible Explanatory Factors
Physical Therapy, November 1, 2008; 88(11): 1365 - 1374.
[Abstract] [Full Text] [PDF]


Home page
ptjournalHome page
D. R Sinacore, M. K Hastings, K. L Bohnert, F. A Fielder, D. T Villareal, V. P Blair III, and J. E Johnson
Inflammatory Osteolysis in Diabetic Neuropathic (Charcot) Arthropathies of the Foot
Physical Therapy, November 1, 2008; 88(11): 1399 - 1407.
[Abstract] [Full Text] [PDF]


Home page
ptjournalHome page
E. A. Gulve
Exercise and Glycemic Control in Diabetes: Benefits, Challenges, and Adjustments to Pharmacotherapy
Physical Therapy, November 1, 2008; 88(11): 1297 - 1321.
[Abstract] [Full Text] [PDF]


Home page
ptjournalHome page
M. J Mueller
People With Diabetes: A Population Desperate for Movement
Physical Therapy, November 1, 2008; 88(11): 1250 - 1253.
[Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Correction (v89,p1103)
Right arrow All Versions of this Article:
ptj.20080019v1
88/11/1385    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when Rapid Responses are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by LeMaster, J. W
Right arrow Articles by Conn, V. S
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by LeMaster, J. W
Right arrow Articles by Conn, V. S
Related Collections
Right arrow Skin Abnormalities and Diseases
Right arrow Therapeutic Exercise
Right arrow Randomized Controlled Trials
Right arrow Diabetes
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?