Failure of negative-pressure wound treatment to improve healing of chronic diabetic foot ulcers
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1 Failure of negative-pressure wound treatment to improve healing of chronic diabetic foot ulcers A randomized case-control trial with a 366-day follow-up Agnetha Folestad 1, Martin Ålund 2, Susanne Asteberg 2, H, Håkan Hallberg 3 and Jean Cassuto 4 1 Department of Orthopedic Surgery, CapioLundby Hospital, Göteborg, 2 Department of Orthopedic Surgery, Sahlgrenska University Hospital, Mölndal, 3 Wound management unit, Department of Surgery, Skövde Hospital, Skövde, 4 Orthopedic Research Unit, Sahlgrenska University Hospital/Mölndal and Göteborg University, Göteborg, Sweden. Correspondence: jean.cassuto@aniv.gu.se Postal address: Jean Cassuto, Orthopedic Research Unit, Staben, Hus U1, Sahlgrenska University Hospital, Mölndal, Sweden Tel: , Fax:
2 ABSTRACT Background and purpose Diabetic foot ulcers (DFU) have proven difficult to treat. Negative pressure wound therapy (NPWT) has been proposed to increase formation of granulation tissue. We investigated the effectiveness of NPWT versus standard wet dressings on time to wound closure, granulation, and patient satisfaction in diabetic patients with chronic foot ulcers. Methods Forty-four consecutive type 1 and 2 diabetic patients with foot ulcers that have failed to heal for 2 months were randomized into two groups. Group A received continuous NPWT for 27 days and group B was treated with standard wet dressings followed by wet dressings in both groups until wound closure or completion of the 366-day follow-up. Results the primary endpoint of the study (time to complete wound closure) showed no significant difference between groups (p=0.33) with a median time to complete closure being in controls 129 days and in the NPWT group 177 days. The proportion of patients reaching complete closure in the control group was 89% and in the NPWT group 71%. The secondary endpoint (time to 90 % granulation) was not significantly different between groups (p=0.82) and the median time to granulation was in controls 21 days and in the NPWT group 15 days. Differences in wound surface area and wound depth during the phase of active treatment (first 30 days) were not significant between groups. Interpretation Our results showing no significant differences between patients treated with traditional wet dressings versus NPWT during 3 weeks as for time to complete wound closure or time to 90 % wound does not support previous suggestions of the beneficial effects of NPWT in the treatment of chronic diabetic foot ulcers and support previous interpretation that sufficient evidence-based support for this technique is lacking to recommend NPWT as standard treatment. 2
3 INTRODUCTION Diabetes mellitus is a chronic metabolic disorder causing a multitude of dysfunctions of the innate and adaptive immune system and as a consequence is associated with a wide range of co-morbidities affecting the cardiovascular, neuronal and metabolic functions of the body. The high incidence of peripheral neuropathy and impaired circulation in the lower limbs paralleled by increased risk of infections due to insufficient immune defence, contribute to the high incidence of chronic lower-limb wound ulcers in diabetic patients. Hard to heal or chronic foot ulcers in diabetic patients (DFU) have proven to be one of the most challenging problems and are major cause for morbidity and amputations in this group of patients. There are more than 300 million diabetic patients in the world and the incidence of DFU in diabetic patients during a lifetime is believed to range between 5-25% with DFU being the main risk factor for subsequent limb amputation and expected to rise with increasing number of diabetic patients worldwide (Lavery et al., 2003; Mulder et al., 2014). Despite considerable efforts to create global standards for management of DFU (Game et al., 2012; Gottrup and Apelqvist, 2012; Peters et al., 2012), the rate of complete wound healing has been reported as low as 60% after a one-year treatment (Mulder et al., 2014). Standard treatment for DFU include debridement of necrotic tissue, mechanical off-loading and anti-bacterial treatment. Various types of dressings have evolved, being predominantly of two types, wet dressings aimed at preserving wound moisture without adding any active component to the wound environment such as hydrocolloids, foams or hydrogels and active dressings containing antimicrobial properties, protease inhibitors, collagen formulations or active bioengineered components believed to accelerate wound healing (Mulder et al., 2014). Negative pressure wound therapy has been used for the treatment of chronic wounds for almost two decades (Ramanujam et al., 2013) and was reported to improve healing rate and healing time of chronic foot ulcers in in diabetic patients (McCallon et al., 2000; Eginton et 3
4 al., 2003; Armstrong et al., 2005; Blume et al., 2008; Sepulveda et al., 2009; Lone et al., 2014). A significant problem with DFU is the extended period of time needed to reach complete wound healing which requires a long-lasting observational phase in order for enough patients to reach 100% wound healing by secondary intention. In the study by Armstrong et al (Armstrong et al., 2005) on NPWT contra wet dressings in postamputation wounds, the observational period was 112 days but still failed to have 30-50% of the patients reaching the primary endpoint of the study, complete wound healing. In the present randomized study we enrolled 48 diabetic patients with chronic DFU into two groups, one treated with continuous negative pressure wound therapy (NPWT) for 27 days and a control group treated with traditional wet dressings. Following the active phase, patients were monitored up to 366 days to minimizing the incidence of censored observations. 4
5 METHODS Approval The study was approved by the Review Board of Västra Götalands Regionen (EPN D-nr ). All the subjects provided informed consent before participating in the study. Patient selection and treatment procedures This 12-month randomized case-control study compared the effectiveness of NPWT versus traditional wet dressings in the treatment of chronic diabetic foot ulcers. Forty-four consecutive ambulatory men and women aged 18 years with diabetes type 1 or 2 admitted to Sahlgrenska University Hospital/Mölndal with a foot ulcer that had failed to heal for 2 months (stage 2 or 3 DFU as defined by Wagner s classification (Wagner, 1981) were randomly allocated into two groups each consisting of 22 patients (NPWT or wet dressings). Patient allocation was done by computer-aided randomization and was delivered in sealed envelopes to the team responsible for patient enrolment and treatment. Due to the nature of treatment, we were unable to blind the team treating the patients and harvesting data whereas the investigator handling the results and conducting the statistical analysis of data was unaware of to which group the patient had been allocated. Exclusion criteria were: Charcot arthropathy, foot ulcers others than diabetes related and patients on corticosteroids, immunosuppressive agents or chemotherapy. Moreover, patients with autoimmune or autoinflammatory skin disease (e.g. SLE, systemic fibrosis, sclerodermia, psoriasis) were excluded as were patients whose wound had been treated with NPWT or biologically active products in the past 30 days prior to study inclusion. After having been assigned to one of the two groups, the wounds of all the patients underwent sharp surgical debridement to remove nectrotic- and fibrinous tissue and slough. Off-loading treatment was provided for all patients 5
6 as recommended by the International Working Group of the Diabetic Foot (IWGDF) (Bus, 2012). NPWT or wet dressings We used the Vacuum Assisted Closure system (VAC, KCI,USA) which consists of a medical-grade, open-cell, sterile polyurethane ether foam dressing with a pore size between µm allowing for tissue growth and equal distribution of negative pressure throughout the wound surface. The polyurethane dressing is cut to fit the shape of the wound with the evacuation tube exiting parallel to the skin. The wound and 5 mm of the surrounding intact skin is covered with adhesive drape creating a closed environment with the proximal end of the tube connected to a canister for wound fluid collection which in turn was connected to an adjustable portable vacuum pump (model: ActiVAC, KCI)(Argenta and Morykwas, 1997). Sharp surgical debridement of the wound to remove necrotic- and fibrinous tissue and slough was performed when considered necessary throughout the study. Continuous negative pressure of 125 mm Hg was applied to the wound during 27 days with dressing changes every 72 hours according to guidelines supplied by KCI. Patients in the control group were treated with wet dressings (alginates, hydrocolloids, or hydrogels) with change of dressing every 72 hours. From day 27, when NPWT was interrupted, both groups were treated with wet dressings as required until complete wound closure or until completion of the 366-day followup period of observation. The primary endpoint of the study was to compare the time to complete wound closure achieved by the two treatment strategies. Complete wound closure was defined as total (100%) re-epithelialization of the wound area. Secondary endpoint was time to 90% granulation of the wound surface area measured by Visitrak (see below). All the patients in the study were subject to the following procedures: 6
7 Blood samples Venous blood was sampled on one occasion for routine analysis (Hemoglobin, thrombocyte count, white blood cell count, serum creatinine, CRP, SR, electrolytes, liver status and HbA1c) whereas blood for cytokine analysis (pre-chilled EDTA tubes immediately centrifuged at 3000xg for 10 minutes at 4 o C before being stored at -85 o C until analysis) was collected at inclusion, 3 days (d), 6d, 9d, 12d, 15d, 18d, 21d, 24d, 27d, 30d and subsequently every month until wound closure or until completion of the 366-day follow-up. Results from the cytokine analyses will be presented in separate studies. Photographs A digital macro photo (Nikon D80 with lens AF-S micro Nikkorr 105 mm 1:2,8) of the wound was taken at each visit immediately before and after tending to the wound at inclusion, 3 days (d), 6d, 9d, 12d, 15d, 18d, 21d, 24d, 27d and subsequently every month until wound closure or until completion of the 366-day follow-up. This was done for objective documentation of wound appearance and, when deemed necessary, a reexamination of the wound was done for verification of data such as percentage granulation. Skin sensitivity and toe pressure Skin sensitivity was measured bilaterally at inclusion on 4 different locations of the foot using the Semmes-Weinstein monofilament test (Weinstein, 1993; Olmos et al., 1995). The monofilament (10 g) was pressed against the skin and the patient s ability or inability to feel the sensation upon buckling of the monofilament was registered. Neuropathy was present if three or more sites were insensate to the monofilament. Toe blood pressure was measured bilaterally at inclusion using a specially designed cuff (Samuelsson et al., 1996). 7
8 Wound culture Two samples for assessing bacterial flora were taken from all the patients at inclusion from the bottom of the ulcer, one by means of a swab and another by means of a 4 mm punch biopsy (Gardner et al., 2006; Lipsky et al., 2012). Before obtaining a culture, the wound was thoroughly cleaned from contaminating materials such as slough, necrotic tissue or other residues by tissue debridement and sampling was done over viable tissue. A swab culture was performed using the z-track 10-point swab culture after irrigating the wound and moistening the swab with sterile saline. The deep-tissue biopsy was done by a trained provider. Identification of a pathogenic wound infection at inclusion and a decision to initiate systemic antibiotic therapy was based on clinical findings, such as odor, increased exudate and purulent or murky secretion, and was followed-up by wound cultures to isolate microbial species and determine their susceptibility or resistance to antibiotics. Based on microbial analysis, patients with clinical signs of infection received as narrow spectrum as possible. Patients with clinically uninfected wound at inclusion did not receive antibiotics. Patients on antibiotics at inclusion were allowed to stay on treatment postinclusion and were reevaluated based on combined clinical and microbiological assessment before decision was taken to interrupt or continue treatment. Wound measurements Wound area was measured by Visitrak Digital (Smith&Nephew) producing a visible record of the dimensions of a wound on a three-layer tracing film designed to minimize the risk of cross-contamination and secondary infection. The patient contact layer is sterile, and the clean layer used to record wound measurements was stored in the patient file. The digital tablet converts the line tracing into a true area measurement (cm 2 ) and was also used to calculate the degree of necrotic tissue, fibrin, granulation and epithelialization as % of the total wound 8
9 area. Measurement of Wound area started prior to initiation of NPWT/wet dressing treatment at inclusion and was done before and after wound debridement at every subsequent visit by the patient until wound closure or termination of study at 366 days. Wound depth measurements (mm) were done parallel to assessment of wound area by use of a sterile disposable depth indicator (Visitrak ). Wound measurements were done at inclusion and repeated every 72 hours until day 30 followed by measurements every 4 weeks until patient achieved complete wound closure or until end of study at 366 days postinclusion. In addition, we measured at each visit the percentage of wound area comprising of necrotic, fibirnous, granulation and epithelial tissue by means of Visitrac. Presence of visible fascia, tendon or bone in the wound was registered (yes/no) before and after each debridement. Only data obtained from the wound after debridement were used for presentation and statistical analysis. We also registered at each visit during the first 30 days of the study the presence of odor from the wound, the amount of wound exudate on a scale 0-3 (0=none, 1=scarce, 2=medium, 3=rich), the appearance of wound exudate (clear, purulent, sanguine, murky or other) and the appearance of the wound perimeter (normal, erythematous, macerated, edematous, intact vesicles, ulcerations). Pain assessment Ungraded visual analogue pain scales (VAS, with 0 being no pain and 100 being unbearable pain ) were used to monitor pain from the wound. Pain during the 72 hour intervals between wound dressings was monitored on 11 occasions, starting before NPWT/wet dressing treatment at inclusion and repeated every 72 h until 30 days postinclusion. Patient discomfort was similarly monitored by repeated VAS measurements to answer the question of (1) to what extent wound pain negatively affected every day quality of life (QOL) and (2) to what extent the off-loading treatment negatively affected QOL, with a scale ranging from where 0 was no discomfort and 100 was extreme discomfort. 9
10 Statistical methods The primary and secondary endpoints, as well as other variables of the study, were assessed by one investigator (JC) who was not involved in patient selection or treatment and was unaware to the treatment allocation of patients. The primary endpoint of the study, i.e. complete (100%) closure of the wound was evaluated by the Kaplan-Meier survival analysis followed by log rank test which takes into consideration censored data. Survival analysis is generally defined as a set of methods for analyzing data where individuals are followed over a specified time period (366 days in our study) and the outcome variable is the time until the occurrence of an event of interest, i.e. complete wound closure. The log rank test is based on the same assumptions as the Kaplan- Meier survival curve, namely that censoring is unrelated to prognosis, the survival probabilities are the same for subjects recruited early and late in the study, and the events happened at the times specified (Altman and Bland, 1998; Bland and Altman, 1998). The log rank test is a nonparametric test that uses a chi-square statistic to reject the null hypothesis assuming that the survival curves came from the same population and thus determines whether survival curves are significantly different between the two study groups but cannot provide an estimate of the difference in significance between the groups or a confidence interval. This test takes the whole follow up period into account and has the advantage of not requiring knowledge of the shape of the survival curve or the distribution of survival times (Altman and Bland, 1998; Bland and Altman, 1998). The secondary endpoint of the study was the time to reach 90% granulation of the wound surface area and was also analyzed by the Kaplan-Meier survival analysis followed by log rank test taking into consideration presence of censored data. 10
11 Moreover, we used the Mann-Whitney rank sum test to analyze significant differences between the two patient groups with regard to wound area at inclusion, at 15 days and 30 days after the start of NPWT. Differences in pain during the 3-day periods between change of dressings, the effect of wound pain on QOL and the effects of off-loading treatment on QOL were assessed by measuring the mean of VAS at each visit followed calculation of the mean value for the whole period of observation (30 days). The estimated mean of accumulated scores during 30 days was calculated for each patient and a statistical comparison of group means was done by Mann-Whitney rank sum test. Other differences between the groups were analyzed by Mann-Whitney rank sum test and are presented in Table 1. 11
12 RESULTS Clinical and demographic data are presented in Table 1. Two patients in the control group and one in the NPWT group interrupted participation before completing the first 30 days of active treatment and without wound closure and were therefore excluded. All study wounds, with the exception of one, healed by secondary intention, i.e. without surgical wound closure or use of biologically active products. One patient in the control group underwent bone chiseling after having completed the active phase and was able to remain in the study as scheduled. The causes and locations of the chronic foot ulcers of the study were: wound secondary to amputation of a toe (control/npwt: 2/2), heel (control/npwt: 5/6), toe (control/npwt: 7/7), plantar surface (control/npwt: 5/6). The primary end point of the study, time to complete (100%) closure of the wound, revealed no significant difference between the NPWT and control group (p=0.33)(fig 1). The proportion of patients with complete healing of the wound (100% closure) after 366 days was in the control group 89 % (17 out of 19) and in the NPWT group 71 % (15 out of 21). The median (range) time to complete closure was in the control group 129 days (40-366) and in the NPWT group 177 days (60-366) with difference not being significant (p=0.44). The secondary endpoint, i.e. time to reach 90 % granulation of the wound surface area, showed no significant difference between the groups (p=0.82) with differences in median and range between groups being in the control group 21 days ((9-366) and in the NPWT group 15 days (9-210). Difference in wound surface area and wound depth between the groups at inclusion and after 30 days showed wound surface area (cm 2 ) not to be significantly different between the groups at inclusion (p=0.86) or after 30 days (p=0.15) (Fig 3). Similarly, differences in wound depth between the groups were not significant at inclusion (p=0.24) or after 30 days (p=0.34) (Fig 12
13 4). Fig 5 illustrates changes in wound area over the entire period of observation with no statistical evaluation of differences between the groups. Bacterial wound culture by swab resulted in positive critical colonization in 8 controls and 9 NPWT patients whereas culture by deep-tissue punch biopsy yielded positive response in 9 controls and 11 NPWT patients. The number of patients receiving antibiotic treatment for their foot ulcer within one month of inclusion into the study was for controls: 18 and for NPWT: 20. Out of these, 12 patients in the control group continued to be treated with antibiotics postinclusion as compared to 17 in the NPWT group as judged from the clinical appearance of the wounds. The most common pathogens were s. aureus, enterococci and E. coli. The degree of mobility in the two study groups at inclusion showed the number of patients moving freely indoor and outdoor to be 13 in the control group and 11 in the NPWT group, 3 patients were confined to wheelchair in the control group and 6 in the NPWT group with the rest of the patients using various kinds of crutches (5 in each group). All the patients received off-loading intervention upon inclusion in the study. The choice of off-loading footwear followed the guidelines at our clinic and included removable cast walkers (control/npwt: 8/8), heal- or forefoot off-loading shoes (control/npwt: 6/4) or cast shoe (control/npwt: 5/9). The estimated mean of accumulated pain scores between changes of wound dressings during the active phase (first 30 days) was in control patients 9±2 and in NPWT 4±1 (p=0.14). VAS scores for the effect of wound pain on QOL was in controls 5±2 and in the NPWT group 6±3 (p=0.78) and the effect of off-loading treatment was in controls 23±5 and in NPWT 30±4 (p=0.22). 13
14 DISCUSSION In comparison with previous studies investigating the effects of NPWT on the treatment of diabetic foot ulcers over time, our study groups were similar to some previous studies (Sepulveda et al., 2009; Lone et al., 2014) and smaller than other (Armstrong et al., 2005; Blume et al., 2008). However, our observation time was significantly longer than that of the longest previous studies which followed the patients between days (Armstrong et al., 2005; Blume et al., 2008). We chose this strategy to maximize the number of patients reaching the primary endpoint of the study, i.e. time to complete wound closure, thereby allowing us to draw conclusions on the actual events. In previous studies (Armstrong et al., 2005; Blume et al., 2008), the authors reported an incidence of censored observations amounting to between %. Diskussion under arbete 14
15 LEGENDS Figure 1 Kaplan-Meier estimates followed by log rank test for time to complete wound closure. Numbers at risk at conclusion of treatment was 6 NPWT and 2 controls. P=0.33. Figure 2: Kaplan-Meier estimates followed by log rank test for time to reach 90 % granulation of total wound surface area. Numbers at risk at termination of treatment was for controls 2 and for NPWT 0. P=0.82 Figure 3: Wound surface area (cm 2 ) during 30 days after inclusion in patients receiving continuous negative pressure treatment during 27 days (NPWT, n=21) and a corresponding control group treated with traditional wet dressings (Control, n=19). Differences between the groups were not significant at inclusion (p=0.86) or after 30 days (p=0.15). Figure 4: Wound depth (cm) during 30 days after inclusion in patients receiving continuous negative pressure treatment during 27 days (NPWT, n=21) and a corresponding control group treated with traditional wet dressings (Control, n=19). Differences between the groups were not significant at inclusion (p=0.24) or after 30 days (p=0.34). Figure 5: Wound surface area (cm 2 ) monitored during 12months (366 days) in the control group treated with wet dressings throughout the observation period and in the NPWT group treated with continuous NPWT during the initial 27 days and subsequently with wet dressings until patients reached complete wound closure or until study termination. 15
16 Table 1. Clinical and demographic data Control patients (n=19) VAC patients (n=21) P-value Age (years), Median (range) 67 (36-91) 74 (44-93) Females/Males (n) 5/16 4/18 Weight (kg) 86±4 88±3 Height (cm) 178±2 179±2 Diabetes type 1/2 (n) 7/17 7/15 Diabetes duration (years) 29±2 33±4 Peripheral neuropathy (n) Insulin/only oral/insulin+oral antidiabetics (n) 17/2/4 16/2/4 Anticoagulants (n) 1 5 Nicotine users (n) 11 4 Systolic blood pressure (mmhg) Diastolic blood pressure (mmhg) 140 ± 5 76 ± ± 4 75 ± 2 Arterial toe pressure (mmhg) 105 ± 9 90 ± 6 Toe Brachial Pressure Index 0.71 ± ± 0.03 Wound history (months) 16 ± ± 1.8 Retinopathy/nephropathy (n) 13/6 12/4 Hb (g/l) S-CRP (mg/l) SR (mm) S-Kreatinin (µmol/l) Leucocyte count Thrombocyte count B-glucose HbA1c (mmol/mol) HbA1c (%) 133 ± 3 12 ± 2 31 ± ± 30 8 ± ± ± 1 63 ± ± ± 3 16 ± 3 24 ± ± 10 8 ± ± 27 8 ± 1 59 ± ±
17 Figure 1 1,0 Control NPWT 0,8 Survival Distribution Estimate 0,6 0,4 0,2 0, Time to complete closure of foot ulcer (days) Visit (days) Numbers at risk NPWT Control
18 Figure 2 1,0 Control NPWT 0,8 Survival Distribution Estimate 0,6 0,4 0,2 0, Time to 90% granulation of wound surface area (days) Visit (days) Numbers at risk NPWT Control
19 Figure Control NPWT Wound surface area (cm 2 ) Continuous NPWT treatment (-125 mm Hg) Inclusion Time after inclusion (days) 19
20 Figure 4 3,0 2,5 Control NPWT Wound depth (mm) 2,0 1,5 1,0 0,5 Continuous NPWT treatment (-125 mm Hg) 0,0 Inclusion Time after inclusion (days) 20
21 Figure Wound area surface (cm 2 ) Wet dressings NPWT 0 NPWT Incl Time after inclusion (months) 21
22 Contributions of authors AF, HH, SA and JC designed the study. SA, MÅ and HH treated the patients and collected the clinical data and samples. JC carried out the statistical analysis and wrote the manuscript. All authors contributed to the intellectual contents of the manuscript. Acknowledgements Financial support was obtained from VästraGötalandsRegionen, VGRFOU (grants# and ). No financial support was received from any industrial company. KCI supplied 3 pumps for the study without any commitments on the part of the investigators (KCI had no access to study protocol, data, statistics, conclusions or manuscript). Conflicts of interest The authors declare no conflict interests Corresponding author Jean Cassuto 22
23 References Altman DG, Bland JM Time to event (survival) data. Bmj 317: Argenta LC, Morykwas MJ Vacuum-assisted closure: a new method for wound control and treatment: clinical experience. Annals of plastic surgery 38: ; discussion 577. Armstrong DG, Lavery LA, Diabetic Foot Study C Negative pressure wound therapy after partial diabetic foot amputation: a multicentre, randomised controlled trial. Lancet 366: Bland JM, Altman DG Survival probabilities (the Kaplan-Meier method). Bmj 317:1572. Blume PA, Walters J, Payne W, Ayala J, Lantis J Comparison of negative pressure wound therapy using vacuum-assisted closure with advanced moist wound therapy in the treatment of diabetic foot ulcers: a multicenter randomized controlled trial. Diabetes care 31: Bus SA Priorities in offloading the diabetic foot. Diabetes/metabolism research and reviews 28 Suppl 1: Eginton MT, Brown KR, Seabrook GR, Towne JB, Cambria RA A prospective randomized evaluation of negative-pressure wound dressings for diabetic foot wounds. Annals of vascular surgery 17: Game FL, Hinchliffe RJ, Apelqvist J, Armstrong DG, Bakker K, Hartemann A, Londahl M, Price PE, Jeffcoate WJ A systematic review of interventions to enhance the healing of chronic ulcers of the foot in diabetes. Diabetes/metabolism research and reviews 28 Suppl 1: Gardner SE, Frantz RA, Saltzman CL, Hillis SL, Park H, Scherubel M Diagnostic validity of three swab techniques for identifying chronic wound infection. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society 14: Gottrup F, Apelqvist J Present and new techniques and devices in the treatment of DFU: a critical review of evidence. Diabetes/metabolism research and reviews 28 Suppl 1: Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJ Diabetic foot syndrome: evaluating the prevalence and incidence of foot pathology in Mexican Americans and non- Hispanic whites from a diabetes disease management cohort. Diabetes care 26: Lipsky BA, Peters EJ, Senneville E, Berendt AR, Embil JM, Lavery LA, Urbancic-Rovan V, Jeffcoate WJ Expert opinion on the management of infections in the diabetic foot. Diabetes/metabolism research and reviews 28 Suppl 1: Lone AM, Zaroo MI, Laway BA, Pala NA, Bashir SA, Rasool A Vacuum-assisted closure versus conventional dressings in the management of diabetic foot ulcers: a prospective case-control study. Diabetic foot & ankle 5. McCallon SK, Knight CA, Valiulus JP, Cunningham MW, McCulloch JM, Farinas LP Vacuumassisted closure versus saline-moistened gauze in the healing of postoperative diabetic foot wounds. Ostomy/wound management 46:28-32, 34. Mulder G, Tenenhaus M, D'Souza GF Reduction of diabetic foot ulcer healing times through use of advanced treatment modalities. The international journal of lower extremity wounds 13: Olmos PR, Cataland S, O'Dorisio TM, Casey CA, Smead WL, Simon SR The Semmes-Weinstein monofilament as a potential predictor of foot ulceration in patients with noninsulindependent diabetes. The American journal of the medical sciences 309: Peters EJ, Lipsky BA, Berendt AR, Embil JM, Lavery LA, Senneville E, Urbancic-Rovan V, Bakker K, Jeffcoate WJ A systematic review of the effectiveness of interventions in the management of infection in the diabetic foot. Diabetes/metabolism research and reviews 28 Suppl 1: Ramanujam CL, Stapleton JJ, Zgonis T Negative-pressure wound therapy in the management of diabetic Charcot foot and ankle wounds. Diabetic foot & ankle 4. 23
24 Samuelsson P, Blohme G, Fowelin J, Eriksson JW A new non-invasive method using pulse oximetry for the assessment of arterial toe pressure. Clinical physiology 16: Sepulveda G, Espindola M, Maureira M, Sepulveda E, Ignacio Fernandez J, Oliva C, Sanhueza A, Vial M, Manterola C [Negative-pressure wound therapy versus standard wound dressing in the treatment of diabetic foot amputation. A randomised controlled trial]. Cirugia espanola 86: Wagner FW, Jr The dysvascular foot: a system for diagnosis and treatment. Foot & ankle 2: Weinstein S Fifty years of somatosensory research: from the Semmes-Weinstein monofilaments to the Weinstein Enhanced Sensory Test. Journal of hand therapy : official journal of the American Society of Hand Therapists 6:11-22; discussion
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