The aim was to compare three ulcer classification systems as predictors of the outcome of diabetic foot ulcers: the Wagner, the University of Texas (UT) and the size (area, depth), sepsis, arteriopathy, denervation system (S(AD)SAD) systems in a specialist clinic in Brazil.
Ulcer area, depth, appearance, infection and associated ischaemia and neuropathy were recorded in a consecutive series of 94 subjects. A novel score, the S(AD)SAD score, was derived from the sum of individual items of the S(AD)SAD system, and was evaluated. Follow-up was for at least 6 months. The primary outcome measure was the incidence of healing.
Mean age was 57.6 years; 57 (60.6%) were male. Forty-eight ulcers (51.1%) healed without surgery; 11 (12.2%) subjects underwent minor amputation. Significant differences in terms of healing were observed for depth (P=0.002), infection (P=0.006) and denervation (P=0.002) using the S(AD)SAD system, for UT grade (P=0.002) and stage (P=0.032) and for Wagner grades (P=0.002). Ulcers with an S(AD)SAD score of ≤9 (total possible 15) were 7.6 times more likely to heal than scores ≥10 (P<0.001).
All three systems predicted ulcer outcome. The S(AD)SAD score of ulcer severity could represent a useful addition to routine clinical practice. The association between outcome and ulcer depth confirms earlier reports. The association with infection was stronger than that reported from the centres in Europe or North America. The very strong association with neuropathy has only previously been observed in Tanzania. Studies designed to compare the outcome in different countries should adopt systems of classification, which are valid for the populations studied.
Foot ulcers are a common complication of diabetes and represent a major source of morbidity (1, 2, 3, 4, 5, 6, 7, 8, 9). Early expert assessment and treatment are required to reduce the impact of the condition and to reduce the incidence of major amputation. The incidence of major amputation has been described, as ‘a marker not just of disease but also of disease management’ (10).
A number of foot ulcer classification systems have been devised in an attempt to categorize ulcers more effectively, and thereby allow effective comparison of the outcome of routine management in different centres and treatment strategies. These systems are variously based on the site of ulcer, depth, presence of neuropathy, infection and peripheral arterial disease, and have been used to compare the outcomes (10, 11, 12, 13, 14). To be useful, a system should be easy to apply, and robust enough to permit reliable classification of all ulcers encountered in routine practice (10, 11, 12, 13, 14). The two most widely used ulcer classification systems are: the Wagner (15) and the University of Texas (UT) systems (16). The size (area, depth), sepsis, arteriopathy, denervation system (S(AD)SAD) was described more recently (17). The S(AD)SAD system differs from the earlier ones by including reference to both ulcer area and neuropathy, and has been validated by demonstrating differences between different baseline variables and clinical outcome in a single centre in the UK (18). The International Working Group on the Diabetic Foot has also suggested a classification for the purposes of prospective research which is based on the same five elements as S(AD)SAD (19), but this system is potentially more complex and is primarily intended for selecting populations for prospective research, and was also not available when this study was planned.
Data were collected prospectively on subjects presenting with diabetic foot ulcers in the period from 1 December 2003 to 31 December 2005 to the specialist multidisciplinary unit at the Endocrinology Division, State University of Campinas, Brazil. All were followed for at least 6 months, or until amputation or death. Management was supervised by an endocrinologist, a specialist trainee, a consultant vascular surgeon, a consultant orthopaedic surgeon, a diabetes specialist nurse, an orthotist and a plaster theatre comprised the health care professionals. If a subject had multiple ulcers at the same time, the most significant (generally the largest) was selected as the index ulcer for the purposes of the study. Each subject was included only once in the study.
The presence of neuropathy was determined using vibration perception (128 Hz tuning fork) at two sites (hallux pulp and malleolus), point pressure (Semmes–Weinstein 10 g monofilament) at seven sites and ankle reflexes (20). The adequacy of arterial blood supply to the foot was determined by palpation of the dorsalis and posterior tibial foot pulses. If the pulses were diminished or impalpable, the ulcers were classified as ischaemic (UT stage C; S(AD)SAD arteriopathy 1 plus 2). The lesion was classified as S(AD)SAD 3 if neither pedal pulse was palpable or if the ankle brachial pressure index (ABPI) was <0.9 (20, 21, 22).
Ulcer depth was judged by inspection and graded as: intact skin, superficial lesion, lesion reaching to tendon, periosteum or joint capsule, and lesion involving bone or joint space. The diagnosis of infection was based on clinical parameters including the presence of inflammation, purulent exudate and a positive probe to bone test. These data were sufficient to allow classification of each ulcer by the three systems mentioned above (Tables 1–3). Ulcers were also graded retrospectively by a novel scoring system derived from the individual component of the S(AD)SAD system. The S(AD)SAD system classifies each of its five components ((AD)SAD) on a scale of 0–3, and the score was derived by totaling them, with a maximum possible score of 15. Demographic data such as gender, age, diabetes duration, smoking habit, hypertension and history of cardiovascular and cerebrovascular disease, and other chronic complications of diabetes were also recorded.
|Grade 0||Pre- or post-ulcerative site|
|Grade 1||Superficial ulcer|
|Grade 2||Ulcer penetrating to tendon or joint capsule|
|Grade 3||Lesion involving deeper tissues|
|Grade 4||Forefoot gangrene|
|Grade 5||Whole foot gangrene involving more than two-thirds of the foot|
The University of Texas (UT) system.
|Grade 0||Grade 1||Grade 2||Grade 3|
|Pre- or post-ulcerative site||Superficial wound not involving tendon, capsule, or bone and grade||Wound penetrating to tendon or capsule||Ulcer penetrating to bone or joint|
|Lesions without infection or ischaemia|
|Ischaemic infected lesions|
|0||Skin intact||Skin intact||Pedal pulses present||Intact|
|1||Lesion <1 cm2||Superficial (skin and s.c. tissue)||No infected lesions||Pedal pulses reduced or one missing||Reduced|
|2||Lesion from 1 to 3 cm2||Lesion penetrating to tendon, periosteum and joint capsule||Cellulitis-associated lesions||Absence of both pedal pulses||Absent|
|3||Lesion >3 cm2||Lesion in bones or joint space||Lesions with osteomyelitis||Gangrene||Charcot joint|
Callus and necrotic tissue was removed by sharp debridement. The ulcerated area was off-loaded using a total contact cast or individually designed cushioned footwear. Revascularization (angioplasty or reconstruction) was undertaken when indicated and if possible. The subjects were seen at intervals of between 1 and 4 weeks. The primary outcome measure was incidence of ulcer healing, with or without minor amputation after at least 6-month follow-up. Secondary outcome measures included incidence of major and minor amputation.
Continuous descriptive variables are presented as mean, s.d., minimum, maximum and median values. The association between two categorical variables was analysed by either χ2 or Fisher's test. Mann–Whitney test was performed to compare numerical variables between the two groups. For logistic regression analysis, the logit model was used to analyse the relation between baseline variables and ulcer healing. Multivariate analysis was carried out using stepwise inclusion of the selected variables. Ulcer duration was evaluated using Kaplan–Meier survival analysis and the accuracy of prediction of ulcer outcome was compared in the three classification systems using the log-rank test. The significance level was set at 5% (P<0.05). Statistical analyses were performed using the statistical analysis system (SAS) for Windows, version 8.02 (SAS Institute Inc., 1999–2001, Cary, NC, USA).
This study was approved by the National Research Ethics Commission in Brazil.
In the 24-month period, 105 individuals with diabetic foot ulcers were evaluated on the foot ulcer unit. Data from 11 were incomplete and these were excluded from the analysis. Baseline clinical features on the remaining 94 are given in Table 4. Complete healing without surgery was observed in 48 (51.1%) by 6 months, and 11 (12.2%) underwent minor amputation. There were no major amputations. None were lost to follow-up and none died. Ulcer survival analysed by Kaplan–Meier showed a median time to healing of 5.0±0.8 months (95% CI: 3.5–6.5). 5.9%±2.6% healed by 1 month, and 31.8%±5.1% and 56.5%±5.4% by three and 6 months respectively.
Baseline characteristics of subjects with diabetic foot and ulcer.
|Subjects (n=94)||n (%)|
|Age (years)||57.61±12.44 (13–89)|
|Duration of diabetes (years)||16.91±8.16 (2–40)|
|Diabetic retinopathy||63 (73.3%)|
|Diabetic nephropathy||55 (62.3%)|
|Cardiovascular disease||30 (33%)|
|Distal sensory neuropathy||55 (58.5%)|
|Peripheral arterial disease|
|Ischaemia (pulses diminished or impalpable)||34 (36.2%)|
|Severe ischaemia (pulses impalp able and/or ABPI <0.9)||5 (5.3%)|
|Plantar ulcer||89 (94.6%)|
|Dorsal ulcer||5 (5.4%)|
There were no differences between those who did and did not heal in terms of gender (P=0.64), age at diagnosis (P=0.52) or duration of diabetes (P=0.49). Using the S(AD)SAD classification, there was no difference in outcome between baseline classification groups for area (P=0.16) and ischaemia (P=0.10). However, there were differences between groups in other baseline parameters, with non-healing ulcers being more deep (P<0.001), more likely to be infected (P<0.001) and associated with distal symmetrical neuropathy (P=0.013). Differences were also observed between the grades of the Wagner system (P<0.001) as well as both UT stage (P=0.015) and grade (P<0.001). Table 5 shows the comparison results between the groups that did and did not heal, according to the three classification systems.
Healing probability according to ulcer classification system: S(AD)SAD (A), University of Texas (B) and Wagner (C).
|Area grade||Depth grade||Sepsis grade||Arteriopathy grade||Denervation grade||Healing probability (%)|
|(A) S(AD)SAD variables|
|SAD score ≥10||20.0|
|SAD score ≤9||65.6|
|Grade||Stage||Healing probability (%)|
|(B) UT variables|
|Grade||Healing probability (%)|
|(C) Wagner variables|
Significant differences in numbers healed by 6 months were observed between groups for depth (P=0.002), infection (P=0.006) and denervation (P=0.002), when classified by the S(AD)SAD system (log rank), and also between groups for UT grade, which uses criteria identical to S(AD)SAD depth (P=0.002) and stage (P=0.032), as well as for Wagner grades (P=0.002). No differences were observed between groups for either ulcer area (P=0.444) or arteriopathy (P=0.152) classified using the S(AD)SAD system.
Multivariate logistic regression was performed to determine which items of each system were independently associated with healing. Subjects with UT stage A ulcers had a 4.6 times greater chance of healing at 6 months than those with stage D ulcers (P=0.014; OR=4.6, 95% CI: 1.37–15.49). However, no differences were observed between stage D ulcers and either stage B (P=0.433; OR=1.68; 95% CI: 0.46–6.11) or stage C (P=0.219; OR=2.26, 95% CI: 0.62–8.32) ulcers. Ulcers classified as UT grade 1 were 2.9 times more likely to heal when compared with grades 2 and 3 combined (P=0.035; OR=2.87, 95% CI: 1.08–7.64). For healing prediction, grade and stage by the UT system were evaluated simultaneously and a confidence agreement coefficient was obtained (c=0.723). Wagner grade 1 ulcers were 3.5 times more likely to heal than levels 2 and 3 combined (P=0.008; OR=3.48, 95% CI: 1.38–8.76; c=0.631), similar to UT grade. Using multivariate analysis, ulcers classified as having sepsis 0 or 1 by the S(AD)SAD system were 4.26 times more likely to heal than those that were clinically infected (grade 2 or 3) (P=0.001; OR=4.26, 95% CI: 1.77–10.26; c=0.668).
Assessment of the S(AD)SAD score indicated that those with a score ≤9 at baseline predicted healing within 6 months with a sensitivity of 87.5%, specificity 52.2% and accuracy 70.2%. Multivariate logistic regression revealed that an S(AD)SAD score ≤9 was associated with a 7.6-fold increase in the incidence of healing (P<0.001; OR=7.64, 95% CI: 2.72–21.45). Healing probability for each ulcer classification system is described in Table 4. The comparison among the assessments of ulcer survival in relation to healing (log rank) showed that for SAD score ≤9, the mean healing time was 6.9±0.7 months (95% CI: 5.6–8.2, median 5.0±0.6, 95% CI: 3.9–6.1). In 22 ulcers with an S(AD)SAD score ≥10 and which eventually healed, the mean time to healing was 28.2±3.4 months (range 2–38). The percentage of ulcers with an S(AD)SAD score ≤9 and which healed by 6 months was 65.6%, compared with 20.0% for those with an S(AD)SAD score >10 (P<0.001).
Data on the burden of diabetes-related complications from developing countries are relatively rare and comparisons between them are made difficult by differing degrees of population selection and by the use of different clinical methods (23). Despite a number of local initiatives to improve access to foot care, the vast majority of people with diabetes in developing countries do not have access (24). The report by the Centers for Disease Control and Prevention (CDC) on geographic disparities in diabetes-related amputations on the Texas–Mexico border reported that incidence of diabetes-related amputations of lower extremity in this area was nearly double the rate of non-border countries (25). Wide differences between other centres have also been reported (10). In order to identify the reasons for such differences, it is necessary to compare the outcomes of clinical care in different populations, both between centres and between countries, and this requires careful definition of the populations selected for the study. A robust system of ulcer classification is necessary for this purpose.
A number of groups have used classification schemes to seek associations between baseline variables and clinical outcome, but the results have been inconsistent. Armstrong and colleagues (16) reported a significant association between outcome and ulcers of increasing depth (UT grade), and especially in the presence of ischaemia, infection or both (UT stage). This study was limited, however, in using just a linear-by-linear association for analysis, and by the use of amputation (which should properly be regarded as a treatment rather than a clinical endpoint), as the single outcome measure. This could have influenced the results if, for instance, amputation was established as the treatment of choice for certain types of lesion, such as osteomyelitis (10).
A close association was later shown between the results of the UT system and the earlier Wagner classification (26). In contrast to the report by Armstrong et al. (16), however, Treece and colleagues (18) found no association between infection and any outcome measure (healing, non-healing, amputation, death), although differences were observed between ulcer area, depth and the presence or not of peripheral arterial disease (PAD). The same group has recently confirmed these findings, reporting that the dominant factors influencing healing in a UK population were ulcer area and the presence of ischaemia (27).
In the present study ulcers were classified using the Wagner, UT and S(AD)SAD systems, and differences were observed in the occurrence of healing between baseline groups with each. The three classifications performed equally well. However, multiple logistic regression analysis demonstrated that among the five factors classified by the S(AD)SAD classification, the absence of infection was the most relevant factor, increasing the likelihood of healing 4.3 times. No effect of arteriopathy was found using either the S(AD)SAD classification or stages 2 and 4 in the UT system, and this contrasts with published work from North America and Europe (16, 18, 26, 27, 28). The failure to demonstrate an association between healing and arteriopathy in the studied population probably reflects the very low prevalence of severe PAD in this population (5.3%). By contrast, the profile was similar to that encountered in countries with similar economic status, in which the prevalence of ischaemia has also been reported to be low and in which infection was the factor most closely associated with outcome (29, 30, 31, 32). The independent association noted between neuropathy and outcome has also been reported very recently in a similar study undertaken in Tanzania (32). These results reinforce the importance of taking note of regional differences when making comparisons between different centres. Systems of classification, which are validated in one group, may not be applicable to all others.
We have also shown that the novel S(AD)SAD score could add a new dimension to the use of the S(AD)SAD system, with scores of ≤9 predicting healing within 6 months, with an accuracy of ∼70%. Ulcers scoring ≤9 were 7.6 times more likely to heal in 6 months than those with greater scores. A score of ≤9 had positive and negative predictive values for healing within 6 months of 65% and 80% respectively. Beckert et al. (28) have also recently described a scoring system for foot ulcers (diabetic ulcer severity score (DUSS)), and have applied it to a very large consecutive cohort managed in Germany, where they found that healing was independently associated with PAD, ulcer depth and site, and ulcer number. A lower DUSS score was strongly associated with healing.
In conclusion, these data indicate that although the overall percentage of ulcers healed by 6 months is similar to that reported in studies undertaken in Europe and North America (18, 29, 30, 31, 33), the population differed both in the types of ulcer managed and the baseline variables, which were most closely associated with outcome. Care should be used to ensure that any future studies that compare the outcome of management between different centres and countries should adopt systems of classification, which are valid for the populations studied. Effective comparison between widely differing populations may require that all five of the baseline criteria of the S(AD)SAD (and perfusion, extent/size, depth/tissue loss, infection and sensation, PEDIS) systems are used to characterize them, and the new S(AD)SAD score may be useful tool for this purpose.
Declaration of interest
The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.
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