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ageing, foot ulcer location, diabetes mellitus, elderly, diabetic foot ulcers
Patrícia Rosinha , Miguel Saraiva, Lia Ferreira, Susana Garrido, André Carvalho, Cláudia Freitas, Cláudia Amaral, Luís Costa, Luís Loureiro, Rui Carvalho
Published: August 19, 2022 (see history)
DOI: 10.7759/cureus.28189
Cite this article as: Rosinha P, Saraiva M, Ferreira L, et al. (August 19, 2022) A Retrospective Cohort Study on Diabetic Foot Disease: Ascertainment of Ulcer Locations by Age Group. Cureus 14(8): e28189. doi:10.7759/cureus.28189
Diabetic foot ulcer location is a known independent predictor for cure with a better healing gradient proximal to distal. Although advanced age is one of the main factors associated with greater diabetic foot ulcer severity, there are no studies evaluating diabetic foot ulcer location specifically in the elderly population in an outpatient setting. This study evaluated diabetic foot ulcer location and age-group interactions in diabetic foot presentation.
A retrospective cohort study including adult patients with diabetic foot ulcers observed on their first visit to our center’s Diabetic Foot Unit in 2018, divided into younger adults (YA) (18 to 64 years) and older adults (OA) (≥65 years).
A total of 435 patients were included in the study with 159 (36.6%) in the YA, and 276 (63.4%) in the OA group.
Neuro-ischemic diabetic foot ulcers were more frequent in the OA group (71.4% vs 43.4%, p<0.001). The number of patients with a history of diabetic foot ulcers was lower in the OA group (18.1% vs 25.2%, p=0.03). A smaller proportion of forefoot diabetic foot ulcers (74.9% vs 86.2%, p=0.007) and plantar location diabetic foot ulcers (9.4% vs 24.5%, p<0.001) occurred in the OA group.
By univariate logistic regression analysis, we found two associations with older age: proximal (odds ratio (OR) 2.09 (1.23-3.53), p=0.006), and non-plantar (OR 3.13 (1.82-5.37), p<0.001) diabetic foot ulcer location. After adjusting for potential confounders in a multivariate analysis, older age lost the association to more proximal (OR 1.72 (0.94-3.15), p=0.081) and non-plantar (OR 1.78 (0.83-3.77), p=0.133) diabetic foot ulcer location.
There are essential age differences in diabetic foot ulcer presentation. The OA group more frequently presents neuro-ischemic diabetic foot ulcers with more proximal and non-plantar locations.
Diabetic foot disease is a chronic complication of diabetes mellitus (DM) defined as foot ulceration associated with neuropathy and different grades of ischemia and infection, whose incidence has been increasing in proportion with the worldwide prevalence of DM [1,2]. Diabetic foot ulcers are important not only because of the high mortality associated with them but also due to the reduction in quality of life and inherent costs [2,3].
The improvement of living conditions and advances in science and medicine in recent years have led to an increase in average life expectancy, with subsequent aging of the population [4]. It is known that during the physiological process of senescence, important changes occur, namely loss of muscle mass and function, increased joint stiffness, reduced range of motion, and changes in gait/balance, phenomena that can be translated into mobility limitation and considerable functional disability [5].
Previous studies also have shown that advanced age is one of the main factors associated with greater severity of diabetic foot ulcers [1,6]. There is also evidence to demonstrate that diabetic foot ulcer location is a known independent predictor for cure with a better healing gradient proximal to distal [7]. No studies evaluating diabetic foot ulcer location specifically in the elderly population in an outpatient setting have been published.
Thus, our study’s aim was to evaluate diabetic foot ulcer location and age interactions in diabetic foot presentation in order to better understand the diabetic foot ulcer location effect on prognosis over different age groups.
The results of this study were previously presented as a meeting abstract at the International Diabetes Federation Congress 2021 on December 6 to 11, 2021.
This is a retrospective observational study including 583 adult patients with diabetic foot ulcers observed on their first visit to the Diabetic Foot Unit of Centro Hospitalar Universitário do Porto, a tertiary care unit in Northern Portugal, during the year 2018. A total of 148 patients were excluded: 59 with no active diabetic foot ulcer and 89 lacking information on clinical records. The final sample of 435 patients was divided into two groups by age at diabetic foot ulcer presentation i.e., younger adults (YA) at 18 to 64 years, and older adults (OA) ≥ 65 years.
Data concerning demographic/clinical information, aspects related to diabetic foot ulcers, and their classification were collected from the electronic clinical record and entered into a database without any patient identifiers. Smoking habits were considered if there was a history of current or previous use. The value of glycated hemoglobin (HbA1c) was determined at the first visit using an HbA1c analyzer. Diabetic foot ulcer location was assessed anatomically (categorized as forefoot and midfoot or above) and according to the surface (plantar and non-plantar) and lateralization (right and left). For diabetic foot ulcer classification, each ulcer was graded/scored using three different scales: the perfusion, extent, depth, infection, sensation (PEDIS)/Infectious Diseases Society of America (IDSA) classification; University of Texas system classification; and Wagner’s classification (Table 1) [8,9].
DFU: Diabetic foot ulcer, IDSA: Infectious Diseases Society of America, PEDIS: Perfusion, extent, depth, infection, sensation
The study protocol was in conformance with the World Medical Association’s Helsinki Declaration and was approved by the Ethics Committee of Centro Hospitalar Universitário do Porto (approval number: 2021.160 (131-DEFI/134-CE)). Informed consent was waived by the Ethics Committee based on the retrospective nature of the study and full data anonymization.
Data analysis was performed using the Statistical Package for Social Sciences (SPSS) version 20 (IBM Corp., Armonk, NY, USA). Categorical variables are presented as frequencies and percentages and continuous variables as means and standard deviations (SD) or medians and interquartile ranges (IQR) for variables with skewed distributions. Normal distribution was checked using the Shapiro-Wilk test or skewness and kurtosis, as appropriate. Categorical variables were compared with Pearson’s chi-square test or Fisher’s exact test. Continuous variables were compared with the t-test for independent samples or the Mann-Whitney U test (if skewed distribution). Binary logistic regression was used to evaluate the presence of an association between older age and diabetic foot ulcer location, by adjusting for possible confounders. Anatomic location of diabetic foot ulcers and surface of diabetic foot ulcers were considered dependent variables in separate analyses. Independent variables included in diabetic foot ulcer surface analysis were the study group (YA/OA) and the following potential confounders: gender, level of education, dyslipidemia, nephropathy, and cerebrovascular disease. Independent variables included in diabetic foot ulcer anatomic location analysis were the study group (YA/OA) and the following potential confounders: gender, smoking habits, and motor autonomy. All reported p-values are two-tailed, with p<0.05 indicating statistical significance.
A total of 435 patients were included in this study with 159 (36.6%) in the YA (18-64 years) and 276 (63.4%) in the OA (≥ 65 years) group. The percentage of elderly people aged 75 or over was 61.6% in this sample.
The results are presented in the following Tables. Table 2 shows that the younger group had statistically more men (78.6% vs 52.5%, p<0.001), more smokers (49.1% vs 24.6%, p<0.001), more mobility (84.3% vs 60.1%, p<0.001) and higher levels of education (42.8%/33.3%/6.3% vs 72.5%/9.8%/1.1%, p<0.001). Type 2 DM was more common in older individuals (93.8% vs 78.6%, p<0.001), with a higher mean DM duration (21.4 ± 11.9 vs 16.1 ± 9.4 years, p<0.001) and a lower median HbA1c value (7.4% (IQR 2.1) vs 8.2% (IQR 2.8), p=0.001). The OA group had a statistically higher percentage of hypertension (81.2% vs 69.8%), dyslipidaemia (73.2% vs 59.1%), nephropathy (30.8% vs 20.8%), cerebrovascular disease (31.5% vs 13.8%), and ischemic heart disease (23.6% vs 13.8%). The prevalence of retinopathy was similar in both groups (39.1% vs 45.3%, p=0.467). There were no significant differences in the percentage of patients on insulin (51.8% vs 56.6%, p=0.541), statin (55.1% vs 49.7%, p=0.145), or anti-aggregation (43.5% vs 36.5%, p=0.116) treatment (Table 2).
HbA1c: Glycated hemoglobin, IQR: Interquartile range, OA: Older adults, SD: Standard deviation, YA: Younger adults
*Pearson’s chi-square, a – independent samples t-test, b – Fisher’s exact test, c – Mann-Whitney U test
The YA group more often had a past history of diabetic foot ulcers (25.2% vs 18.1%, p=0.03) (Table 3). The number or type of previous amputation did not differ significantly between groups (80.0%/18.5%/1.5% vs 86.1%/12.6%/1.3%, p=0.301; 14.4%/2.5%/1.9%/0% vs 6.5%/2.2%/2.5%/1.4%, p=0.055). Neuropathic diabetic foot ulcers were more common in the YA group (56.6% vs 28.6%, p<0.001). A greater proportion of both forefoot and plantar location diabetic foot ulcers (86.2% vs 74.9%, p=0.007; and 24.5% vs 9.4%, p<0.001, respectively) occurred in the YA group. No differences were found in terms of diabetic foot ulcer evolution time, lateralization, or previous course of antibiotic therapy (Table 3).
DFU: Diabetic foot ulcer, IQR: Interquartile range, TF: Transfemoral, TM: Transmetatarsal, TTP: Transtibioperoneal, OA: Older adults, YA: Younger adults
*Pearson’s chi-square, b – Fisher’s exact test, c – Mann-Whitney U test
Table 4 summarizes diabetic foot ulcer classification by age group according to PEDIS infection, University of Texas, and Wagner classifications. There were no differences between groups in the percentage of patients in grade 1 (66.9% vs 70.7%) and grade ≥ 2 (33.1% vs 29.3%) in the PEDIS scale, nor in the stages and grades in the University of Texas classification. However, 68% of patients presented with a grade 1 ulcer as per the PEDIS scale and had a stage A and a grade 1 ulcer as per the University of Texas classification (60% and 79.1%, respectively) (Table 4).
OA: Older adults; PEDIS: Perfusion, extent, depth, infection, sensation; YA: Younger adults
*Pearson’s chi-square
In the univariate logistic regression analysis, we found two associations with older age: proximal diabetic foot ulcer location (OR 2.09 (1.23-3.53), p=0.006) (Table 5), and non-plantar diabetic foot ulcer surface (OR 3.13 (1.82-5.37), p<0.001) (Table 6). After adjusting for potential confounders in a multivariate analysis, older age lost the association both to more proximal (OR 1.72 (0.94-3.15), p=0.081), and non-plantar (OR 1.78 (0.83-3.77), p=0.133) diabetic foot ulcer location.
CI: Confidence interval, DFU: Diabetic foot ulcer, DM: Diabetes mellitus, HbA1c: Glycated hemoglobin, OR: Odds ratio
CI: Confidence interval, DFU: Diabetic foot ulcer, DM: Diabetes mellitus, HbA1c: Glycated hemoglobin, OR: Odds ratio
In this study, there was a higher prevalence of diabetic foot ulcers (63.4% vs 36.6%) in the elderly. We also found a lower proportion of males and a higher prevalence of comorbidities (namely dyslipidemia and hypertension) and type 2 DM in advanced age. In terms of ulcer-related factor results, there was a higher prevalence of neuro-ischemic diabetic foot ulcers and a smaller proportion of forefoot and plantar location diabetic foot ulcers in the older group. In the univariate logistic regression analysis, we found associations between older age and both proximal and non-plantar diabetic foot ulcer location even though these associations did not persist after adjusting for potential confounding factors.
The higher prevalence of neuro-ischemic diabetic foot ulcers in the older group is in line with the expected atherosclerosis continuous progress during aging [10,11]. In terms of location, proximal and non-plantar diabetic foot ulcers occurred more frequently in the older group, both with predictably lower healing rates according to the literature [7]. These aspects combined with their greater vulnerability, lower average life expectancy, and considerable age group heterogeneity reinforce the need to individualize the approach and treatment of diabetic foot ulcers in this age group [4].
The only study that we know of evaluating ulcer location and age group was published by Dörr et al. in 2021. However, patients in this study were hospitalized while our patients were seen in the outpatient setting and had less advanced disease [12]. When comparing our results with those of Dörr et al., they may, at first glance, seem contradictory as it was suggested that ulcers tend to move from the plantar and hindfoot to the forefoot and toes with increasing age [12]. Both results can be reconciled if we consider the substantial differences between the samples: one corresponded to hospitalized patients with diabetic foot ulcer infection and ours evaluated predominantly patients with uninfected diabetic foot ulcers observed in an outpatient setting. Thus, the key to explaining the disparity in outcomes appears to be the presence and severity of the infection. Although the most frequent diabetic foot ulcer location in the elderly is more proximal and non-plantar, infection is more frequently diagnosed in plantar and more distal ulcers. In our point of view, the most plausible explanations for this could be that the plantar and distal regions of the foot are more prone to trauma and therefore enable an easier “gateway” for infectious agents [13].
Furthermore, logistic regression analysis results suggest the presence of a potential confounding factor underlying the loss of association with more proximal diabetic foot ulcer location in the multivariate analysis. Thus, we admit that most of the confounding effects may have resulted from the patient’s lack of autonomy, a factor that maintained its association with the more proximal location of diabetic foot ulcers in the multivariate analysis and that may have increased the risk of developing ulcers, especially proximal pressure-linked ones, or from other factors not considered in the analysis (for example vascular supply). We cannot assure that a part of the ulcers evaluated could not correspond to pressure-linked ulcers in individuals with DM, whose pathophysiology and risk factors differ. This topic has been debated. Our results support an overlap between diabetic foot ulcers and some pressure-linked ulcers in the elderly. Moreover, we consider that older age might have lost its association with both more proximal and non-plantar diabetic foot ulcers in the multivariate analysis due to the limited sample size.
This study is the first, to our knowledge, to assess diabetic foot ulcer location according to age group in an outpatient and predominantly non-infected setting. Moreover, we provide a complete assessment of diabetic foot ulcer severity based on the three most used and widely accepted diabetic foot ulcer classification systems [9]. However, a few limitations should be noted. Firstly, its retrospective nature accounts for the existence of missing values in some of the studied variables. We also acknowledge that there are inter-observer differences in the use of diabetic foot ulcer classification systems, which, despite evidence of a moderate inter-observer agreement between scales [9], might have led to a classification bias. Finally, it is also worth mentioning that vascular studies underlying the classification of diabetic foot ulcers were not included.
In conclusion, elderly individuals are a very special population in several aspects, namely in diabetic foot ulcer presentation and location. Our results showed that this group is more prone to non-plantar and proximal diabetic foot ulcer location on univariate analysis, both with predictably lower healing rates according to literature, even though these associations did not persist in the multivariate analysis. We hope that these results may represent an advance for better prevention and management of diabetic foot ulcers in older individuals with diabetes.
Endocrinology, Centro Hospitalar Baixo Vouga, Aveiro, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Orthopedics, Centro Hospitalar Universitário do Porto, Porto, PRT
Vascular Surgery, Centro Hospitalar Universitário do Porto, Porto, PRT
Endocrinology, Centro Hospitalar Universitário do Porto, Porto, PRT
Human subjects: Consent was obtained or waived by all participants in this study. Ethics Committee of Centro Hospitalar Universitário do Porto issued approval 2021.160 (131-DEFI/134-CE). The study protocol was in conformance with the World Medical Association’s Helsinki Declaration and was approved by the Ethics Committee of Centro Hospitalar Universitário do Porto [approval number: 2021.160 (131-DEFI/134-CE)]. Informed consent was waived by the Ethics Committee based on the retrospective nature of the study and full data anonymization. . Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.
10.7759/cureus.28189
Rosinha P, Saraiva M, Ferreira L, et al. (August 19, 2022) A Retrospective Cohort Study on Diabetic Foot Disease: Ascertainment of Ulcer Locations by Age Group. Cureus 14(8): e28189. doi:10.7759/cureus.28189
Peer review began: August 01, 2022
Peer review concluded: August 15, 2022
Published: August 19, 2022
© Copyright 2022
Rosinha et al. This is an open access article distributed under the terms of the Creative Commons Attribution License CC-BY 4.0., which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
DFU: Diabetic foot ulcer, IDSA: Infectious Diseases Society of America, PEDIS: Perfusion, extent, depth, infection, sensation
HbA1c: Glycated hemoglobin, IQR: Interquartile range, OA: Older adults, SD: Standard deviation, YA: Younger adults
*Pearson's chi-square, a – independent samples t-test, b – Fisher's exact test, c – Mann-Whitney U test
DFU: Diabetic foot ulcer, IQR: Interquartile range, TF: Transfemoral, TM: Transmetatarsal, TTP: Transtibioperoneal, OA: Older adults, YA: Younger adults
*Pearson's chi-square, b – Fisher's exact test, c – Mann-Whitney U test
OA: Older adults; PEDIS: Perfusion, extent, depth, infection, sensation; YA: Younger adults
*Pearson's chi-square
CI: Confidence interval, DFU: Diabetic foot ulcer, DM: Diabetes mellitus, HbA1c: Glycated hemoglobin, OR: Odds ratio
CI: Confidence interval, DFU: Diabetic foot ulcer, DM: Diabetes mellitus, HbA1c: Glycated hemoglobin, OR: Odds ratio
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Diabeets
18/10/2022