Diabetic foot ulcers (DFUs), which are one of the widespread and serious complications in patients with diabetes, have been defined as ulcers on the feet associated with infection, destruction of the deep tissues, neurological abnormalities and peripheral vascular disease (PVD) in the lower limb.1 DFUs are a common reason for hospital admissions among patients with diabetes and are a major factor reducing their quality of life.2,3 DFUs increase patients' morbidity, mortality and healthcare expenditure.4,5 The lifetime incidence of foot ulcers in patients with diabetes is 34%.6 More than half of nontraumatic lower-extremity amputations have been related to DFU infections, and 85% of patients with diabetes and with amputations had DFUs.7,8 Patients with diabetes and with amputation because of DFUs have a mortality rate of >70% within five years.7 Statistical data in Taiwan from 2001–2015 showed that 20–30% of hospitalisation fees were caused by DFU and 18.6% of patients with DFUs underwent amputation.9
The key to the management of DFUs is prevention, with education and foot screening playing a vital role.10 Our previous studies showed that patients with a longer duration of diabetes, foot complications and foot lesions had a higher risk of developing DFUs than other patients with diabetes.11 Therefore, the prevention of DFUs requires the intervention of professional podiatrists.
Podiatrists are health professionals who can independently implement nursing management of the foot in strict accordance with the guidelines and requirements for sanitation and disinfection. They are also able to recognise the pathological changes and symptoms of DFUs and then follow doctors' advice regarding the prevention, treatment and rehabilitation of foot disorders.12 Although podiatrists in China have been recognised as qualified therapists for diabetic foot treatment, they have not been ratified by the Chinese government as medical personnel. Unlike other countries, where podiatrists are mainly physicians, podiatrists in China are mainly nurses whose main job involves tasks such as: early screening of diabetic foot; simple treatment for diabetic wounds; changing wound dressings for patients with diabetic foot; and health education on podiatry, excluding performing surgical operations.
The data for the current study were obtained from patients with diabetes (including outpatients and inpatients) who were treated in the Endocrinology department of Handan Central Hospital in Hebei Province, China, from 2016–2018. The purpose of this study was to investigate the role of podiatrists in the prevention and treatment of DFUs by comparing the changes in the incidence of foot ulcers after one year of podiatrist intervention. The results of this study could provide an objective basis for the prevention and early treatment of DFUs.
Methods
Inclusion and exclusion criteria
All participants met the following inclusion criteria:
- Diagnosed with type 2 diabetes according to the International Classification of Diseases (ICD-10)
- Upper arm blood pressure below 180/110mmHg
- Glycosylated haemoglobin ≤9.0%.
The diagnosis of DFUs followed the 2019 International Working Group on the Diabetic Foot (IWGDF) guidelines.13 Patients with diagnoses of malignant tumour were excluded from the study.
Ethical approval and patient consent
All selected participants signed an informed consent form before participating in the survey and agreed to cooperate with the study procedures. All of the treatments were optional, and this study was just a questionnaire survey. Approval for this study was granted by the Ethics Committee of Handan Central Hospital (No.HDCH2016S13).
Enrolment
From May 2016 to May 2018, 338 patients were enrolled in the study; 38 of them did not complete the survey. During the one-year follow-up period, we provided medical treatment. We informed patients of the potential benefits and risks, and asked for the patients' written consent before conducting the treatment.
Study design
Basic information was collected from all patients at the start of the study, and this information was recorded on a questionnaire designed by the study team. All participants were followed for one year, and the updated patient information after the intervention of the podiatrist was recorded by filling out the questionnaire again. This new information was compared to the baseline information from the previous year.
The questionnaire for this study was designed by diabetic foot experts and statistical experts; it was administered by a professionally trained podiatrist. The questionnaire included: demographic characteristics; health status; risk factors for foot ulcers; lifestyle; medical pedicures; DFU risk grading2 before the intervention; the number of DFU occurrences during the intervention; and the number of intervention visits by the podiatrists. Patients who needed to undergo intervention by the podiatrist were notified by telephone. All participants were followed for one year, and the number of intervention visits and DFUs were recorded. All participants were asked to verbally complete the questionnaire. All contents of the survey were then completed by one professionally trained podiatrist and reviewed by another to ensure that the information was accurate.
Intervention of the podiatrists
The intervention methods and frequency were mainly based on the requirements of the Diabetes Foot Treatment and Prevention Guide published by the IWGDF.2 The patients were reminded by telephone to come to the hospital for an evaluation at least once every three months. The contents of each podiatrist intervention included:
- Diabetes health education
- Checking the arterial blood supply and peripheral neuropathy of the lower limbs and asking a specialist for treatment if there were lesions
- Performing examinations of patients with diabetes and with neurovascular disease and foot lesions
- Assessing the DFU risk level, removing risk factors such as tinea pedis, and treating patients with ulcers.
Data analysis
The data collected by each survey form were entered into a database built by Epi Data (The Epi Data Association, Denmark). The database was analysed and statistically processed with SPSS 24.0 (IBM Corp., US). To avoid data entry errors, all data were entered by two independent researchers and compared one by one. The Chi-squared test was used to assess the relationship between each DFU impact factor and the incidence of DFUs. Only if p<0.05 were the data considered significantly different.
Results
Characteristics of participants
The ratio of men to women among the 300 participants was 55:45. Their ages were mainly concentrated in the 50–59-year-old and 60–69-year-old age groups, accounting for 58% of the total. We observed that most of the patients had a long duration of diabetes; more than two-thirds of them had been diagnosed with diabetes for at least 10 years. Patients with a duration of diabetes between 10–19 years accounted for 54.3% of the total. The bulk (91.3%) of the patients' medical expenses were covered by medical insurance and the New Cooperative Medical System.
Most of the patients had a low level of education, and 73.7% only had a junior high school or primary school education or less. Most (64.3%) of the patients lived with their spouses. The main income for the family was provided by the patients, either themselves or in combination with their spouses, in 78.7% of cases. Our survey showed that 40.3% of the patients could afford their medical expenses, 50.7% of the patients could barely afford their medical expenses, and the remainder could either hardly bear the cost or found the cost unbearable. Before the intervention, 20.7% of the 300 observed patients were diagnosed with DFUs. Other foot lesions were also noted, such as foot calluses (43.7%), feet with cracked skin (10.7%), and ingrown toenails (15.3%).
Relationship between blood glucose control and incidence of DFUs
Before the podiatrist intervention, the prevalence of DFUs was related to the control of blood glucose. The results of self-testing blood glucose at the patient's own home was the main criterion (blood glucose <11.1mmol/l two hours after a meal was defined as good glycaemic control, and ≥11.1mmol/l was considered poor glycaemic control). Before the podiatrist intervention, 78.7% of the patients had poor glycaemic control. DFUs occurred in only 14.1% of patients who had good blood glucose control. In contrast, 23.3% of patients with poor glycaemic control developed DFUs (Table 1). At the same time, during the investigation of foot complications, 76.3% of patients had lower extremity neuropathy before the intervention, and 65.7% had lower extremity vascular disease.
Table 1. Basic characteristics of the patients with DFUs prior to the intervention
| Factor | Blood glucose control | x2 | p | |
|---|---|---|---|---|
| Good (21.3%) | Poor (78.7%) | |||
| Number of DFUs in a year, n (%) | ||||
| 0 | 55 (85.9) | 181 (76.7) | ||
| 1 | 5 (7.8) | 42 (17.8) | 3.799 | 0.150 |
| 2 | 4 (6.3) | 13 (5.5) | ||
| Complication, n (%) | Yes | No | Total | |
| Amputation caused by DFU | 7 (2.3) | 293 (97.7) | 300 (100) | |
| Lower extremity neuropathy | 229 (76.3) | 71 (23.7) | 300 (100) | |
| Lower extremity vascular disease | 197 (65.7) | 103 (34.3) | 300 (100) | |
Good (Good glycaemic control): blood glucose below 11.1 mmol/l two hours after a meal. Poor (Poor glycaemic control): blood glucose ≥11.1 mmol/l two hours after a meal. DFU—diabetic foot ulcer
Effect of the intervention
We noticed that, among all patients, there was a negative correlation between the frequency of podiatrist intervention visits and the number of DFU occurrences (Spearman correlation coefficient: –0.496; p<0.001), meaning that the more interventions by the podiatrist, the more difficult it was for DFUs to occur. The prevalence of DFUs was significantly lower in the patients who received the intervention than in the patients who did not. Half (57/114) of the patients who did not receive interventions by the podiatrist had DFUs at least once in the past year, while only 3.8% (7/186) of the patients who underwent interventions by the podiatrist had a DFU; none of the patients who received two interventions in the past year had more than one DFU (Table 2).
Table 2. Comparison of the number of intervention visits with the podiatrist and the number of foot ulcers in a year
| Factor, n (%) | Podiatrist intervention visits | Total | ||
|---|---|---|---|---|
| Number of DFUs | 0 | 1 | ≥2 | |
| 0 | 57 (50.0) | 111 (95.9) | 68 (97.1) | 236 (78.7) |
| 1 | 42 (36.8) | 3 (2.6) | 2 (2.9) | 47 (15.7) |
| 2 | 15 (13.2) | 2 (1.7) | 0 (0.0) | 17 (5.7) |
| Total | 114 (38) | 116 (38.7) | 70 (23.3) | 300 (100) |
Spearman correlation coefficient: -0.496, p<0.001.
DFU—diabetic foot ulcer
The incidence of ulcers and amputation was reduced after the podiatrist intervention
According to their risk of DFUs, we classified patients into the following grades:
- Normal patients (patients without peripheral neuropathy, peripheral arterial disease (PAD), foot deformity or a history of foot disease)
- Patients with peripheral neuropathy or a loss of protective sensation
- Patients with neuropathy, malformation or PAD
- Patients with a history of ulcers and amputation.
Comparing the incidence of DFUs among patients of different grades, it was found that there was no change in the first three grades during the year. Therefore, we focused on the 68 patients with a history of DFU or amputation. Their incidence of ulcers was 89.7% and 27.9%, respectively, at one year (p<0.000) (Fig 1). The incidence of ulcers and amputation was significantly reduced after the intervention. Among 61 patients with ulcers one year previously, 45 patients had healed one year later, and the ulcer rate was only 26.2%. There were three patients who developed ulcers among the seven who did not have ulcers a year ago, and thus the new ulcer rate was 42.9% (Fig 2). All details are shown in Table 3.
Table 3. Cross-tabulation of patients with a previous DFU or an amputation history with or without DFUs
| DFU occurred a year later | ||||
|---|---|---|---|---|
| Yes, n (% of Hc) | No, n (% of Hc) | Total, n (% of Hc) | ||
| DFU occurred a year ago | Yes % of Vc | 16 (26.2) | 45 (73.8) | 61 (100.0) |
| 84.2 | 91.8 | 89.7 | ||
| No % of Vc | 3 (42.9) | 4 (57.1) | 7 (100.0) | |
| 15.8% | 8.2% | 10.3% | ||
| Total % of Vc | 19 (27.9) | 49 (72.1) | 68 (100.0) | |
| 100 | 100 | 100 | ||
Pairing X2 test: McNemar test, exact probability p<0.001. Before the intervention, patients with DFUs had a thorough examination; Fisher's exact test for the ulcer rate after one year of intervention in patients without DFUs a year ago: p=0.390.
DFU—diabetic foot ulcer; Hc—horizontal comparison; Vc—vertical comparison
Effect of frequency of podiatrist intervention
Among the 68 patients with a history of previous ulcer or amputation, 11 patients received one or more podiatrist intervention and 57 patients never received an intervention. All 57 patients without intervention by podiatrists developed foot ulcers within one year. Among them, 73.7% of patients had one ulcer, and 26.3% had two ulcers. In contrast, among the 11 patients who had been treated, four patients did not have ulcers, accounting for 36.4%, and the percentages of patients having one and two ulcers were 45.5% and 18.2%, respectively (Fig 3). The difference was statistically significant (Fisher's exact test: p=0.001) (Table 4). These results demonstrated that the intervention by the podiatrist could reduce the frequency of ulcers in patients with a previous history of ulcers or amputation and was a protective factor against DFUs.
Table 4. Relationship between the intervention and the frequency of DFU occurrences in a year among the patients with DFU or amputation one year ago
| Intervention | DFU occurrences in a year, n (%) | Total, n (%) | ||
|---|---|---|---|---|
| 0 | 1 | 2 | ||
| No | 0 (0.0) | 42 (73.7) | 15 (26.3) | 57 (83.8) |
| Yes | 4 (36.4) | 5 (45.5) | 2 (18.2) | 11 (16.2) |
| Total | 4 (5.9) | 47 (69.1) | 17 (25.0) | 68 (100) |
Fisher's exact test: p=0.001;
DFU—diabetic foot ulcer
The relationship between standardised foot care and DFUs
After one year of intervention, we investigated the patients' own approach to foot nursing during the study period (see Table 5). Applying emollient oil when the feet were dry (before intervention χ2=2.859; p=0.091 versus after intervention χ2=3.463; p=0.063), checking the skin of the feet daily (before intervention χ2=1.285; p=0.257 versus after intervention χ2=0.408; p=0.523) and trimming the toenails short (before intervention χ2=0.235; p=0.628 versus after intervention χ2=2.742; p=0.098). Because their p-values were >0.05, these factors could not be considered to be significantly related to the occurrence of DFUs. There was no positive result, probably because the number of participants was too small and the number of interventions by the podiatrist in this study was insufficient.
Table 5. The change in patient foot care after one year
| Factor | One year ago | One year later | ||||||
|---|---|---|---|---|---|---|---|---|
| DFU (%) | X2 | p-value | DFU (%) | X2 | p-value | |||
| Yes (20.7) | No (79.3) | Yes (6.7) | No (93.3) | |||||
| Check the skin of the feet every day, n (%) | ||||||||
| Yes | 22 (17.6) | 103 (82.4) | 1.285 | 0.257 | 7 (5.6) | 118 (94.4) | 0.408 | 0.523 |
| No | 40 (23.0) | 134 (77.0) | 13 (7.5) | 161 (92.5) | ||||
| Apply emollient oil when the feet are dry, n (%) | ||||||||
| Yes | 22 (16.3) | 113 (83.7) | 2.859 | 0.091 | 5 (3.7) | 130 (96.3) | 3.463 | 0.063 |
| No | 40 (24.2) | 126 (75.8) | 15 (9.1) | 150 (90.9) | ||||
| Trimming the toenails short, n (%) | ||||||||
| Yes | 37 (19.8) | 150 (80.2) | 0.235 | 0.628 | 9 (4.8) | 178 (95.2) | 2.742 | 0.098 |
| No | 25 (22.1) | 88 (77.9) | 11 (9.7) | 102 (90.3) | ||||
DFU—diabetic foot ulcer
Discussion
The effects of foot lesions, hyperglycaemia and diabetic complications on DFUs
Many factors contribute to the development of DFUs. Foot lesions such as foot deformities, calluses, corns, blisters and skin ruptures often occur in patients with diabetes and are very serious risk factors for DFUs. Peripheral neuropathy and PVD are the underlying causes of DFUs and, in turn, contribute to the development of supernumerary risk factors such as changes in muscle tension, limited joint activity and deformities of the foot.14,15 Increased plantar pressure caused by neuropathy is also a major risk factor for DFUs.14 It can lead to limited joint mobility or even deformity of the foot joints and place abnormal pressure on various locations on the foot.15 Over time, the pressure points will form a callus, which will further aggravate the local pressure to form a vicious circle and eventually form a pressure ulcer.16 Motor neuropathy in patients with diabetes results in an imbalance in muscle strength.15 Due to the loss of the distal innervation of the foot and the unbalanced pull from the proximal muscles, the muscles on the back of the foot contract to form a permanently ‘cocked’ toe, referred to as claw toe.17,18 In addition, diabetic autonomic nerve lesions will cause dry skin on the feet,14 which will cause foot lesions such as tinea pedis and corns and increase the risk of DFUs.
The persistence of hyperglycaemia causes a series of biochemical reactions, such as the generation of reactive oxygen species, particularly superoxide and peroxynitrite, leading to vascular endothelial damage, vascular dysfunction and atherogenesis.15 Long-lasting hyperglycaemia may also result in thinner and more fragile skin tissue, making the skin more susceptible to damage from physical or chemical exposure.19,20,21 Micro- and macrovascular lesions in the skin of patients with diabetes will delay the healing of foot ulcers by causing ischaemia of the corresponding skin and connective tissue fibrosis in the patient's foot.22,23,24 It has been reported that 90% of amputations in patients with diabetes are caused by ischaemia.25,26
In our study, among 300 patients in the survey, 43.7% had foot calluses, 78.7% had poor glycaemic control, 76.3% had lower extremity neuropathy and 65.7% had lower extremity vascular disease. Therefore, an intervention was necessary to reduce the risk of complications. Compared with previous studies, the reason for the higher proportion of lower extremity vascular lesions in our study (57.9%27 versus 65.7%) may be the small number of participants involved in the study and the general admission of patients with severe disease. These survey data indicate the direction for our future work. We advocate that patients with high-risk factors should regularly perform related examinations and treatments, such as removing foot lesions, including calluses, corns and tinea pedis, and trying to control their blood sugar at normal levels. This will help prevent the development of new DFUs and slow the progression of existing DFUs.
The need for intervention by a podiatrist to prevent DFUs
DFUs are a chronic, costly, multidisciplinary disease that places a heavy burden on patients and their families. A podiatrist can greatly reduce the occurrence of DFUs by increasing the health education of patients, the screening of patients with high-risk diabetes, the evaluation of the patient's foot, and interventions for any foot lesions. The podiatrist plays an important role in the multidisciplinary team (MDT) managing DFUs. Many studies have shown that there are several obstacles in the management of diabetic foot infections, including identifying an ‘at-risk’ foot, treating an acutely diseased foot, preventing further problems, lacking awareness of diabetes and its complications, and lacking proper foot services. To address these obstacles a team of health professionals who are specifically focused on diabetic foot complications is essential.28 At the same time, many experts believe that podiatrists should be the gatekeepers for the management and prevention of diabetes-related foot complications.29
In this study, firstly, we found that the difference in data was statistically significant through Fisher's exact test in Table 4. Then we conducted a correlation analysis and found that the Spearman correlation coefficient was –0.496, which proved that there was a negative correlation between intervention and ulcer occurrence. The intervention of the podiatrist was a protective factor against DFUs. Patients at Wagner grade 0 (patients without current ulcers but at risk of suffering from foot ulcers) are the focus of foot disease prevention.30 According to the risk factors for foot disease in the Diabetes Foot Treatment and Prevention Guide published by the IWGDF, Wagner level 0 patients can be divided into low-risk feet and high-risk feet and further subdivided into four levels,31 which was the classification of foot risk factor grade considered in this study. This study found that the podiatrist intervention for patients with a history of DFUs or amputation was particularly effective and could significantly reduce the incidence of new DFUs.
These findings are consistent with several other studies. Gibson et al.29 showed that patients who received pre-ulcer care by a podiatrist before DFU development were less likely to have adverse events such as amputation and hospitalisation. Lavery et al.32 found that in a US-managed care programme, when a team including podiatrists implemented a foot risk-based disease management programme for diabetes foot care, after two years there was a 38% reduction in hospital admissions, a 47% reduction in amputations and a 70% reduction in skilled nursing facility admissions. The multidisciplinary foot team, which consisted of chiropodists and diabetes doctors, intervened according to the consensus guidelines for foot care and found that the amputation rate of patients with DFUs was reduced by 60%.33 Numerous studies have also shown that the work of podiatrists can contribute significantly to reducing the incidence of DFUs, the hospitalisation rate and the amputation rate in patients with diabetes, which is consistent with our findings. All of these studies, including the present study, demonstrated that the intervention of the podiatrist was important and necessary for patients with diabetes.
However, there are also different views on the role of podiatrists in preventing the deterioration of DFUs. According to Buckley et al.,34 the influence of podiatrists on preventing patients with diabetes from having their lower extremity amputated was not obvious. This is due to the fact that apart from the influence of podiatrists, many other potential confounders can affect the amputation rate among patients with diabetes, of which MDT management of DFU care is the main influencing factor. Building on this point of view, we argue that podiatrists can play an active role in the prevention of DFUs in collaboration with an MDT. This can be verified by the rather satisfying outcome of better foot care provided by podiatrists under the guidance of the IWGDF.2
Current status of podiatrists in China and other countries
In many developed countries, podiatrists have formed an independent profession, and there is a college that specialises in training podiatrists. They need to be professionally trained and pass an examination for their qualification as a podiatrist. After passing the examination, they are issued a certificate to serve patients. In Germany, a podiatrist must have at least 2000 hours of theoretical study and 1000 hours of professional study to practice (approximately 2.5 years).35 In the UK, only licensed doctors are allowed to provide foot care services such as medical pedicures.11 The requirements for podiatrists worldwide are extremely strict.
In some high-income countries, the prevalence of DFUs has decreased significantly in the last three decades, and this achievement is related to the extensive use of multidisciplinary foot treatment, increased foot screening and podiatrist care.36,37 Asia, Japan, Hong Kong and Taiwan have diabetes specialists, but other countries do not have such medical specialties.38 In China, attention to diabetic foot disease began later than in many countries. It was not until 2003 that diabetic foot disease centres were established in Shanghai, Guangzhou and Beijing. Although China started late with specialist treatment for diabetic foot care, it has made significant progress in the past decade;39 clinical prevention and research into diabetes have made significant progress, but compared with developed countries, there is still a large gap.40
Most patients in China have not yet realised the importance of podiatrists. DFU treatment requires a team of professionals rather than relying solely on podiatrists.41 However, podiatrists are indispensable to the treatment of DFUs. One study showed that a systematic difference existed between patients with DFU with and without foot podiatric care; that is, patients with diabetes who are treated by podiatrists are often older or more severely ill.29 Therefore, the necessary future work of our podiatrists is not only to improve their working ability but also to strengthen patients' recognition of the work of the podiatrist to reduce the incidence of DFUs.
The results of this research were consistent with those of other studies, which supports the reliability of our experimental results. It also provides a basis for relevant clinical work in the future while increasing patients' attention to DFUs and deepening patient trust in the podiatrist.
Limitations
In this study, we surveyed a total of 338 patients, which is not a particularly large sample. Among them, only 300 patients finished the whole study; 38 patients withdrew, a rather high rate of loss to follow-up. Only basic patient information was collected before the intervention, and this was not re-examined after one year of intervention, which is a limitation of this experiment. According to international standards, patients with (IWGDF)2 grade (1), grade (2), grade (3) and grade (4) foot ulcer risk levels need to be examined once a year, once every six months, once every three months and once every month, respectively. In our study, following these guidelines, patients who needed to undergo intervention by a podiatrist received health education and telephone reminders. However, for various reasons, such as lack of patient adherence and economic conditions, there was no regular pattern to the podiatrist intervention visits. Our future research will improve on these limitations, one by one, and eliminate the shortcomings of this experiment.
Conclusion
The results of this study help to understand the situation of patients with diabetes in China and to prove that standardised podiatrist intervention has an important role in inhibiting the occurrence and development of DFUs. This study confirms the significant role of podiatrists in preventing DFUs in China, particularly among patients with a history of DFUs or amputation. While the current diabetic foot prevention model in China needs further development and standardisation, the observed decrease in DFU incidence with regular podiatrist intervention underscores the importance of integrating podiatrists into diabetes care to improve patient outcomes.
Reflective questions
- How can podiatrists personalise interventions to increase efficiency in preventing the development of diabetic foot ulcers (DFUs)?
- How can podiatrists use the Internet and cell phones to improve their effectiveness in preventing and treating DFUs.
- Peripheral neuropathy is the most important risk factor for foot ulcers in patients with diabetes, but how can it be prevented?