Abstract
Development of the triad of peripheral arterial disease, peripheral neuropathy, and end stage renal disease puts people with diabetes at an increased risk of diabetic foot ulcerations and subsequent infections that often precede lower extremity amputations. In patients on hemodialysis, there is a ten-fold increased risk of amputation and an estimated 40%–82% one-year mortality rate if the amputation is a major amputation. This study aimed to examine if patients presenting to a podiatric clinic with stage 3a or 3b chronic kidney disease and a diabetic foot ulcer had decreased rates of amputations as compared to patients who presented after initiating dialysis. Our results demonstrated all major amputations occurred in patients who did not establish with podiatry prior to initiating HD. Additionally, our study revealed a potential access to care disparity for African American patients with chronic kidney disease, as African American patients were established with podiatry prior to initiating dialysis less often in comparison to Caucasian individuals. Our study lays the groundwork for future work investigating the impact of podiatric surveillance on patients with diabetes and end stage renal disease.
Keywords: diabetic foot complications, chronic kidney disease, end stage renal disease, chronic ulcer, dialysis
Introduction
Nearly half of end stage renal disease (ESRD) cases are attributed to diabetes mellitus (DM) and up to 40% of patients with DM will develop diabetic nephropathy.1 As persons with DM develop diabetic nephropathy, they may also develop other complications including diabetic polyneuropathy and peripheral arterial disease (PAD). PAD has a prevalence of approximately 25%2 while the prevalence of neuropathy is estimated to be around 28% in persons with DM.3 When patients develop this triad, there is an increased risk for diabetic foot ulceration (DFU) and subsequent non-healing. Exposure to a DFU nearly always precede amputations to treat both limb- and life-threatening conditions.4
There is a strong association between developing a DFU leading to an amputation and patients with ESRD and hemodialysis (HD).5 On average, a patient on HD will undergo a lower extremity amputation within seven months of starting HD.6 In patients with DM on HD, nontraumatic lower extremity amputations range from 11.8 to 13.8 per 100 persons per year and at rates tenfold higher than in the overall DM population.7 More striking is that one year mortality rates for major amputations, such as below the knee amputation (BKA) or above the knee amputation (AKA), is estimated to be between 13%–40% but can rise to as high as 40%–82% when patients have additional comorbidities such as renal disease, DM, and peripheral vascular disease.8–10
There is a critical need to prevent lower extremity ulcerations and major amputations in patients with DM and ESRD. As podiatric care and surveillance has been associated with reduction of DFU events in persons with a history of previous DFU,11 we hypothesize that for patients who are established with a podiatrist for routine pedal exams, prior to initiation of HD, will undergo fewer amputations. In addition, we will assess the rates of amputations for individuals on HD versus those individuals who have CKD but do not receive HD.
Methods
A retrospective study of adult patients (≥ 18 years old) presenting to a tertiary academic hospital podiatry or an affiliated wound care clinic between January 2016 through March 2020 using a cohort discovery tool (DataDirect) was performed. DataDirect is a self-serve tool enabling access to clinical data such as diagnoses, encounters, procedures, medications (ordered and administered), and labs (ordered and results). DataDirect provides aggregate counts for cohort discovery and the ability to download patient health data.12 Patients were eligible for this study if they presented to these clinics as a new patient with a wound and diagnosis of DM, had at least two years of follow up from this initial visit, were being followed by a podiatrist, had a diagnosis of at least stage 3a CKD according to Kidney Disease: Improving Global Outcomes (KDIGO) Diabetes Work Group, or if they demonstrated an estimated glomerular filtration rate (eGFR) of <60 mm/hr for three consecutive months. Patients were excluded from this study if they did not have DM, if they had CKD stage 1 or 2, if lab values did not support the diagnosis of CKD 3a or worse as defined by the KDIGO, received a majority of their care visits by a non-podiatrist, and did not present with a DFU at initial visit. This study was deemed exempt via internal institutional review board (IRB no.: HUM00243485).
Cohort Designation
Patients were separated into two cohorts based on the KDIGO guidelines.13 If a patient was either on HD or had initiated HD during their two years of follow-up they were assigned to the HD cohort. If a patient had CKD but was never on dialysis, they were designated to the CKD Cohort.
Participant Data Abstraction From Electronic Medical Record
Patients were followed for two years after initial presentation for corresponding lab values, such as eGFR, HbA1c, microalbumin, creatinine, and serum bicarbonate. The presence of a continuous glucose monitoring device was recorded for both patient cohorts. In both patient cohorts, level of amputation (if any), previous amputation history (if any), and demographic factors such as age (years old at initial visit), sex, race, body mass index (kg/m2), and additional comorbidities including the presence of PAD, CAD, COPD, CHF, anxiety and depression were extracted from diagnoses that were readily available in patient’s chart were collected (Table 1). In patients who were categorized into the HD cohort, a subanalysis was performed for patients who had established with podiatry prior to initiation of HD. Levels of amputation, including major versus minor amputation were abstracted from medical record. A minor amputation was defined as any amputation that occurred at the talonavicular joint (ie, Chopart) or distally, and a major amputation was defined as any amputation that was proximal to the talonavicular joint.
Table 1.
Patient Demographics for Patients with CKD not on Dialysis Versus Patients with ESRD on Dialysis. Data are Reported as the Mean (SD) or %.
| CKD N = 49 N (%) |
HD N = 33 N (%) |
P-value | |
|---|---|---|---|
|
| |||
| Age (years of age), mean ± SD | 61.4 ± 12.3 | 53.1 ± 10.4 | .002* |
| BMI (kg/m2) mean ± SD | 35.4 ± 8.2 | 31.9 ± 6.2 | .02* |
| Gender, n (%) | |||
| Male | 32 (65.3) | 21 (63.6) | .88 |
| Female | 17 (34.7) | 12 (36.3) | |
| Race, n (%) | |||
| Caucasian | 37 (75.5) | 20 (60.6) | |
| African American | 10 (20.4) | 13 (39.4) | .10 |
| Hispanic | 2 (4.1) | 0 (0.0) | |
| Diabetes Mellitus, n (%) | |||
| Type 1 | 7 (14.3) | 13 (39.4) | .009* |
| Type 2 | 42 (85.7) | 20 (60.6) | |
| CGM Usage, n (%) | |||
| Never | 29 (59.2) | 22 (66.7) | .49 |
| Prior or during study | 20 (40.8) | 11 (33.3) | |
| PAD, n (%) | |||
| Yes | 15 (30.6) | 18 (54.5) | .03* |
| CAD, n (%) | |||
| Yes | 24 (49.0) | 9 (27.3) | .05* |
| COPD, n (%) | |||
| Yes | 7 (14.3) | 3 (9.1) | .48 |
| CHF, n (%) | |||
| Yes | 15 (30.6) | 11 (33.3) | .8 |
| Anxiety, n (%) | |||
| Yes | 13 (26.5) | 6 (18.2) | .38 |
| Depression, n (%) | |||
| Yes | 16 (32.7) | 11 (33.3) | .94 |
| Previous Amputation, n (%) | |||
| Yes | 13 (26.5) | 11 (33.3) | .5 |
| Re-ulceration During Study, n (%) | |||
| Yes | 46 (93.9) | 30 (90.9) | .61 |
| Amputation During Study n (%) | |||
| Minor | 17 (34.7) | 14 (42.4) | .4 |
| Major | 4 (8.2) | 5 (15.2) | |
Data Analysis
Analyses were performed between patients in the CKD cohort and the HD cohort. Additional analyses were performed in the HD cohort between patients who had established with podiatry either prior or after initiating HD. The cohorts were compared with Fischer’s exact test for categorical data (frequency and counts) and two sample t tests for continuous (average ± mean). A type I error rate of 0.05 was used to determine statistical significance. Analysis was completed using Microsoft Excel and MedCalc Software Ltd (Ostend Belgium). Missing data for variables such as lab values and demographic information were excluded from analyses as applicable, and the corresponding variable was analyzed with a reduced sample size.
Results
288 charts were retrospectively reviewed with 82 patients meeting eligibility criteria. 59.8% (49) of patients did not progress to dialysis during the course of this study (CKD cohort) with 40.2% (33) of patients progressing to HD (HD cohort). Of these, 33 patients who progressed to HD, 20 were not established with podiatry prior to initiating dialysis and 13 were established with podiatry. 24.4% (20) of the patients had type 1 DM, and 75.6% (62) had type 2 DM. Overall, 37.8%(31) of patients underwent a minor amputation and 11.0% (9) underwent major amputation.
Patients in the CKD cohort were on average older in years of age in comparison to patients in the HD cohort (61.4 ± 12.3 v. 53.1 ± 10.4, P = .002). The CKD cohort had an increased BMI in comparison to the HD cohort (35.4 kg/m2 vs 31.9 kg/m2, P = .02). There was no statistical difference seen in terms of race or sex in regards to the progression to HD. Patients with type 1 DM with a DFU progressed to HD more often (14.3% vs 39.4%, P = .009) during the study. These patients who progressed to HD were diagnosed with PAD (30.6% vs 54.5% P = .03) more frequently than patients in the CKD cohort. Patients in the HD cohort did not have higher rates of previous amputation history (P = .5), re-ulceration (P = .61), or higher occurences of amputation (both major and minor; P = .4) (Table 1). There were no differences between these two cohorts in counts or frequency of minor amputations (Table 2).
Table 2.
Patient Demographics of Patients Undergoing a Minor Amputation by CKD w/o Dialysis or ESRD w/Dialysis During this Study Period. Data are Reported as the Mean (SD) or %.
| CKD N = 17 N (%) |
HD N = 14 N (%) |
P-value | |
|---|---|---|---|
|
| |||
| Age (years of age) ± SD | 58.8 ± 12.4 | 51.9 ± 11.1 | .05* |
| BMI (kg/m2) mean ± SD | 33.2 ± 6.3 | 30.8 ± 5.8 | .06 |
| Gender | |||
| Male | 12 (70.6) | 11 (78.6) | .6 |
| Female | 5 (29.4) | 3 (21.4) | |
| Race | |||
| Caucasian | 13 (76.5) | 10 (71.4) | .8 |
| African American | 4 (23.5) | 4 (28.6) | |
| Hispanic | 0 (0.0) | 0 (0.0) | .6 |
| Previous Amputation History, n (%) | |||
| Yes | 7 (41.2) | 7 (50) | |
| Amputation Level, n (%) | |||
| Digit | 9 (52.9) | 5 (35.7) | .5 |
| Partial Ray | 4 (23.5) | 6 (42.9) | |
| Transmetatarsal | 4 (23.5) | 3 (31.4) | |
| Diabetes mellitus n (%) | |||
| Type 1 | 4 (23.5) | 7 (50) | .1 |
| Type 2 | 13 (76.5) | 7 (50) | |
| CGM Monitoring | |||
| Never | 7 (41.2) | 8 (57.1) | .4 |
| Prior or during study | 10 (58.8) | 6 (42.9) | |
| PAD, n (%) | |||
| Yes | 5 (29.4) | 6 (42.9) | .4 |
| COPD, n (%) | |||
| Yes | 2 (11.8) | 1 (7.1) | .7 |
| CHF, n (%) | |||
| Yes | 7 (41.2) | 3 (21.4) | .3 |
All patients in the HD cohort who underwent major amputation were African American while the patients undergoing major amputation in the CKD only 50% were African American (P = .09). 80% were female in the HD group but not different among groups (P = .37). In addition, all patients (n = 5) in the HD cohort who underwent a major amputation had a concomitant diagnosis of PAD (P = .2) (Table 3).
Table 3.
Patient Demographics of Patients Undergoing a Major Amputation by CKD w/o Dialysis or ESRD w/Dialysis During this Study Period. Data are Reported as the Mean (SD) or %.
| CKD N = 4 N (%) |
HD N=5 N (%) |
P-value | |
|---|---|---|---|
|
| |||
| Age (years of age) ± SD | 54.5 ± 6.2 | 51.2 ± 11.3 | .3 |
| BMI (kg/m2) mean ± SD | 42.1 ± 6.0 | 30.7 ± 6.7 | .05* |
| Gender | |||
| Male | 2 (50.0) | 1 (20.0) | .4 |
| Female | 2 (50.0) | 4 (80.0) | |
| Race | |||
| Caucasian | 2 (50.0) | 0 (0.0) | .09 |
| African American | 2 (50.0) | 5 (100) | |
| Previous Amputation History, n(%) | |||
| Yes | 1 (25.0) | 1 (20.0) | .9 |
| Diabetes mellitus n (%) | |||
| Type 1 | 0 (0.0) | 2 (40.0) | .2 |
| Type 2 | 4 (100) | 3 (60.0) | |
| CGM Monitoring | |||
| Never | 3 (75.0) | 4 (80.0) | .9 |
| Prior or during study | 1 (25.0) | 1 (20.0) | |
| PAD, n (%) | |||
| Yes | 3 (75.0) | 5 (100) | .2 |
| COPD, n (%) | |||
| Yes | 0 (0.0) | 1 (20.0) | .4 |
| CHF, n (%) | |||
| Yes | 1 (25.0) | 2 (40.0) | .7 |
Of the 33 patients in this study on HD, 39.4% had presented to podiatry prior to initiating HD, and 60.6% presented after initiating HD. Patients establishing with podiatry prior to dialysis were, on average older in years of age (57.1 years of age vs 50.5 years of age P = .04), but there was no difference in terms of gender. There was an apparent race disparity in terms of access to podiatric care. Of the 13 African American patients on HD, 15.4% of patients were established with podiatry prior to dialysis as opposed to 84.6% of patients who did not establish with podiatry prior to initiating HD (P = .03).
In the sub-cohort of patients who presented to podiatry after initiating HD, 60% underwent an amputation with 25% of this sub-cohort undergoing a major amputation, and 35% of this sub-cohort undergoing a minor amputation. In the sub-cohort of HD patients who had established with podiatry prior to initiating dialysis, 53.8% underwent an amputation; however, all of these amputations were minor amputations. In comparing patients undergoing minor amputations in this sub cohort, there was no difference between establishing with podiatry prior to initiating HD and minor amputations (P = .5). When comparing patients undergoing major amputations, major amputations only occurred in patients who did not establish with podiatry prior to HD (P = .1) (Table 4).
Table 4.
Patient Demographics of Patients with End Stage Renal Disease on Dialysis Subdivided by Establishment with Podiatry Prior to Beginning Dialysis or After Beginning Dialysis.
| Podiatry Before Dialysis N = 13 N (%) |
Podiatry After Dialysis N = 20 N(%) |
P-value | |
|---|---|---|---|
|
| |||
| Age (years of age) ± SD | 57.1 ± 9.4 | 50.6 ± 10.1 | .04* |
| BMI (kg/m2) mean ± SD | 32.2 ± 4.9 | 31.8 ± 6.9 | .4 |
| Gender | |||
| Male | 9 (69.2) | 12 (60.0) | .7 |
| Female | 4 (30.8) | 8 (40.0) | |
| Race | |||
| Caucasian | 11 (84.6) | 9 (45.0) | .03* |
| African American | 2 (15.4) | 11 (55.0) | |
| Diabetes mellitus n(%) | |||
| Type 1 | 5 (38.5) | 8 (40.0) | 1.0 |
| Type 2 | 8 (61.5) | 12 (60.0) | |
| CGM Monitoring | |||
| Never | 7 (53.8) | 15 (75.0) | .3 |
| Prior or during study | 6 (46.2) | 5 (25.0) | |
| Amputation | |||
| Minor | 7 (53.8) | 7 (35.0) | .5 |
| Major | 0 (0) | 5 (25.0) | .1 |
| PAD, n (%) | |||
| Yes | 5 (38.5) | 13 (65.0) | .2 |
| COPD, n (%) | |||
| Yes | 2 (15.4) | 1 (5.0) | .5 |
| CHF, n (%) | |||
| Yes | 4 (30.8) | 7 (35.0) | 1.0 |
Discussion
This study revealed a that all major amputations occurred in patients who did not establish with podiatry prior to initiating HD. Prominently, we discovered there was a lack of access to podiatric medicine for African Americans, with approximately 85% of African American patients not establishing with podiatric medicine prior to initiating HD, as opposed to approximately 50% of Caucasian patients who did not. This aligned with previous research showing that even leading up to the decision to initiate HD, access to a nephrologist for African Americans is often decreased and delayed.14,15 It has been shown to lead to severe adverse outcomes including increased mortality rates,16 increased rates of hospitalizations,17 lower rates of renal transplantation18 and lower rates of arteriovenous fistula creations.19
Podiatry interventions have been demonstrated to reduce higher level amputations through regular podiatric care. The use of extra depth shoes/plastazote inserts and implementation of multidisciplinary teams to address DFU demonstrate efficacy to reduce DFU recurrence and prevent major amputations.11 Additionally, ESRD has been continually demonstrated as a risk factor for non- and poor-healing in the DFU population. However, the evidence evaluating podiatry care before or after initiation of dialysis is limited. Therefore, our study was one of the first studies to investigate if outcomes are associated with initiation of podiatric care with respect to initiation of dialysis.
A study of 14,935 adults with kidney failure and newly diagnosed DFU found that only 18.4% received podiatric care prior to diagnosis, yet this care was associated with significantly lower rates of death and major amputation, highlighting a critical gap in preventive care for this high-risk population.20 Our study directly assessed the impact of receiving podiatric care, and although non-significant, revealed there was an increased chance of undergoing a major amputation in patients who did not establish with podiatry prior to initiating dialysis.
There were several advantages and limitations to this study. First, our study had a retrospective design and therefore has a potential inability to address all confounding variables and was notable in the clinically significant different ages and BMI between the two groups. Although this may confound the results, to address this, we evaluated the HD and CKD patient population using strict eligibility criteria and assessed charts consecutively. Secondly, there is an inherent subjectivity bias. We limited reviewers to two individuals who standardized eligibility criteria prior to chart review and were both in agreement to terms and criterion. In cases of dispute, the third author acted as an arbiter. Third, we had a limited sample size. Despite these limitations there are advantages to our study in that this study compared advanced stage kidney disease to end stage renal disease and uniquely assessed diabetic foot complications in this patient population. In addition this study did show an imperative need for preventative care in both of these patient populations. Our study lays the foundation for a future prospective study to evaluate the effectiveness of podiatry intervention to prevent diabetes-related amputations in patients with kidney disease. This would provide information on whether patients with chronic kidney disease should be established with a podiatrist versus being able to wait until they are initiated on ESRD.
In our population, there was no difference in amputations with patients receiving podiatry intervention before or after initiation of dialysis. Our study demonstrated several important additional findings: a potential racial disparity evident in African Americans and access to podiatry care prior to initiating HD, patients with PAD were less likely to establish with podiatry prior to initiating HD, and patients were more likely to undergo major amputation if they did not establish with podiatry prior to initiation of HD. More work is needed to further examine this relationship to determine if the disparities revealed through our analysis are truly secondary to a disparity or if improved access diminishes these concerns.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Footnotes
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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