Abstract
Background:
The contralateral foot in Charcot arthropathy or neuroarthropathy (CN) is subject to increased plantar pressure. To date, the clinical consequences of this pressure elevation are yet to be determined. The aim of this study was to evaluate ulcer and amputation rates of the contralateral foot in CN.
Methods:
We abstracted the medical records of 130 consecutive subjects with unilateral CN. Rates of contralateral CN development and recurrence, contralateral ulcer development, and contralateral amputations were recorded. Statistical analysis was performed to identify possible risk factors for contralateral CN and ulcer development, and contralateral amputation. Mean follow-up was 6.2 (SD 4) years.
Results:
After a mean of 2.5 years, 19.2% patients developed contralateral CN. Female gender was associated with contralateral CN development (odds ratio 3.13, 95% confidence interval 1.27, 7.7). Overall, 46.2% patients developed a contralateral ulcer. Among the patients who developed contralateral CN, 60% developed an ulcer. Sanders type 2 at the index foot (midfoot CN) was significantly associated with contralateral ulcer development. Ulcer-free survival (UFS) differed significantly between patients with diabetes type 1 (median UFS 5131 days) and patients with diabetes type 2 (median UFS 2158 days). A total of 25 amputations had to be performed in 22 (16.9%) patients. Three of those 22 patients (2.3%) needed major amputation.
Conclusion:
Almost 20% of patients developed contralateral CN. Nearly half of people with CN developed a contralateral foot ulceration. Patients with type 2 diabetes had significantly shorter UFS than patients with diabetes type 1. Every sixth patient needed an amputation, with the majority being minor amputations. The contralateral foot should be monitored closely and included in the treatment in patients with CN.
Level of Evidence:
Level IV, retrospective study.
Keywords: Charcot foot, diabetes, ulcer, limb loss, major amputation
Background
Charcot arthropathy or neuroarthropathy (CN) was first described in 1868 as a mainly painless, progressive, and degenerative arthropathy of single or multiple joints.8,17,23 It occurs in patients with peripheral neuropathy with most of the patients having diabetes.6,7,18,20,22 CN has a prevalence ranging from 0.08% in the general diabetic population to 13% in high-risk diabetic patients.7,29,30 Recurrence of CN is a major concern and occurs in up to 15% of the patients.18 A rate of 2% to 33% of contralateral CN involvement has been described in the literature.4,19,24,30 Additionally, people with CN may be at greater risk of mortality than similar patients with diabetes without CN.3,28
Therapy aims at preserving the affected limb. Slightly more than half (51.5%) of the patients with CN need operative treatment.21 Osteomyelitis secondary to pressure related ulcerations often complicates treatment but does not preclude successful realignment arthrodesis in most cases. A major amputation rate of 2.7% per year has been reported, but this likelihood is elevated by a factor of 6 when CN related foot wounds are present.25,32 Foot biomechanics change significantly in CN. Plantar pressure peak is significantly elevated, leading often to pressure ulcers. The risk for ulcer development in patients with diabetic CN is 4 times elevated compared with the overall risk of foot ulcers in diabetic feet.13
However, there are no significant differences in peak plantar pressures between the affected foot and the contralateral one, suggesting pressure elevation in the “healthy” contralateral foot as well.2 Further, in patients treated with removable casts and walkers, the contralateral side is subject to high-pressure loads beneath the forefoot, including the hallux, first, second, third, and fifth metatarsal heads.14 The clinical consequences of this pressure elevation on the contralateral foot are unclear. Whether patients and surgeons should expect an increase on contralateral ulcers and amputations has yet to be reported. Long-term clinical outcome data concerning the contralateral foot and occurrence of contralateral CN is scarce. Contralateral extremity studies have mainly been focused on patients undergoing major amputation for PAD: 11.5% have contralateral major amputation and 9% have contralateral minor amputation within 5 years with atherosclerosis with diabetic neuropathy being a predictor for contralateral major amputation among others.11
Therefore, the aim of the present study was to determine the midterm outcomes of the contralateral foot in patients after being diagnosed with CN. To objectify the outcome, rates of contralateral CN development, ulcers, and amputations were evaluated. Further, a statistical analysis of possible predictors for contralateral CN, ulcer occurrence, and amputation was conducted. To prevent confusion, the site of initial CN was named “index foot” and the contralateral foot “foot of interest” throughout this manuscript.
Methods
A retrospective chart review was performed. The study was approved by the local ethical committee. Inclusion criteria were unilateral CN, age > 18 years, and length of clinical follow up of at least 2 years. Exclusion criteria were patients with insufficient documentation in the medical history, status after major amputation on the foot of interest site before diagnosis of CN was made, and clinical follow up of less than 2 years.
A total of 130 patients with unilateral CN treated at our institution between January 1, 1995, and March 31, 2018, were included in this study. In 81 patients, the index foot was the right foot, in 49 the left foot was affected with CN. Hence, 81 left and 49 right feet of interest were investigated. Information collected included demographic data, characteristics of CN of the index foot (Eichenholtz stage [Charcot activity classification] at diagnosis, Sanders and Frykberg type [anatomical distribution], therapy and complications), contralateral CN development, contralateral amputations, and ulcers.
Statistical analysis was performed using SPSS software, version 26 (IBM Corp, Armonk, NY). Age, gender, BMI, cause of polyneuropathy, diabetes type, renal insufficiency, PAD, and the type of operative procedure at the index foot (minor and/or major amputation, exostosis removal, realignment arthrodesis, soft tissue debridement) were tested as predictors for CN and ulcer development, and for amputation at the foot of interest. Associations between a categorical and an interval scaled variable were assessed using Mann-Whitney U test. Differences in continuous predictive variables were investigated using Student t tests. Relationships between categorical variables were tested using chi-square tests. Kaplan-Meier survival estimates were calculated for contralateral CN–free, ulcer-free, and amputation-free survival. A log-rank test was used to test for the association of those 3 outcome parameters with the above-named variables. Statistical significance was set at α = 0.05.
Results
Demographics
Patient demographics and CN characteristics of the index foot are summarized in Table 1. Forty-one patients (30.8%) were female. Mean age was 63.2 (SD 12.6) years. Mean follow-up was 6.2 (SD 4) years. Seventeen (13.1%) patients died during the follow-up period after a mean of 5.6 (SD 2.9) years, unrelated to CN. Cause of neuropathy was unknown in 17 patients, diabetes in 97 patients, vitamin B12 deficiency in 3 patients, pharmacologic in 1 patient, alcohol abuse in 7 patients, traumatic spinal cord injuries in 2 patients, and inflammatory in 3 patients.
Table 1.
Patient Demographics, (N = 130).
| n (%) | |
|---|---|
| Gender, n (%) | |
| Female | 40 (30.8) |
| Male | 90 (69.2) |
| Foot of interest, n (%) | |
| Right | 49 (37.7) |
| Left | 81 (62.3) |
| Cause of neuropathy, n (%) | |
| Diabetes | 97 (74.6) |
| Type 1 | 15 (11.5) |
| Type 2 | 82 (63.1) |
| Idiopathic | 17 (13.1) |
| Alcohol | 7 (5.4) |
| Vitamin B12 deficiency | 3 (2.3) |
| Inflammatory | 3 (2.3) |
| Spinal | 2 (1.5) |
| Pharmacologic | 1 (0.8) |
| Smoking, n (%) | |
| Yes | 41 (31.5) |
| No | 89 (68.5) |
| Peripheral artery disease, n (%) | |
| Yes | 30 (23.1) |
| No | 100 (76.9) |
| Renal insufficiency, n (%) | |
| Yes | 27 (20.8) |
| No | 103 (79.2) |
| Eichenholtz stage, index foot | |
| 0 (prodromal) | 8 (6.2) |
| 1 | 75 (57.7) |
| 2 | 15 (11.5) |
| 3 | 16 (12.3) |
| Infection | 16 (12.3) |
| Sanders type, index foot | |
| 1 | 19 (14.6) |
| 2 | 63 (48.4) |
| 3 | 37 (28.5) |
| 4 | 7 (5.4) |
| 5 | 4 (3.1) |
Charcot Development (Foot of Interest)
Twenty-five (19.2%) patients developed CN in the foot of interest after a mean of 2.5 (SD 3.2) years. Three patients (15.8%) developed recurrence of CN in the foot of interest after another 1.5 years. Four patients (16%) were diagnosed at the prodromal stage (added to the Eichenholtz classification9 by Shibata et al27), 6 patients (24%) at Eichenholtz stage 1, 13 (52%) at stage 2, and 2 (8%) at stage 3. Anatomically (using the Sanders and Frykberg classification26), 5 patients (20%) had type 1, 11 (44%) type 2, 7 (28%) type 3, and 2 (8%) type 4. CN characteristics of the foot of interest are shown in Table 2. A Kaplan-Meier survival estimate for CN-free survival of the foot of interest is shown in Figure 1.
Table 2.
CN Characteristics Foot of Interest.
| CN development (n = 25, 19.2%) | n (%) |
|---|---|
| Eichenholtz stage | |
| 0 (prodromal) | 4 (16) |
| 1 | 6 (24) |
| 2 | 13 (52) |
| 3 | 2 (8) |
| Infection | 0 |
| Sanders type | |
| 1 | 5 (20) |
| 2 | 11 (44) |
| 3 | 7 (28) |
| 4 | 2 (8) |
| 5 | 0 |
| CN recurrence (n = 3/25, 12%) | |
| Eichenholtz stage | |
| 0 (prodromal) | 0 |
| 1 | 0 |
| 2 | 3 (100) |
| 3 | 0 |
| Infection | 0 |
| Sanders type | |
| 1 | 1 (33.3) |
| 2 | 2 (66.7) |
| 3 | 0 |
| 4 | 0 |
| 5 | 0 |
Abbreviation: CN, Charcot arthropathy or neuroarthropathy.
Figure 1.
Kaplan-Meier survival estimate for Charcot arthropathy or neuroarthropathy (CN)–free survival (foot of interest).
Predictors for Charcot Foot Development (Foot of Interest)
Only female gender (P = .015) was significantly associated with contralateral Charcot foot development whereas age (P = .36), BMI (P = .98), Sanders type of the index foot (P = .32), cause of neuropathy (P = .24), presence of diabetes (P = .64), presence of PAD (P = .8), renal insufficiency (P = .41), and type of operative therapy of the index foot (P = .88) were not. Figure 2 shows a gender-dependent Kaplan-Meier survival estimate for CN-free survival of the foot of interest. The log-rank test was statistically significant (P = .003), reaffirming female gender as a risk factor for CN development at the foot of interest. Odds ratio (OR) for female patients to develop CN at the foot of interest was 3.13 (95% CI 1.27, 7.7; P = .013).
Figure 2.
Gender dependent Kaplan-Meier survival estimate for Charcot arthropathy or neuroarthropathy (CN)–free survival (foot of interest).
Ulcer Development
Sixty (46.2%) patients developed an ulcer at the foot of interest. Forty-two of 60 ulcers (70%) were located at the forefoot level, 17/60 (28.3%) at the midfoot level, and 1/60 (1.7%) at the hindfoot level. Mean time from CN diagnosis to ulcer occurrence was 3.5 (SD 3.8) years. Among the 25 patients who developed CN at the foot of interest, 15 (60%) developed an ulcer. Seven of 15 ulcers (46.7%) were located at the forefoot level, and 8/15 (53.3%) at the midfoot level. Mean time from CN diagnosis at the foot of interest to ulcer occurrence was 14.6 days. There was no statistically significant difference for ulcer development between patients with and without CN at the foot of interest (P = .12). Thirty-six patients (27.7%) had ulcer recurrence; 21 (58.3%) were forefoot ulcers, 12 (33.3%) midfoot ulcers, and 3 (8.3%) hindfoot ulcers. Mean time from primary ulcer healing to ulcer recurrence was 2.2 (SD 1.9) years. In 24 patients (66.7%), ulcer recurrence occurred at the same localization as the first ulcer.
Predictors for Ulcer Development (Foot of Interest)
Sanders type at the index foot (P = .031) was significantly associated with ulcer development on the foot of interest. In patients with a Sanders type 2 deformity, the percentage of contralateral ulcer development was the highest with 57.1%. (Sanders type distribution in patients with and without ulcers is shown in detail in Table 3.) Age (P = .44), BMI (P = .52), cause of neuropathy (P = .22), diabetes (P = .066), PAD (P = .408), renal insufficiency (P= .055), gender (P = .57), and type of operative therapy of the index foot (P = .3) showed no statistically significant association with ulcer development. Figure 3 shows a Kaplan-Meier survival estimate for ulcer-free survival (UFS) of the foot of interest depending on diabetes type and absence of diabetes. The log-rank test showed no statistically significant difference between patients without diabetes and diabetes type 1 (P = .175) and patients without diabetes and diabetes type 2 (P = .349). However, there was a statistically significant difference in UFS between patients with diabetes type 1 (median UFS 5131 days) and diabetes type 2 (median UFS 2158 days) (P = .01). Figure 4 shows a Kaplan-Meier survival estimate for UFS of the foot of interest depending on the Sanders type of the index foot. The log-rank test revealed a significant difference in ulcer development between Sanders type 2 and Sanders type 3 (P = .03). There was no statistically significant association between ulcer recurrence and CN recurrence at the foot of interest.
Table 3.
Sanders Type (Index Foot) in Patients With and Without Ulcers.
| Sanders type | Total, n (%) |
With ulcer, n (%) |
Without ulcer, n (%) |
|---|---|---|---|
| 1 | 19 (100) | 9 (47.4) | 10 (52.6) |
| 2 | 63 (100) | 36 (57.1) | 27 (42.9) |
| 3 | 37 (100) | 12 (32.4) | 25 (67.6) |
| 4 | 7 (100) | 2 (28.6) | 5 (71.4) |
| 5 | 4 (100) | 0 (0) | 4 (100) |
Figure 3.
Diabetes-dependent Kaplan-Meier survival estimate for ulcer-free survival (foot of interest).
Figure 4.
Sanders type (index foot)–dependent Kaplan-Meier survival estimate for ulcer-free survival (foot of interest).
Amputations
A total of 25 amputations were performed in 22 (16.9%) patients. Three patients (2.3%) had 2 subsequent amputations. Twenty-two (88%) were minor amputations, and 3 (12%) were major amputations (transtibial amputation). Hence, limb loss occurred in 2.3% of the study cohort. Mean time to first amputation was 6.1 (SD 3.6) years. The second amputation was performed at 0 (13 days), 4, and 49 months after the first amputation. The 3 major amputations occurred after 28, 28, and 111 months, respectively, and were all primary major amputations. Thus, no minor amputation had to be converted to a major one. Reasons for major amputation were osteomyelitis in 2 cases whereas the remaining patient had fulminant soft tissue infection with sepsis. Figure 5 shows a Kaplan-Meier survival estimate for amputation-free survival of the foot of interest.
Figure 5.
Kaplan-Meier survival estimate for amputation-free survival (foot of interest).
Predictors for Amputations (Foot of Interest)
Among the tested variables, there were no statistically significant associations with amputations performed at the foot of interest (age, P = .48; BMI, P = .56; Sanders type index foot, P = .41; cause of neuropathy, P = .85; diabetes, P = .57; PAD, P = .59; renal insufficiency, P = .25; gender, P = .2; and type of operative therapy of the index foot, P = .98)). However, the log-rank test calculated for renal insufficiency–dependent Kaplan-Meier survival estimate for amputation-free survival of the foot of interest revealed a statistically significant difference (P = .043) (Figure 6).
Figure 6.
Amputation-free survivorship curves for patients initially presenting with renal insufficiency vs patients without renal insufficiency (foot of interest).
Discussion
The clinical relevance of this study is that patients with CN often develop complications in the contralateral foot, which must be included in the treatment strategy. CN occurred in 19.2% after a mean of 29.4 months at the foot of interest. Prior studies reported bilateral CN involvement in 2.4% to 33% but relied almost exclusively on clinical findings and radiographs for diagnosis or were subject to selection bias.5,10,12,16,19,25 In contrast, the diagnosis in our population was made based on clinical signs, radiographs, and MRI, preventing under- and overestimation of true CN activity by the addition of information on bone edema. Previously unreported, female gender was associated with contralateral CN development (OR 3.13, 95% CI 1.27, 7.7). Women are known to lose bone at a younger age, more rapidly than men, to have higher bone resorption markers and to have less peri-osteal bone.1 The result of decreased bone strength is a possible explanation for women to be more susceptible to contralateral CN development. Admittedly, the rather broad range of the 95% CI could reflect an undersized sample size.
Overall, 46.2% of the patients overall developed an ulcer at the foot of interest during the follow-up period. UFS was 81.5% after 1 year (95% CI 75.66%, 87.34%). Comparative data are not available for CN. As patients with CN have neuropathy, the importance of our results is best reflected by comparing them to neuropathic feet. In a prospective observational study, O’Hare reported an annual ulcer prevalence of 1.9% in patients with diabetic neuropathy.17 Compared with O’Hare’s results, ulcer incidence at the foot of interest within the first year after diagnosis of CN at the index foot was almost 10 times more frequent in the present cohort. We attribute the accentuation of ulcer development at the foot of interest within the first year to total contact casting and unloading of the index foot and the subsequent overuse of the contralateral foot.
Twenty-five amputations were performed on the foot of interest in 22 (16.9%) patients overall; 22 (88%) were minor and 3 (12%) were major amputations (transtibial amputation). Hence, limb loss occurred in 2.3% of the study cohort. Analyzing the Kaplan-Meier survival curve of our cohort, only 6.2% (8/130) patients needed an amputation within the first 5 years. The 10-year amputation rate increased to 16.2%. The literature reports a 5-year amputation rate in patients with neuropathy of 11%.15 A possible explanation for the lower number of amputations compared to neuropathic ulcers after 5 years might be activity reduction originating from CN at the index foot. Further, outpatient-based control of the index foot was made at least every 3–6 months. In our institution, undressing and examination of both feet is mandatory, so critical wounds may have been detected early enough to prevent amputations.
Eight of 25 (32%) patients with CN at the foot of interest needed an amputation. The literature reports that up to 25.7% of patients with unilateral CN need an amputation.5,10,12,16,19,25,31 Hence, the overall necessity of amputation procedures was higher than in patients with unilateral CN.
Our study results confirm that the contralateral foot in CN is at risk of developing severe complications. It is plausible that these complications arise at least partially from plantar pressure elevation. We believe for the management of CN there are several consequences:
Protecting the contralateral foot (eg, with a custom molded insole) to adapt for plantar pressure elevation is paramount. This must be started immediately when diagnosis of CN at the index foot was made and upheld lifelong.
Once CN has been diagnosed, both feet must be uncovered and checked for ulcers and CN activation signs at every outpatient visit. The contralateral foot is particularly vulnerable to ulcer development within the first year after diagnosis of CN. The authors recommend evaluations every 2 to 4 weeks as long as there is CN activity.
Visits cannot be stopped when CN at the index foot has transferred to an inactive Eichenholtz 3 stage as CN development, ulcer development, and need of amputations should be anticipated at the contralateral foot during the entire clinical course. Thus, the authors recommend lifelong evaluations every 3 months once the index foot has reached an inactive Eichenholtz stage 3.
Limitations are the retrospective study design, the heterogeneity of neuropathy, the small sample size, and a possible treatment bias.
In conclusion, we found that in CN, every fifth patient developed contralateral CN. Almost every second patient developed contralateral foot ulceration, 40% within the first year after diagnosis of CN. Patients with diabetes type 2 had significantly shorter ulcer-free survival than patients with diabetes type 1. Every sixth patient needed an amputation, with the majority being minor amputations and a higher frequency if CN occurred bilaterally. Almost two-thirds of these amputations occurred 5 years after diagnosis of CN at the index foot. Thus, special care of the contralateral foot in CN should be taken on a long-term basis as well in order to maintain skin integrity and walking ability.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Footnotes
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. ICMJE forms for all authors are available online.
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