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Peer Review

Peer Reviewed

Literature Review

Reviewing Recommendations From the IWGDF 2023 Guidelines on the Diagnosis and Treatment of Active Charcot Neuro-Osteoarthropathy: Highlighting the Role of Temperature Monitoring With Illustrative Case Reports

June 2024
1943-2704
Wounds. 2024;36(6):206-211. doi:10.25270/wnds/24029

Abstract

The International Working Group on the Diabetic Foot (IWGDF) has consistently published evidence-based guideline recommendations on the prevention and management of diabetes-related foot complications. In 2023, the group published their first guidelines on the diagnosis and treatment of Charcot neuro-osteoarthropathy (CNO) in persons with diabetes. The guidelines highlight 26 recommendations based on 4 categories: diagnosis, identification of remission, treatment, and prevention of re-activation. As reviewed in the guidelines, there are 2 recommendations suggesting the use of temperature assessment and monitoring as a tool for management of patients with CNO. Utilizing the systematic review and the GRADE system of evaluation, the authors deemed the level of evidence around temperature monitoring and Charcot to be low with a conditional recommendation for use. The purpose of this manuscript is to summarize the IWGDF guidelines while highlighting the role of foot temperature monitoring. Several case examples are given to illustrate the use of temperature monitoring in patients with CNO. Until there are guidelines determining active vs quiescent CNO, skin temperature monitoring can be a fast, easy-to-use, and effective tool for the clinician.

Abbreviations: CNO, Charcot neuro-osteoarthropathy; Hb, hemoglobin; IDF, International Diabetes Foundation; IWGDF, International Working Group on the Diabetic Foot; MRI, magnetic resonance imaging; PAD, peripheral artery disease.

Background

For over 20 years, the IWGDF has published evidence-based guideline recommendations on the prevention and management of diabetes-related foot complications. In 2023, the group published their first guidelines on the diagnosis and treatment of CNO in persons with diabetes.1 According to the authors, the recommendations are based on “evidence from systematic reviews and expert opinion, accounting for the benefits and harms, patient preferences, feasibility and applicability, and costs related to interventions.”

CNO is considered an inflammatory condition in persons with peripheral polyneuropathy which can result in significant injury to bones, joints, and soft tissues. The disease is most common among people with diabetes and may result in significant foot deformity. It is a known risk factor for decreased quality of life, ulceration, amputation, and increased mortality rates. According to the IDF, in 2021 approximately 537 million adults were living with diabetes. Given CNO foot prevalence of 0.3% and using the IDF estimates from 2021, this translates to 1.6 million people worldwide and 160 000 new cases diagnosed annually left to manage the challenging issues associated with CNO.2

Pakarinen et al reported the average duration of diabetes prior to developing CNO is around 10 years, and it is more commonly seen in males in their fifth and sixth decades of life.3 While the absolute etiology of CNO is still debated, peripheral neuropathy is the most widely accepted precursor to CNO. The clinical findings of sympathetic denervation, loss of protective sensation, hyperemia, and osteopenia are the most significant findings associated with CNO. Furthermore, the pathogenesis is linked to pro-inflammatory cytokines resulting in progressive inflammatory destruction of weightbearing joints in the foot.4 

IWGDF Charcot Neuro-osteoarthropathy Recommendations

The guidelines highlight 26 recommend-ations based on 4 categories: diagnosis, identification of remission, treatment, and prevention of re-activation (Table).1 The guidelines were written for all providers treating patients with diabetes. As these are the first guidelines for CNO, they were designed to make recommendations for patients with intact skin only.
Table 1A

Table 1B

 

It is proposed that all clinicians treating people with diabetes and neuropathy have a high clinical index of suspicion for CNO when a patient presents with a red, hot, swollen foot, especially in the absence of a wound. Schmidt et al reported on survey results that 67% of doctors working in a major teaching center admitted that their knowledge of the Charcot foot was either scant or nonexistent.5 The most common misdiagnosis for CNO is cellulitis and may cause a delay in appropriate treatment. The goal of CNO management is to convert the active process to quiescent. This can be challenging for the clinician as return to full activity and standard shoes prematurely may result in further disability. Determining CNO quiescence is often based on clinical intuition, as there are little objective data available to help in the decision-making process. 

 

Temperature Monitoring

Charcot

Along with these guidelines, temperature assessment and monitoring has become a tool for management of patients with CNO. Recommendations 2 and 3 of the IWGDF guidelines reference temperature monitoring. Utilizing systematic review and the GRADE system of evaluation, the authors deemed the level of evidence around temperature monitoring and Charcot to be low with a conditional recommendation for use.1 A systematic review conducted by Jones et al studied contralateral foot temperature monitoring during Charcot immobilization. They reported “temperature monitoring is typically performed every 2–6 weeks using handheld thermometry of the CNO site after feet rested for 15 minutes. The threshold for cessation of immobilization ranged from <1°C to <2°C although frequently it was <2°C sustained for 2–3 visits.” They did report that the number of temperature measurement sites and their location did vary across studies. There are insufficient data within the research to determine whether contralateral temperature differences at presentation is usually lower in stage 0 than stage 1 CNO.5,6 Therefore, a specific benchmark threshold for asymmetry has not been established and/or related to CNO staging. 

Foot temperature monitoring in CNO is complicated as there is a complex relationship between neuropathy and distal limb blood flow. Several studies have demonstrated increased distal limb blood flow in people with established neuropathy, as is commonly associated with CNO. However, there is also evidence that people with distal neuropathy may develop vascular calcification.7 This calcification is recognized to directly correlate with osteopenia, also a predisposing complication factor in CNO. However, it is unclear what role calcification plays on distal limb blood flow. Arteriovenous shunting and reduction in the capacity for arterial dilatation may occur with vascular calcification. Ultimately, this may be associated with decreased peripheral resistance and a compromise in the ability for local tissue to mount an appropriate inflammatory response. Though not commonly associated, there is a possibility that PAD and CNO can coexist.7,8 While these challenges are significant, temperature monitoring remains an available option in the management of CNO. 

 

Case examples

The first randomized clinical trials utilizing temperature monitoring in high-risk feet were performed by Lavery and Armstrong.8,9 Collectively, they demonstrated a 72% reduction in recurrent ulcerations in an at-risk population. In these studies, patients were asked to perform skin temperature monitoring on the soles of their feet in 6 specific locations. They were told to self-monitor for skin temperature asymmetry and contact their providers if temperature differences were discovered. While the science proved successful, the patient burden was significant. Physical and cognitive challenges such as obesity, limited mobility, and eye disease limited successful implementation of this process; there was much room for error, though when performed correctly infrared thermometry remains a reliable assessment for these patients.10,11

In 2017, Frykberg et al published results on an innovative mat utilized for remote temperature monitoring of at-risk patients for recurrent ulceration.12 Clinical results revealed detection of 97% of ulcerations at a lead time of approximately 5 weeks. The innovation of remote temperature monitoring differs from the work of the early 2000s in that there are clinical recommendations provided via clinical support teams monitoring these patients. These offloading protocols are effective in eliminating inflammatory changes to the feet in 67% of patients preventing the potential development of ulceration and other complications.13

Here, the authors present 2 cases of temperature monitoring in active CNO with the use of a smart mat remote temperature monitoring (SmartMat, Podimetrics). There was no ethics or institutional review board approval for these cases as the institutional policy where the cases originate stated anything under 5 subjects does not constitute research. Both participants were veterans who lived remote to the clinic (240 miles and 75 miles, respectively) and were diagnosed with active CNO by a combination of infrared temperature measurements and radiography. As part of education on the disease process, both participants were instructed on the importance of temperature monitoring and offloading with the goal of deformity prevention. They were taught to stand for 20 seconds on the smart mat daily while a thermogram was performed. Deidentified thermometric data were sent to the cloud where algorithmic comparisons to the contralateral foot were performed at the level of the hallux; 1st, plantar 3rd, and 5th metatarsal-phalangeal joints; arch; and heel.13 If the difference between matching locations was greater than 1.75°C in 2 consecutive uses, a message was sent to the clinic and the podiatrist instructed the patient on a visual inspection of the feet over the phone. This temperature threshold was set below the usual 2°C due to the patients being at high risk for ulceration and their distance from the clinic.

Case 1. The patient is a 56-year-old male with diabetes (HbA1c: 8.3%), neuropathy, chronic kidney disease stage 3, osteoarthritis of the knees, obesity, and tobacco use disorder. Two months prior to presentation, the patient was diagnosed with a Sangeorzan type II navicular fracture on MRI at an outside hospital.14 He was given a tall boot (DH walker, Össur) and continued ambulating. When the patient maintained the red, hot, and swollen appearance of the foot, he presented to the authors’ hospital in normal shoe gear. The diagnosis of CNO was made with further MRI scans, and the patient was educated on the progressive nature of deformity, especially in the setting of a known fracture. The patient was instructed to wear the boot for protection only and be non-weightbearing with a knee scooter until out of the active stage, upwards of 6 to 12 months.15,16 He was seen in the clinic every other month for radiographic monitoring. 

On day 28, a temperature asymmetry was seen in one scan (Figure 1). On telephone outreach, the patient reported development of a superficial blister on the arch of the right foot. He was instructed to remain non-weightbearing and did daily foot checks to keep the skin protected until it healed without incident several days later.
Figure 1

The patient’s thermograms showed diffuse asymmetry averaging 2.7° through day 87 with significantly warmer right foot temperatures. On day 42, there was bony coalescence on radiograph, though the remote temperature monitoring continued to show asymmetry, with a peak delta of 6.7° on day 73. Complete non-weightbearing status continued. From day 86 to 98, the patient’s average temperature asymmetry reduced to 1.6°, when he started a program of gradual protected weightbearing. Thermography allowed the clinician to have timely outreach to the patient and potentially prevent the superficial break in the skin from progressing to a full-thickness ulcer by tailoring an offloading recommendation.

Case 2. The patient is a 67-year-old male with diabetes (HbA1c: 8.1%), neuropathy, hyperlipidemia, aortic stenosis, hypertension, and obesity. The patient was diagnosed with left foot Eichenholtz stage 1 CNO with fractures of all 5 metatarsal bases and medial and lateral cuneiforms 9 months prior to receipt of the smart mat. At the time of diagnosis, the patient was educated on the importance of non-weightbearing status due to fracture pattern. The patient declined total contact casting, though did wear an offloading boot “sometimes.” He was given a bone stimulator (Exogen, Bioventus) approximately 4 months into the flare for fracture consolidation and custom molded shoes to replace slippers for use inside the house. Monthly radiographs were performed. One month prior to commencing thermometry, radiographs suggested consolidation, though the patient reported continued “extreme pain and swelling” in the foot (Figures 2, 3).
Figure 2
Figure 3

The patient was found to have low to moderate asymmetry, with 2 episodes of 2.2° noted on days 33 and 54 (Figure 4). Both prompted a phone call by the podiatrist. The patient was instructed to remain non-weightbearing and decrease physical activity; both resolved without clinical intervention. Monthly radiographs were performed and non-weightbearing continued until stable consolidation was seen for 3 months before introducing protected weightbearing. Thermography aided the clinician in this case where there was a discrepancy between clinical and radiographic signs of consolidation for several months. The patient was kept non-weightbearing and clinicians were able to better inform the patient of when it would be safe to start weightbearing by tracking the resolution of soft tissue inflammation.
Figure 4

Limitations

While there are recommendations for the initial treatment of Charcot, a major limitation is that there is no consensus on the signs and symptoms required to define the emergence out of the active phase. The question remains: When is it safe to reintroduce protected weightbearing and return to activities of daily living? An ongoing study in the United Kingdom is investigating this timepoint by employing MRI in conjunction with temperature monitoring and radiography.17 Another ongoing study in France aims to investigate the factors associated with quality of life in patients with diabetes and chronic, stable Charcot foot.18 Their secondary endpoints are changes in radiographic angles over 24 months.

Conclusion

In a meta-analysis by Yammine et al, it was reported that mortality frequencies in people with diabetes and CNO are higher than those reported in the population of people with diabetes without Charcot arthropathy.4 In the absence of the ability to prevent CNO, the goal is to prevent deformity, maintain a plantigrade foot and keep patients ulcer-free. Until there are guidelines determining active vs quiescent CNO, skin temperature monitoring can be a fast, easy-to-use, and effective tool for the clinician. 

Acknowledgments

Authors: Gary M. Rothenberg, DPM, CDCES, CWS1; Amanda L. Killeen, DPM, CWSP2; and Crystal Holmes, DPM, CWSP1

Affiliations: 1Department of Internal Medicine, University of Michigan Medical School, Ann Arbor, MI; ²University of Texas Rio Grande Valley School of Podiatric Medicine, Harlingen, TX 

ORCID: Killeen, 0000-0002-8461-9139

Disclosure: G.M.R. serves as Director of Medical Affairs for Podimetrics, Inc. The remaining authors disclose no financial or other conflicts of interest.

Correspondence: Gary M. Rothenberg, DPM; 24 Frank Lloyd Wright Drive, Internal Medicine / MEND Suite 1300, Ann Arbor, MI 48106; gmrdpm@med.umich.edu

Manuscript Accepted: May 24, 2024

Recommended Citation

Rothenberg GM, Killeen AL, Holmes C. Reviewing recommendations from the IWGDF 2023 Guidelines on the diagnosis and treatment of active Charcot neuro-osteoarthropathy: highlighting the role of temperature monitoring with illustrative case reports. Wounds. 2024;36(6):206-211. doi:10.25270/wnds/24029

References

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2. International Diabetes Foundation. IDF Diabetes Atlas, 10th Edition. 2021. https://www.diabetesatlas.org

3. Pakarinen TK, Laine HJ, Mäenpää H, Mattila P, Lahtela J. Long-term outcome and quality of life in patients with Charcot foot. Foot Ankle Surg. 2009;15(4):187-191. doi:10.1016/j.fas.2009.02.005 

4. Yammine K, Boulos K, Assi C, Hayek F. Amputation and mortality frequencies associated with diabetic Charcot foot arthropathy: a meta-analysis. Foot Ankle Surg. 2022;28(8):1170-1176. doi:10.1016/j.fas.2022.08.004. 

5. Schmidt BM, Wrobel JS, Holmes CM. Physician knowledge of a rare foot condition - influence of diabetic patient population on self-described knowledge and treatment. Clin Diabetes Endocrinol. 2017;3:2. doi:10.1186/s40842-017-0041-4 

6. Rosenbaum AJ, DiPreta JA. Classifications in brief: Eichenholtz classification of Charcot arthropathy. Clin Orthop Relat Res. 2015;473(3):1168-1171. doi:10.1007/s11999-014-4059-y

7. Aragón-Sánchez J, Lázaro-Martínez JL. Factors associated with calcification in the pedal arteries in patients with diabetes and neuropathy admitted for foot disease and its clinical significance. Int J Low Extrem Wounds. 2013;12(4):252-255. doi:10.1177/1534734613511636

8. Lavery LA, Higgins KR, Lanctot DR, et al. Preventing diabetic foot ulcer recurrence in high-risk patients: use of temperature monitoring as a self-assessment tool. Diabetes Care. 2007;30(1):14-20. doi:10.2337/dc06-1600

9. Armstrong DG, Holtz-Neiderer K, Wendel C, Mohler MJ, Kimbriel HR, Lavery LA. Skin temperature monitoring reduces the risk for diabetic foot ulceration in high-risk patients. Am J Med. 2007;120(12):1042-1046. doi: 10.1016/j.amjmed.2007.06.028. Erratum in: Am J Med. 2008;121(12). doi:10.1016/j.amjmed.2008.09.029 

10. Jebasingh F, Paul J, Bhattacharji S, et al. Plantar temperature and pressure distribution in subjects with diabetes mellitus and chronic Charcot arthropathy. Diabetes Res Clin Pract. 2023;197(1): 110290. doi10.1016/j.diabres.2023.110290

11. Dallimore SM, Puli N, Kim D, Kaminski MR. Infrared dermal thermometry is highly reliable in the assessment of patients with Charcot neuroarthropathy. J Foot Ankle Res. 2020;13(1):56. doi:10.1186/s13047-020-00421-z

12. Frykberg RG, Gordon IL, Reyzelman AM, et al. Feasibility and efficacy of a smart mat technology to predict development of diabetic plantar ulcers. Diabetes Care. 2017;40(7):973-980. doi:10.2337/dc16-2294

13. Rothenberg GM, Page J, Stuck R, Spencer C, Kaplan L, Gordon I. Remote temperature monitoring of the diabetic foot: from research to practice. Fed Pract. 2020;37(3):114-124.

14. Sangeorzan BJ, Benirschke SK, Mosca V, Mayo KA, Hansen ST Jr. Displaced intra-articular fractures of the tarsal navicular. J Bone Joint Surg Am. 1989;71(10):1504-1510.

15. Jansen RB, Jørgensen B, Holstein PE, Møller KK, Svendsen OL. Mortality and complications after treatment of acute diabetic Charcot foot. J Diabetes Complications. 2018;32(12):1141-1147. doi:10.1016/j.jdiacomp.2018.09.013

16. Güven MF, Karabiber A, Kaynak G, Oğüt T. Conservative and surgical treatment of the chronic Charcot foot and ankle. Diabet Foot Ankle. 2013;4. doi:10.3402/dfa.v4i0.21177

17. Gooday C, Game F, Woodburn J, et al. A randomised feasibility study of serial magnetic resonance imaging to reduce treatment times in Charcot neuroarthropathy in people with diabetes (CADOM): a protocol. Pilot Feasibility Stud. 2020;6:85. doi:10.1186/s40814-020-00611-3

18. WCG Clinical Trials Listing Service. Factors Associated with an Evolution in the Quality of Life of Diabetic Patients with Chronic, Wound-free Charcot Foot. Accessed January 2024. https://www.centerwatch.com/clinical-trials/listings/NCT05491577/factors-associated-with-an-evolution-in-the-quality-of-life-of-diabetic-patients-with-chronic-wound-free-charcot-foot

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