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Association between sarcopenia and the foot-ankle function in type 2 diabetic foot ulcer

Diabetology & Metabolic Syndrome volume 16, Article number: 270 (2024) Cite this article

Abstract

Background

The diabetic foot (DF) ulcer is the severe complication of type 2 diabetes mellitus (T2DM). Sarcopenia is characterized as the loss of muscle mass and strength, resulting in the increased risk of fracture and physical disability. Sarcopenia may affect the foot-ankle function in DF ulcer patients, compromise the quality of life.

Objective

The aim was to clarify the effect of sarcopenia on foot-ankle function in patients with DF ulcer.

Methods

In total of 108 T2DM patients with DF ulcer were enrolled. Based on the examination of muscle mass by dual energy X-ray absorptiometry (DXA) and grip strength and 5x sit-to-stand test, the DF patients were divided into sarcopenia and non-sarcopenia groups. The severity of DF ulcer was evaluated by Wagner classification. The foot-ankle function was evaluated by American Orthopaedic Foot and Ankle Society (AOFAS) Ankle-Hindfoot Score.

Results

DF patients with sarcopenia showed advanced age, lower BMI, longer duration of T2DM, and more severe Wagner classification, reduced appendicular skeletal muscle mass index (ASMI), grip strength, transcutaneous oxygenpressure (TcPO2) and prolonged time of 5X sit-to-stand test. The stratified comparison analysis indicated that severity of sarcopenia and DF ulcer, reduced TcPO2, and grip strength were aggravated with the impaired foot-ankle function (P < 0.05). Multivariate Logistic analysis showed that age, TcPO2, and severe sarcopenia were risk factors deteriorating the foot-ankle function.

Conclusion

The sarcopenia is a key risk factor of decreasing foot-ankle function in patients with DF ulcer. Thus, the prevention of muscle mass and strength loss could be considered as part of comprehensive therapy for DF ulcer.

Introduction

The diabetic foot (DF) ulcer is severe complication of type 2 diabetes mellitus (T2DM), which has become one of the main causes of disability and death. It is estimated that 9.1–26.1 million diabetic patients develop DF ulcers each year in worldwide [1], according to a national cohort study in Scotland, the overall incidence rate of DF ulcers was 11.2 per 1,000 person [2]. The therapy costs for DF ulcer become the financial burden.

In recent years, the incidence of T2DM in China has been rapidly increased. The prevalence of DF among T2DM patients is 25%, within which the rate of amputation is 26.4% [3]. It worsen the physical function and quality of life of T2DM patients. The foot and ankle joint play a vital role in maintaining proprioception, preserving balance and movement. Foot-ankle dysfunction can be characterized as gait changes, plantar pressure, pain, mobility and support stability. Factors including aging, reduced muscle strength, altered joint mobility, mechanical structural changes of foot, diabetic peripheral neuropathy (DPN) and diabetic peripheral vascular disease (DPVD) could affect foot-ankle function. These factors increase the risk of falls, bone fractures, and foot ulcers, leading to worse prognosis.

Sarcopenia is characterized as the loss of muscle mass and strength. Sarcopenia may affect physical mobility, resulting in the risk of fracture, disability, and even death [4, 5]. DF ulcer may worsen sarcopenia due to the infection and muscle dystrophy. Furthermore, patients with DF ulcer always showed long disease duration and muscle atrophy due to the long-term physical disability and restriction of movement. The combined effects of those factors result in changes of walking pattern and a decrease in overall body stability. It may increase the risk of developing ulcers, amputations and mortality. During the therapy of DF ulcer, the resistance to movement and bedridden lead to the quick muscle loss. The loss of muscle mass and strength forms a vicious circle and aggravates DF ulcer and impaired joint function in turn. However, the pathophysiology mechanism by which the reduced muscle mass and strength affect foot-ankle function was unclear. The sarcopenia may affect the foot-ankle function in DF ulcer patients, leading to prolonged recovery time and poor prognosis of physical function, thus compromise the quality of life. However, there were limited studies to clarify the relationship between sarcopenia and foot-ankle function in DF patients.

In this study, we aimed to clarify the effect of sarcopenia on foot-ankle function in patients with DF ulcer. It could provide clinical evidence for the early examination and prevention of muscle loss to achieve advanced foot-ankle function. The prevention and therapy for sarcopenia may be considered as part of comprehensive therapeutic strategy for DF ulcer.

Materials and methods

Study population

This study enrolled 108 patients with type 2 diabetic foot ulcer who were hospitalized in the Affiliated Hospital of Qingdao University from January 2021 to December 2022. Inclusion criteria: (1) meeting the diagnostic criteria of the Asian Working Group for Sarcopenia (AWGS) 2019 [6]; (2) age ranged from 18 to 80 years old, and diagnosed as T2DM according to the diagnostic standard of the World Health Organization (WHO) in 1999. All the Participants signed the informed consent. Exclusion criteria: (1) patients with type 1 DM (T1DM) or special types of DM; (2) patients with severe cardiac, liver and renal dysfunction, neurological diseases, bone and joint diseases, or autoimmune disorders; (3) bedridden for a long-term, or patients fitted with fracture internal fixation plates; (4) patients who are cognitively impaired and mentally ill; (5) malignant tumors, acute infectious diseases, or other chronic consumptive diseases.

General clinical data collection and laboratory tests

The general clinical data collection and test examinations were performed. We collected the general clinical characteristics including gender, age, body mass index (BMI is calculated as weight/height2), duration of T2DM, and duration of DF ulcer. All patients were fasted for more than 12 h. The serum and plasma were collected and examined according to the standard protocol.

Assessment of Sarcopenia

Body composition was assessed by dual energy X-ray absorptiometry (DXA) (Norland, USA). Height-corrected appendicular skeletal muscle mass index [ASMI = limb skeletal muscle mass (kg)/height2 (m2)] was used. Based on the diagnostic consensus of AWGS 2019 [6], patient with the appendicular skeletal muscle mass index (ASMI) < 7.0 kg/m2 for men and < 5.4 kg/m2 for women is diagnosed with sarcopenia.

Muscle strength was assessed using a medical grip strength device. The patient was seated with their elbow bent at a 90° angle. The dominant hand was measured twice and the maximum value was recorded. According to the grip strength diagnostic thresholds of AWGS Consensus 2019 [6], the diagnostic criteria of sarcopenia is grip strength < 28 kg for male, and < 18 kg for female. The patient’s trunk function was assessed using the 5X sit-to-stand test instead of using gait speed [6]. Patients were instructed to place their hands on their shoulders and stand up from a chair that was 46 cm in height. This process was recorded five times. The diagnostic criteria of reduced trunk function is that the patient takes 12 s or more to complete all 5 times of sit-stands. Based on AWGS Consensus of sarcopenia, patient with decreased muscle mass in their limbs, along with reduced muscle strength or trunk function is diagnosed as sarcopenia. In addition, if patient shows decreased muscle mass in their limbs along with reduced muscle strength and trunk function, they can be diagnosed with severe sarcopenia.

Grade assessment of diabetic foot ulcers

Grade assessment was conducted by medical professionals using the Wagner classification (Grade 0–5): Grade 0 represents a high-risk foot, with no ulceration but presenting risk factors for ulceration and infection; Grade 1 represents superficial ulceration without infection; Grade 2 indicates a moderately deep ulceration, often accompanied by soft tissue infection, without abscess or osteomyelitis; Grade 3 is characterized as deep ulceration, commonly accompanied by abscess and osteomyelitis; Grade 4 corresponds to localized gangrene, frequently associated with neuropathy, and Grade 5 denotes extensive or total foot gangrene [7].

Assessment of foot-ankle function and measurement of TcPO2

Specialists evaluate foot-ankle function using American Orthopaedic Foot and Ankle Society (AOFAS) Ankle-Hindfoot Score [8]. According to the AOFAS ankle-hindfoot score, the ankle-foot function was evaluated and graded as “excellent, good, fair, poor” groups. The parameters included pain, function, autonomous activity, support, maximum walking distance, grand walking, abnormal gait, anteroposterior movement, hind-foot movement, ankle-hindfoot stability, and alignment. The grade was classified as Excellent group: 90 ~ 100 points, Good group: 75 ~ 89 points, Fair group: 50 ~ 74 points, and Poor group: <50 points (Suppl Table 1) [9]. The analysis of TcPO2 was performed by skilled technicians using a TcPO2 analyzer manufactured (Radiometer Medical ApS, Denmark).

In order to minimize bias, two experienced physicians performed the AOFAS ankle-hindfoot scale assessments independently. Both physicians received comprehensive training on the administration and physical examination of the AOFAS ankle-hindfoot score from an experienced podiatrists.

Statistical analysis

The statistical analyses were conducted using SPSS Statistics 26.0. Results were presented as mean ± standard deviation (SD). The t-test was performed for comparison between two groups of normally distributed continuous data (mean ± SD). For comparison of continuous data among multiple groups, one-way analysis of variance (ANOVA) was used. For non-normally distributed continuous data, the comparison was conducted using non-parametric tests represented by median. Then we performed post-hoc analysis on these continuous data using Bonferroni correction. The comparison of categorical data was presented as percentages, and the analysis performed using the chi-squared test or Fisher’s exact test. Logistic regression analysis was employed for the analysis of influencing factors. P < 0.05 was considered as statistically significant differences.

Results

Parameters of foot-ankle function aggravate in the DF patients with Sarcopenia

Patients with DF ulcer were divided into DF with sarcopenia group and DF without sarcopenia group. As shown in Tables 1 and 2, age, BMI, duration of diabetes, Wagner classification, ASMI, Grip strength, 5X sit-to-stand test, transcutaneous oxygenpressure (TcPO2), and serum creatine (sCr) were significant different between the two groups (P < 0.05). DF with sarcopenia patients showed advanced age, lower BMI, longer duration of T2DM and DF ulcer, and more severe Wagner classification (Table 1). In addition, sarcopenia group showed reduced ASMI, grip strength, prolonged 5X sit-to-stand time, and reduced TcPO2 (Table 2).

Table 1 Comparison of clinical characteristics between the Sarcopenia and non-sarcopenia groups in DF ulcer patients
Full size table
Table 2 Comparison of indicators between the Sarcopenia and non-sarcopenia groups in DF patients
Full size table

Comparison of clinical characteristics between DF patients with or without Sarcopenia

We compared the clinical characteristics between groups of DF with or without sarcopenia. In DF with sarcopenia group, patients showed higher sCr after adjusted age, sex, BMI, duration of DM, Wagner classification. There was no difference between two groups of the blood glucose level, including FBG and HbA1c, liver function, uric acid, UACR, or lipid profiles including total cholesterol (TC), triglyceride (TG), low-density-lipoprotein cholesterol (LDL-C) and high-density-lipoprotein cholesterol (HDL-C) (Table 3).

Table 3 Comparison of biochemical indicators between the Sarcopenia and non-sarcopenia groups in DF patients
Full size table

The stratified comparison analysis of foot-ankle function in patients with DF ulcer

The ankle-foot function was evaluated and graded as “excellent, good, fair, poor” groups according to the AOFAS ankle-hindfoot score [8] (Suppl Table 1). The univariate analysis showed that age, severity of ulcer, sarcopenia severity, TcPO2, grip strength, 5X sit-to-stand test, lumbar T-score, femoral T-score were significant different among excellent, good, fair and poor groups of foot-ankle function in patients with DF ulcer (P < 0.05) (Table 4). The foot-ankle function significantly exacerbated with aging. The severity of ulcer and sarcopenia, including grip strength, 5X sit-to-stand test, and TcPO2 deteriorated with the progression of impaired foot-ankle function. In addition, TG, HDL-C, D-dimer, and CRP were significantly different among excellent, good, fair and poor groups of foot-ankle function (P < 0.05) (Table 4). The stratified comparison analysis indicated that severity of sarcopenia and DF ulcer, grip strength, 5X sit-to-stand test, reduced TcPO2, and bone mineral density (BMD) were aggravated with the impaired foot-ankle function.

Table 4 Stratified comparison of foot-ankle function in patients with type 2 diabetic foot
Full size table

Logistic analysis of the factors influencing foot-ankle function in DF ulcer patients

Multivariate Logistic regression analysis showed that the age, TcPO2, and severity of sarcopenia were independent risk factors for foot-ankle function. Compared to patients with severe sarcopenia, the odds ratio (OR) was 0.056 (P = 0.032), 0.082 (P = 0.041), and 0.091 (P = 0.043) in sarcopenia grading of 0, 1, and 2 patients, respectively (Table 5). The TcPO2, age, and sarcopenia severity were identified as the vital risk factors influencing foot-ankle function in DF ulcer patients.

Table 5 Multivariate logistic regression analysis of factors influencing foot-ankle function in patients with DF
Full size table

Discussion

In this study, we investigated the relationship of sarcopenia and foot-ankle function in patients with DF ulcer. Sarcopenia was identified as the risk factor which affecting foot-ankle function. The AOFAS ankle-hindfoot scores were significantly reduced in sarcopenia group compared to those of non-sarcopenia. Furthermore, the stratified comparison of foot-ankle function showed that the impaired foot-ankle function deteriorated with the severity of sarcopenia. Thus, our study provided clinical evidence that sarcopenia aggravates the foot-ankle function in DF ulcer. The early examination and intervention of sarcopenia should be considered to defense the muscle wasting during the long-term comprehensive therapy for DF ulcer.

It is widely recognized that skeletal muscles play a crucial role in providing support and protection to joints. Impaired skeletal muscle function could lead to the decreased mobility and increased risk of falls and bone fractures. Recent studies indicate that the prevalence of sarcopenia among elderly Chinese patients with diabetes is 14.8% [10]. However, studies on sarcopenia in the DF population are limited. Previous studies indicated that sarcopenia in DF patients was associated with advanced age, longer duration of diabetes, poor glycemic control, and impaired vascular function [11, 12]. Oxidative stress and inflammation infiltration may disrupt the balance between muscle synthesis and degradation, thereby exacerbating muscle atrophy [13]. Severe lower extremity stenosis and DPN in DF patients, combined with factors including infections, malnutrition, immobility, could potentially increase the risk of sarcopenia and deteriorate the progression. DPN leads to the loss of motor units and reduction in nerve fibers, resulting in atrophy of lower extremity muscles and reduced muscle strength, especially in the intrinsic muscles of the lower extremities [14, 15]. With the neuro-degeneration, the skeletal muscle atrophy was progressive, leading to the alterations in the structure, gait, and changes in foot pressure. Those factors contribute to the increased risk of foot ulcers. Diabetic autonomic neuropathy leads to abnormal sweat secretion, dry and cracked skin, facilitating the formation of calluses, and alters foot pressure. Moreover, the opening of arteriovenous shunts is increased, results in the lower extremity hemodynamic disorders [16, 17]. The sensory abnormalities caused by DPN could manifest as lost of pain, temperature, and touch sensations. This lack of protective sensation leads to the exacerbating the occurrence of DF [18]. DPN impacts the sensory, motor, and autonomic nervous systems. It can also result in bone deformities, restricted joint mobility, unstable gait, and increased plantar pressure. In the condition of trauma, it can further lead to the development of DF ulcer [18,19,20]. Multiple studies have indicated that alterations in gait and body stability in T2DM patients occur before the clinical symptoms of DPN [21,22,23].

TcPO2 is a vital factor affecting foot-ankle function. DPVD results in heightened plantar pressure in T2DM patients. The increased pressure leads to the compression of plantar capillaries, and microangiopathy, then results in a vicious cycle [25]. Jung et al. reported that muscle mass in DF patients was related to the lower limb preservation [26]. In addition, sarcopenia increases the risk of mortality in diabetic amputees. The lower skeletal muscle capillarization may affect exercise capacity with aging [27]. A cross-sectional study suggested that decreased capillary density in skeletal muscles was observed in elderly individuals with sarcopenia, and the severity of sarcopenia was correlated with skeletal muscle capillarization [29]. Atherosclerosis occurs in T2DM patients due to poor glycemic control and dyslipidemia, leading to lower extremity arterial occlusion. The primary manifestations include intermittent claudication, rest pain, ulcers, and gangrene, which can affect the patient’s gait and balance stability [29]. A few studies reveal that peripheral arterial disease (PAD) is an independent risk factor for amputation in patients with DF [30,31,32].

There are several limitations of this study. First, this study was a cross-sectional observational study. We did not conduct the analysis of fellow-up and prognosis due to the poor compliance of DF patients. Further investigation associated with prognosis and long-term fellow-up will be performed in the future. Second, this study was conducted in small sample size. We will expand the sample size to provide firm clinical evidence. Third, several factors associated with sarcopenia were not included in this study, such as detailed evaluation of nutrition condition, exercise restriction, bedrest duration, anti-diabetic agents.

In summary, we indicated that DF patients with sarcopenia showed deteriorated foot-ankle function compared to those without sarcopenia. The severity of sarcopenia, age, and TcPO2 are the risk factors for impaired foot-ankle function in DF patients. Therefore, it is necessary to recognize the impact of sarcopenia on foot-ankle function, to improve quality of life, and decrease the risk of falls, fractures, and even mortality in aged T2DM patients.

Conclusion

In conclusion, the sarcopenia aggravates the foot-ankle function in patients with DF ulcer. Thus, the prevention of muscle mass and strength loss could be considered as part of comprehensive therapy for DF ulcer to improve the prognosis.

Data availability

The data generated and analyzed is included in the publication. Further detailed data are available from the corresponding author on reasonable request.

Abbreviations

T2DM:

type 2 diabetic mellitus

T1DM:

type 1 diabetic mellitus

DF:

diabetic foot

DXA:

dual energy X-ray absorptiometry

AOFAS:

American Orthopaedic Foot and Ankle Society

BMI:

Body mass index

ASMI:

appendicular skeletal muscle mass index

TcPO2 :

transcutaneous oxygenpressure

AWGS:

Asian Working Group for Sarcopenia

FINS:

fasting insulin

UACR:

urinary albumin creatinine ratio

CRP:

C-reactive protein

BMD:

bone mineral density

BMC:

bone mineral content

DPN:

diabetic peripheral neuropathy

DPVD:

diabetic peripheral vascular disease

OR:

odds ratio

SD:

standard deviation

ANOVA:

analysis of variance

HbA1c:

Hemoglobin A1c

FBG:

fasting blood glucose

C-P:

C-peptide

ALT:

Alanine transaminase

AST:

Aspartate transaminase

TG:

triglyceride

TC:

total cholestero

LDL-C:

low-density-lipoprotein cholesterol

HDL-C:

high-density-lipoprotein cholesterol

BUN:

Blood urea nitrogen

WBC:

white blood cell

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Funding

This work was supported by the grant from National Natural Science Foundation of China (Grant No. 82370890), The Shandong Higher Education Young Science and Technology Support Program (2023KJ224), Shandong Province medical health science and technology project (202303061702) and the Taishan Scholars Program of Shandong Province (Grant No.tsqn202312383).

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Author notes

  1. Shujing An and Weina Kuang contributed equally to this work.

Authors and Affiliations

  1. Department of Oral and Maxillofacial Surgery, The Affiliated Hospital of Qingdao University, Qingdao, China

    Shujing An

  2. Department of Endocrinology and Metabolism, The Affiliated Hospital of Qingdao University, Qingdao, 266003, China

    Shujing An, Weina Kuang, Yonglu Hu, Bingzi Dong, Chengqian Li & Yangang Wang

  3. University of North Carolina at Chapel Hill, Chapel Hill, USA

    Xinwei Li

  4. Cell and Developmental Biology, Rutgers University, New Brunswick, USA

    Xinwei Li

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Contributions

Weina Kuang collected the clinical data, and Shujing An performed statistical analysis. Shujing An, Weina Kuang and DBZ wrote the manuscript. Yonglu Hu and Xinwei Li assisted the study. Yangang Wang provided helpful suggestion. Chengqian Li and Bingzi Dong conceived and designed the study. Chengqian Li supervised project. Shujing An and Weina Kuang contributed equally to this work.

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Correspondence to Bingzi Dong or Chengqian Li.

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This study was approved by the ethics committee of the Affiliated Hospital of Qingdao University. All procedures performed in this study involving human participants were in accordance with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The written informed consent from all the participants was obtained.

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An, S., Kuang, W., Hu, Y. et al. Association between sarcopenia and the foot-ankle function in type 2 diabetic foot ulcer. Diabetol Metab Syndr 16, 270 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13098-024-01507-5

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13098-024-01507-5

Keywords

Diabetology & Metabolic Syndrome

ISSN: 1758-5996

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