Handgrip Strength But Not Malnutrition According to Global Leadership Initiative on Malnutrition Criteria Is a Risk Factor for Mortality in Hospitalized Patients with Ischemic Diabetic Foot Ulcers

Abstract

Objective:

This study aimed to test the hypothesis that patients with malnutrition and impaired muscle function determined by hand grip strength (HGS) will have adverse outcomes.

Approach:

We conducted a prospective observational study of 77 patients admitted for ischemic diabetic foot ulcers (IDFU). Global Leadership Initiative on Malnutrition (GLIM) criteria were used to diagnose malnutrition. Values obtained with a dynamometer were dichotomized into values < and ≥ mean according to the values obtained in both sexes. The Cox proportional hazards model and the Kaplan–Meier method were applied. STROBE guidelines for cohorts were met in the present study.

Results:

In total, 55 patients (71.4%) were malnourished. Malnutrition according to GLIM criteria was not associated with adverse outcomes. HGS < mean was associated with patient age, duration of diabetes mellitus, body mass index, brachial circumference, plasma albumin, prealbumin, hemoglobin, transferrin, and HbA_1c levels. Predictive variables of mortality after applying multivariate Cox model were age >69years (hazard ratio [HR] 4.0, 95% confidence interval [CI] 1.3–12.0, p = 0.01), and HGS < mean (HR 3.7, 95% CI 1.2–11.3, p = 0.01). Survival time in patients with HGS < mean was shorter than in those with HGS ≥ mean, p < 0.01.

Innovation:

HGS is an easy and useful tool associated with nutritional parameters and with prognosis in patients admitted for IDFU.

Conclusions:

Neither malnutrition nor muscle function impairment were associated with limb loss or a need for readmission. Patients with HGS < mean presented shorter survival times. As HGS is a simple and cost-effective tool, it should be implemented as part of the nutritional admission evaluation.

Javier Aragón-Sánchez, MD, PhD

INTRODUCTION

Malnutrition is defined as a state resulting from lack of intake or uptake of nutrition that leads to altered body composition and body cell mass leading to diminished physical and mental function.¹ Malnutrition is a condition associated with longer length of hospitalization, increased susceptibility to infections, higher rates of perioperative complications, and morbimortality. It has been reported that malnutrition can be found in 20–60% of patients admitted to hospital.^2,3 Diabetes mellitus (DM) has been reported as a condition increasing the risk of malnutrition in hospitalized patients.^4,5 Thirty-nine percent of patients admitted with diabetes had high risk of malnutrition and 21.2% had malnutrition in a Spanish observational study.⁴ According to PREDYCES study in Spain, 23.7% of hospitalized patients were at risk of malnutrition; this percentage increased up to 37% in those >70 years of age.⁶ Malnutrition was diagnosed in 12.4% of a prospective cohort (GERODIAB) of type 2 diabetic patients 70 years of age and older.⁷ Using the Mini Nutritional Assessment (MNA) screening tool, up to 58% of outpatients with diabetes were at risk of malnutrition or malnourished.⁸ DM is considered a risk factor for not only malnutrition but also muscle impairment. Factors, such as diabetes-related comorbidities (heart and renal failure and neuropathy), chronic inflammation, reduced physical activity, or decline in anabolic hormones, negatively impact over muscle loss and nutritional status.⁹ Furthermore, patients with diabetic foot ulcers (DFUs) had higher rates of malnutrition and sarcopenia than patients with diabetes without this condition.¹⁰ Even though malnutrition could have a negative impact on outcomes, few studies have evaluated the nutritional status and muscle strength in patients admitted with DFUs. Nutritional status has been related to a higher risk of lower extremity amputations, worse Wagner ulcer degree, severity of infection, and worse survival rate.^11,12 However, that issue is controversial because other groups have reported that malnutrition does not affect outcomes.^13,14

Sarcopenia is considered a skeletal muscle disease associated with low muscle strength. Impairment of muscle strength is associated with frailty, disability, prolonged length of hospital stay, and increased mortality.¹⁵ Even though the literature is scarce, DM has been shown to accelerate muscle mass loss related with aging, by as much as two to four times in comparison with non-DM patients.^16,17 Hand grip strength (HGS) is the usual way to determine muscle strength and for diagnosing sarcopenia. Among older patients with DM, low grip strength was significantly associated with the development of diabetic foot disease, among other factors such as hypertension or diabetes-related peripheral neuropathy.¹⁸ Furthermore, an association between HGS and time to healing in DFUs has been reported.¹⁹ HGS can be easily tested upon the admission of the patient and could be a useful tool associated with prognosis.

CLINICAL PROBLEM ADDRESSED

The prognosis of patients requiring admission for ischemic diabetic foot ulcers (IDFU) may be associated with the type of lesion and/or general conditions. The nutritional status of the patient has an important role because it is associated with the immunological response and the healing process and could condition the outcomes of the treatment. An assessment of nutritional status and sarcopenia screening should be implemented during the admission of the patient because both parameters could be associated with prognosis.

We hypothesize that patients admitted to the vascular service for IDFU have a high prevalence of malnutrition and impaired muscle function and these conditions are associated with short-term (complications and/or limb loss during the index episode) and mid-term adverse outcomes (readmission, limb loss during follow-up and/or mortality).

MATERIALS AND METHODS

We prospectively recruited a cohort of 77 patients with DM who were admitted to the Department of Vascular Surgery at Juan Ramón Jiménez Hospital from December 2019 to November 2020. Inclusion criteria were patients previously diagnosed with DM and IDFU as the main diagnosis for admission. Exclusion criteria were patients younger than 18 years of age, pregnant patients, patients with neurological and/or cognitive disorders that could interfere in muscle evaluation, with active cancer or on immunosuppressive treatments, and patients who did not agree to be included in the study. DM duration and its treatment, age at admission, surgical treatment of peripheral arterial disease (PAD), history of DFU and lower limb amputations, and chronic complications such as stroke, coronary artery disease, and diabetic neuropathy were obtained from the medical records. Chronic kidney disease was determined at admission and was defined as an estimated glomerular filtration rate (eGFR) <60 mL/min/1.73 m² and/or the presence of albuminuria in more than two consecutive urinary analyses for at least 3 months.

PAD was diagnosed at the discretion of vascular surgeons based on a clinical evaluation, noninvasive methods, and angiography when indicated. Virtually every patient was admitted to the vascular department diagnosed with PAD. Neuropathy was evaluated by the Semmes–Weinstein monofilament test, pinprick test, sensory testing evaluation temperature changes, and vibration perception threshold (using the C-64 quantitative tuning fork). If any of those tests were altered, peripheral neuropathy diagnosis was stated.

Nutritional evaluation was carried out during the first 48 h after admission. The physical evaluation included height, weight, and body max index (BMI). Unintentional or unplanned weight loss >5% in the last 3–6 months or >10% beyond 6 months was collected in research database. In patients who were unable to stand, the knee height was used to estimate their height using Chumlea's equation.²⁰ The knee height as well as brachial circumference (BC) were also used for estimating weight when needed.

Malnutrition diagnosis was held according to the two-step model recommended in the Global Leadership Initiative on Malnutrition (GLIM) criteria.²¹ According to GLIM criteria for diagnosing malnutrition, the presence of at least one phenotypic criteria is necessary (nonvolitional weight loss, low body mass index, or reduced muscle mass) along with one etiologic criteria (reduced food intake/assimilation or inflammation/disease burden).²¹ GLIM criteria allow for the classification of patients according to the degree of malnutrition (moderate or severe). For the purpose of the present study, moderate and severe malnutrition were combined as a unique variable, that is, “malnutrition.”

HGS was evaluated with the Jamar^© hydraulic hand dynamometer (Sammons Preston; Rolyon, Bolingbrook, IL). Patients were instructed to squeeze the dynamometer with the dominant hand, in a seated position and with their elbow flexed at 90°. Three measurements per patient were obtained with 1 min of rest between measurements, and the mean value was calculated.

Venous blood samples were obtained after a 12-h fast to determine plasma glucose, creatinine, eGFR, protein, albumin, pre-albumin, HbA_1c, and vitamins. Urinary tests were also analyzed to evaluate albuminuria and the albumin/creatinine ratio. Electronic laboratory notebook was not used.

Complications were defined as any unexpected event (metabolic, infectious, cardiologic, or other type), which was the cause of prolonged hospital stay and/or modified the planned treatment and/or modified the medical status of the patient.

The medical history of every patient was checked monthly after hospital discharge. We analyzed the duration of hospitalization and complications during admission. In addition, the number and type of amputations defined as minor (distal to ankle joint) or major (through or above the ankle joint) were recorded.

Adverse outcomes were defined as follows: more than two complications during the index episode, need for readmission, and limb loss (major amputation) during the index episode or during follow-up and overall.

Statistical methods

Sample size was determined considering the discharges from our hospital codified with diabetic foot as the main diagnosis. A 3% precision with 95% confidence intervals (CIs) bilateral based on the normal distribution of the sample was stated, while assuming a 60% expected rate of malnutrition in an overall population of 82 people. The resultant sample size was 76 patients. Normal distribution was analyzed using the Kolmogorov–Smirnov test. The mean and standard deviation (SD) in normally distributed variables and median and first and third quartiles in non-normally distributed variables were used for descriptive purposes. Student's t-tests and nonparametric Mann–Whitney tests were carried out to compare groups. We analyzed independence between discrete variables by the χ² test and Fisher's exact test when indicated. We calculated the HGS mean values among men and women and then dichotomized the cohort in patients with HGS <and ≥ mean according to the mean obtained by sex. Patient data were censored on February 20, 2021 when the status of the patient, dead or alive, was verified in clinical records. Univariate analysis between survivors versus those who died was carried out. Age was dichotomized according to > or ≤ mean value. Statistically significant variables were included in a Cox proportional hazards model for time to death and hazard ratios (HRs) were estimated. Survival times were plotted using the Kaplan–Meier method and were calculated from the date of index admission to death or the end of the study. The median survival time was calculated with a 95% CI. The Kaplan–Meier method was adjusted by statistically significant variables in the univariate analysis between survivors versus those who died. The stratified log-rank test was used to determine differences across patients with HGS < and ≥ mean. Statistical analysis was performed with SPSS version 20 for macOS (SPSS, Inc., Chicago, IL), and a p-value <0.05 (two-tailed) was set as the threshold for statistical significance.

The present study was conducted following the Declaration of Helsinki guidelines as revised in 2013. Every patient provided written informed consent to enter in this study, which was approved by the Ethics Committee of Juan Ramón Jiménez Hospital (Huelva, Spain) with the number PI 010/20.

The STROBE guidelines for cohorts were met in the present study.

RESULTS

Most patients were men (74%) and had DM2 (96.1%). Mean age was 69.6 years of age. Mean duration of DM was 21 years (SD 10.5). Forty patients (51.9%) had undergone previous amputations and 35.1% had undergone a previous vascular surgery.

According to GLIM criteria, 55 patients (71.4%) were malnourished. The mean age of the malnourished patients was 72.0 (SD 10.3) versus 63.5 (SD 12.2) in patients without malnutrition (p < 0.01). Mean BMI was 26.8 kg/m² (SD 4.8) in malnourished patients and 30.2 kg/m² (SD 6.8) in nonmalnourished patients (p = 0.01). No difference in terms of sex and diabetes duration was found between patients with and without malnutrition. Comorbidities were detected as follows: history of cardiac infarction (n = 31, 40.3%), history of stroke (n = 18, 23.4%), peripheral neuropathy (n = 36, 46.8%), retinopathy (n = 57, 78.1%), and hemodialysis (n = 11, 14.3%). We did not find any association of these comorbidities with malnutrition.

The mean value of HGS in both sexes was 17.7 (SD 8.4) and 46 patients (59.7%) had values under this cutoff. Men had a mean HGS of 19.9 kg (SD 8.3) and women of 11.2 kg (SD 4.3), p < 0.01. Forty-one patients (53.2%), 31 men and 10 women, had HGS values < mean.

Patient characteristics according to HGS above/below mean value is summarized in Table 1.

Table 1.

Patient characteristics according to hand grip strength above/below mean value (univariate analysis)

	HGS < mean	HGS ≥ mean	p
Age, years	73.7 (SD 9.5)	64.8 (SD 11.8)	<0.01
Duration of DM, years	21.9 (SD 10.2)	20 (SD 10.9)	0.43
Mean BMI, kg/m²	26.3 (SD 4.3)	29.4 (SD 6.4)	0.01
Brachial circumference, cm	27.9 (SD 3.9)	30.9 (SD 5.9)	0.01

BMI, body mass index; DM, diabetes mellitus; HGS, hand grip strength; SD, standard deviation.

Peripheral neuropathy was diagnosed in 36 patients (46.8%) and was associated neither with malnutrition nor HGS < mean. We did not find any association of comorbidities with HGS<mean.

Laboratory values related to malnutrition and dynamometry are shown in Table 2.

Table 2.

Laboratory values regarding the presence of malnutrition and grip strength (univariate analysis)

	Malnutrition (GLIM)		p	HGS < mean
	No	Yes	p	No	Yes	p
Albumin, g/dL, mean (SD)	3.6 (0.5)	3.3 (0.5)	0.05	3.6 (0.4)	3.2 (0.5)	<0.01
Prealbumin, mg/dL, mean (SD)	20.1 (7.1)	17.1 (6.8)	0.09	19.9 (6.5)	16.2 (7.0)	<0.01
Total proteins, g/dL, mean (SD)	6.7 (0.5)	6.3 (0.6)	<0.01	6.5 (0.5)	6.3 (0.7)	0.15
Hemoglobin, g/dL, mean (SD)	11.9 (1.9)	11.1 (1.9)	0.12	11.8 (1.9)	10.9 (1.8)	0.03
Transferrin, mg/dL, mean (SD)	191.4 (64.5)	170.1 (47.0)	0.11	199.6 (51.2)	155.6 (46.2)	<0.01
Ferritin, ng/mL, mean (SD)	424.4 (584.7)	412.3 (459.9)	0.92	306.1 (398.0)	511.7 (551.8)	0.06
HbA_1c, %, mean (SD)	7.9 (1.6)	7.5 (1.4)	0.26	8.1 (1.5)	7.2 (1.3)	0.01
Vitamin B12, pg/mL, mean (SD)	389.4 (181.7)	455.1 (220.6)	0.23	365.7 (151.2)	497.1 (236.9)	<0.01
eGFR, mL/min/1.73 m², mean (SD)	76.3 (28.8)	63.4 (36.7)	0.17	73.3 (32.3)	60.5 (36.8)	0.13
eGFR <60 mL/min/1.73 m², n (%)	7 (31.8)	27 (49.1)	0.16	9 (29)	25 (54.3)	0.02
Folic acid, ng/mL, mean (SD)	6.9 (5.3)	7.0 (5.8)	0.92	6.1 (3.6)	7.7 (6.8)	0.21
Vitamin D, 25-hydroxy, ng/mL, mean (SD)	14.9 (7.1)	11.4 (6.8)	0.06	12.4 (6.3)	12.3 (7.8)	0.94

eGFR, estimated glomerular filtration rate; GLIM, Global Leadership Initiative on Malnutrition.

Complications were as follows: 94.8% patients had metabolic complications, 75.3% had other complications (mostly blood transfusion), infectious complications in 74%, and cardiac complications in 24.7% of patients. During the index admission, 33 patients (42.9%) had more than 2 complications.

Seven patients died during the perihospitalization period: two for hypovolemic shock, one for stroke, and four for systemic infections. Follow-up was carried out for a period of 11 months, being finished 6 months after the index admission of our last patient. No patients were lost to follow-up. During the follow-up, 38 patients (49.4%) were readmitted for IDFU and 37 patients (48.1%) had a complication during the readmission. Twenty-two patients (28.6%) suffered from 2 or more amputations and 31 underwent a major amputation (40.3%). At the end of follow-up, 24 patients (31.2%) had died. Outcomes related to malnutrition and HGS are shown in Table 3. Several values related to malnutrition were significantly lower in patients with HGS < mean. Plasma albumin mean was 3.2 g/dL (SD 0.7) in patients who died versus 3.5 g/dL (SD 0.4) in the survivors (p = 0.01).

Table 3.

Outcomes regarding the presence of malnutrition and grip strength (univariate analysis)

	Malnutrition (GLIM)		p	HGS < mean		p
	No	Yes	p	No	Yes	p
Hospital stay in days, mean (SD)	16.4 (12.6)	12.7 (7.2)	0.26	19.2 (14.3)	18.1 (7.2)	0.67
>2 complications during index admission, n (%)	8 (36.4)	25 (45.5)	0.46	10 (27.8)	23 (56.1)	0.01
Readmission, n (%)	11 (50)	27 (49.1)	0.94	19 (52.8)	19 (46.3)	0.57
Limb loss, n (%)	8 (36.4)	23 (41.8)	0.65	12 (33.3)	19 (46.3)	0.24
Overall mortality, n (%)	7 (31.8)	17 (30.9)	0.93	4 (11.1)	20 (48.8)	<0.01

Univariate analysis between survivors and patients was as follows. Age >69 years (p < 0.01), albumin values (p = 0.01), HGS < mean (p < 0.01), eGFR <60 mL/min/1.73 m² (p = 0.02), and cardiac infarction before index admission (p = 0.03). Predictive variables of mortality after applying multivariate Cox model were age >69 years (HR 4.0, 95% CI 1.3–12.0, p = 0.01), and HGS < mean (HR 3.7, 95% CI 1.2–11.3, p = 0.01).

The Kaplan–Meier survival time curve was plotted (Fig. 1). Global survival mean time was 47.1 weeks (SD 2.6, 95% CI 41.9–52.4). The mean survival time in patients with HGS < mean was 38.7 weeks (SD 4.0, 95% CI 30.8–46.7) and 55.7 weeks (SD 2.4, 95% CI 55.7–61.7) for those with HGS ≥ mean. Log-rank (Mantel–Cox) test between the two groups was χ² = 11.5 (p < 0.01). The log-rank test was significant with p < 0.01 after adjusting by eGFR <60 mL/min/1.73 m², cardiac infarction, age>mean, and albumin.

Figure 1.

Kaplan–Meier survival curve regarding HGS. HGS, hand grip strength.

DISCUSSION

We found that 71.4% of patients requiring admission for IDFU have malnutrition. However, malnutrition was not associated with adverse outcomes. On the other hand, 53.2% of the patients had HGS values below the mean, which was associated with nutritional impairment and mortality.

A previous study evaluated nutritional status with Geriatric Nutritional Risk Index (GNRI) and MNA in patients with DFU.¹¹ Malnutrition was detected in 14.6% of patients and both screening tools were predictors of amputations. Other authors detected malnutrition with the Subjective Global Assessment (SGA) in 62% patients with DFU and malnutrition was associated to poor outcomes.¹² Actually, 69% of malnourished patients had not healed in 6 months versus 17% of those without malnutrition. Furthermore, the authors reported that only a small proportion of patients with mild and moderate infections were malnourished versus 43.2% of patients with severe infections who were severely malnourished. Other authors reported that GNRI was a predictive factor of mortality (26.6% died) in patients with DFU undergoing amputations.²² Unlike the aforementioned studies, we used GLIM criteria for diagnosing malnutrition. Another study using GLIM criteria found that malnutrition was present in 23.6% of their patients and was associated with the severity of ulcers but not with outcomes.¹³ It is remarkable how series using GNRI and SGA found an association between malnutrition and outcomes, unlike series using GLIM criteria. We think that this is related to the fact that GLIM does not include albumin values as a criterion, unlike GNRI and SGA. Lower values of plasma albumin were found in patients with HGS < mean in the present study. Furthermore, lower levels of plasma albumin were found in patients who died, although this finding was not significant in the multivariate model. Lower levels of albumin were found in patients who underwent amputations versus a conservative approach in one study.²³ Serum albumin <2.8 g/dL was found to be a risk factor of treatment failure in cases of diabetic foot osteomyelitis.²⁴ Mortality has also been associated with low levels of plasma albumin in patients with DFU.²⁵ Furthermore, supplementation with arginine, glutamine, and β-hydroxy-β-methylbutyrate could improve healing in patients with DFU and serum albumin <4 g/dL.²⁶ Therefore, GLIM criteria might not be useful to evaluate malnutrition in patients with DFU and it would be better to use GNRI or SGA criteria, which has a prognostic value.

Loss of HGS is strongly related to disability, morbidity, and mortality.²⁷ Low muscle strength has been related to worse glycemic control and insulin resistance.²⁸ However, the optimal cutoff point for a dynamometer should be obtained from different populations with a study designed for such an aim.²⁸ Low muscle strength detected by hand grip is a primary parameter of sarcopenia. Currently, according to the Revised European Working Group on Sarcopenia in Older People (EWGSOP II), the cutoff value of HGS is 27 kg for men and 16 kg for women.²⁷ The mean in our patients was lower than these cutoffs. The mean obtained in the present study was indeed associated with relevant variables. HGS < mean was associated with patient age, duration of DM, and laboratory parameters like plasma albumin, prealbumin, hemoglobin, transferrin, and HbA_1c levels. HGS < mean was also associated with BMI and BC. These associations could establish the role of this simple test as a tool for diagnosing malnutrition. Low HGS has recently been reported as a risk factor associated with diabetic foot disease together with hypertension and peripheral neuropathy.¹⁸ A prospective study, including patients with DFU reported an association of HGS with time to healing, but not with mortality.¹⁹ We have demonstrated the usefulness of HGS as a predictor for mortality in patients with IDFU. One study reported that sarcopenia was a predictive factor of overall mortality in patients with critical limb ischemia.²⁹ However, just 46.8% of patients had DM and the authors used computed tomography (CT) scans to define sarcopenia.²⁹ Not only mortality should be taken into account when dealing with treatment of patients with IDFU. Functional ambulatory status is a relevant outcome in the treatment of these patients. Khan et al. have proposed a score grading patient's mobility, in adjunction with WIfI system as clinical decision-making tools.³⁰ It seems mandatory to include functional ambulatory evaluation in patients with IDFU. The relationship between functional ambulatory status and muscle strength determined by HGS should be explored. Furthermore, one valuable tool to identify patients with sarcopenia is SARC-F questionnaire.³¹ This is composed of five questions, being a score ≥4 suggestive of sarcopenia. Adding HGS to this screening test could be useful to predict mortality and functional status after treatment of IDFU. Sarcopenia has also been associated with the risk of cardiovascular events in patients with critical limb ischemia in a cohort including 43.8% of patients with DM.²⁹

Our study has limitations. First, we did not classify DFU according to the WIfI classification. We could not assess the influence of infection, location of the ulcer, and degrees of ischemia on the adverse outcomes. It would have been interesting to establish a relationship between HGS and the type of lesion. Second, we have provided information about DFU patients admitted for vascular surgery. This is a bias and the association of HGS and nonischemic DFU could not be evaluated, giving incomplete view of the problem. The type of vascular intervention was not recorded in the research database and it could not be evaluated. Third, the number of women included in this study is lower than that of men, which could limit the statistical power of the study. Fourth, serial determinations of HGS were not carried out during follow-up. Fifth, sarcopenia was not evaluated by magnetic resonance imaging or CT. Finally, the small size of the sample may limit the statistical power of the results.

Our study also has some strengths. The present study was conducted in a prospective manner and every patient was evaluated by an endocrinologist with expertise in nutrition. Furthermore, no patients were lost to follow-up.

INNOVATION

In this selected group of patients with DFU requiring admission in a vascular department, we found that malnutrition was very common, although it was not associated with limb loss, longer hospital stay, or complications. HGS determined by a dynamometer is a quick, easy, and cost-effective tool for predicting mortality in hospitalized patients with IDFU. More research is needed to evaluate whether improvements in grip strength by nutritional support and other interventions could reduce adverse outcomes.

KEY FINDINGS

GLIM criteria for diagnosing malnutrition in patients with IDFU is not associated with prognosis.

Other scores like GNRI or SGA could be more useful to diagnose malnutrition in patients with IDFU and could have a prognostic value.

Mortality but not limb loss is associated with lower values of HGS than those used for diagnosing sarcopenia. Detection of impaired muscle function associated with sarcopenia should be performed at the initial evaluation of patients with IDFU.

Footnotes

AUTHORs' CONTRIBUTIONS

M.E.L.-V. had the concept idea for studying the prevalence of malnutrition in her patients. She designed the clinical database used in this study, collected data, and analyzed the data. J.A.-S. designed the clinical database, prepared date for analyzing, performed the statistical analysis, and wrote the article. G.V.-M. edited and contributed to the writing of the article, especially, the discussion, and reviewing the English language.

ACKNOWLEDGMENTS AND FUNDING SOURCES

None declared. No funding was received for this article.

AUTHOR DISCLOSURE AND GHOSTWRITING

The authors declare that there is no conflict of interest. No ghostwriter was used for the preparation of this article.

ABOUT THE AUTHORS

Dr. María Eugenia López-Valverde, MD, is an Endocrinologist interested in the epidemiology, prevention, and management of diabetic foot ulcers and amputations. She is interested in malnutrition in patients with foot ulcers and epidemiology of lower extremity amputations and its associated mortality. Dr. Javier Aragón-Sánchez, MD, PhD, is a General Surgeon. He is the Medical Director and the Chief of the Department of Surgery and Diabetic Foot Unit of La Paloma Hospital in Las Palmas de Gran Canaria (Spain). He is the author of three textbooks, more than 22 chapters, and more than 100 peer-reviewed articles and several monographs, especially dealing with diabetic foot infections and osteomyelitis. He is a member of the Board of the IWGDF infections. Dr. Gerardo Víquez-Molina is the Chief of the Diabetic Foot Unit at San Juan de Dios Hospital in San José de Costa Rica, Costa Rica. His main research fields are diabetic foot infections and osteomyelitis.

SUPPLEMENTARY MATERIAL

STROBE Statement

Abbreviations and Acronyms

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