Diabetes & Metabolic Syndrome: Clinical Research & Reviews 11S (2017) S583–S587

Contents lists available at ScienceDirect

Diabetes & Metabolic Syndrome: Clinical Research &

Reviews
journal homepage: www.elsevier.com/locate/dsx

Original Article

Diabetic foot ulcer carries high amputation and mortality rates,

particularly in the presence of advanced age, peripheral artery disease
and anemia
Rafael Henrique Rodrigues Costaa , Natália Anício Cardosob , Ricardo Jayme Procópioc ,
Túlio Pinho Navarrod , Alan Dardike , Ligia de Loiola Cisnerosf,*
a
University Hospital, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
b
Post-Graduate Program for Surgery and Ophthalmology, Faculty of Medicine, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
c
Endovascular Unit of University Hospital, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
d
Faculty of Medicine, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
e
Department of Surgery, Yale School of Medicine, New Haven, CT, USA
f
Department of Physiotherapy, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil

A R T I C L E I N F O A B S T R A C T

Introduction: Foot ulcer is also a clinical marker for limb amputation and for death in diabetic patients.
Keywords: The purpose of this study was to determine amputation and mortality rates and its associated factors in
Diabetic foot
patients with diabetic foot ulcerations in a tertiary hospital in Brazil.
Foot ulcer
Amputation
Methods: Retrospective medical records from 654 diabetic foot patients were reviewed. The risk factors
Death were determined using the conditional logistic regression model analysis.
Results: The mean patient age was 63.1 years (SD 12.20). Peripheral arterial disease was present in 160
patients (24.5%). Major amputations were performed in 135 (21%). The in-hospital mortality rate was 12%
and the mortality rate of the amputees was 22.2%. The lowest hemoglobin level, the median value was
9.50 g/dL, (4.0–17.0). Anemia was detected in 89.6% of patients submitted to amputation and in 82,1% of
those who died. Hemoglobin <11 g/dL was the most significant risk factor for major amputation (odds
ratio 5.57, p < 0.0001). The presence of peripheral arterial disease and old age were also a risk for major
amputation (odds ratio 1.84, p = 0.007 and 1.02, p = 0.028, respectively). Factors associated with increased
risk for death were hemoglobin <11 g/dL (odds ratio 4.04, p < 0.001), major amputation (1.79, p = 0.03)
and old age (1.05, p < 0,001).
Conclusions: Diabetic foot ulcer is associated with high amputation and mortality rates. Old age,
peripheral arterial disease and low hemoglobin level are risk factor for major amputation. Old age, major
amputation and low hemoglobin level are risk factors for death.
© 2017 Published by Elsevier Ltd on behalf of Diabetes India.

1. Introduction hospitalization in diabetic patients, are among the most common,

serious and costly complications of diabetes mellitus, resulting in
The impact of the global diabetes burden is evidenced by the major medical, financial, and social consequences for patients,
growing morbidity and mortality rates, and by permanent their families and society in general [3,4]. Foot ulcer is also a
disabilities such as blindness, diabetic retinopathy, end-stage clinical marker for limb amputation and for death in these patients
renal failure and lower extremity amputations [1]. The diabetic [5,6].
foot is one of the major complications of this disease, with an The etiology of diabetic foot ulcers is complex and risk factors
estimated 10% to 25% of diabetic patients developing a diabetic foot include peripheral vascular disease, peripheral neuropathy, foot
ulcer in their lifetimes [2]. Foot ulcers, the leading cause of deformities and local foot trauma [7]. The coexistence of
neuropathy, ischemia and immunosuppression in diabetic
patients, favors development of severe ascending infections
* Corresponding author at: Universidade Federal de Minas Gerais EEFFTO, Av
emanating from the ulcer and is associated with a poor prognosis
Antonio Carlos 6627, Pampulha, Belo Horizonte, Minas Gerais, Brazil. as these infections frequently lead to amputation and even death
E-mail address: ligialoyola@gmail.com (L. de Loiola Cisneros). [8]. In the literature, the amputation rates associated with diabetic

http://dx.doi.org/10.1016/j.dsx.2017.04.008
1871-4021/© 2017 Published by Elsevier Ltd on behalf of Diabetes India.
S584 R.H.R. Costa et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 11S (2017) S583–S587

foot disease range from 4.7 in Germany [9] to 47.7% in a study This study was approved by the Federal University of Minas
carried out in Brazil [10]. The in-hospital mortality rate from Gerais Ethics Committee (ETIC number 15638113.5.0000.5149).
diabetic foot ulcer can reach 40,5% in a prospective study
conducted in Nigeria11. 3. Results
Therefore, the early recognition and management of risk factors
for foot complications may prevent amputations and deaths [12]. Demographic and clinical characteristics of 654 consecutive
The present study was undertaken to determine amputation and patients with diabetic foot ulcers are summarized in Table 1. The
mortality rates and its associated factors in patients with diabetic mean patient age was 63.1 years (SD 12.20), 441 (67%) were male.
foot ulcerations in a tertiary hospital in Brazil. The most common co-morbidities were hypertension (60.55%) and
active smoking (32.72%). Peripheral arterial disease was present in
2. Methods 160 patients (24.5%). The mean ABI was 0.41, with the majority of
ischemic patients having an ABI lower than 0.4. On the other hand,
This retrospective study was conducted in the Vascular Surgery only eleven subjects had incompressible ABIs, as shown in Table 1.
Unit of Hospital Risoleta Toletino Neves, a tertiary university In the amputees subgroup the mean ABI was 0.33, and within the
hospital in Belo Horizonte, Brazil. The records of 654 consecutive patients that eventually died the median was 0.42; there was no
patients admitted to the vascular surgery service with diabetic foot statistically difference between these groups. The median serum
lesions between January 2007 and December 2012 were reviewed. level of the highest creatinine during any admission was 1.29 mg/
All patients presented with deep ulceration, gangrene, infection dL (range 0.47-11.73). For the lowest hemoglobin level, the median
and/or deep tissue injury in the foot below the ankle, e.g. Wagner value was 9.50 g/dL, ranging from 4.0 to 17.0.
wound classification equal or greater than 3. All patients had From the total sample, 487 participants (74%) required only a
diabetes and neuropathy, independent of the presence or absence single surgical procedure. Eighty patients (12%) required two
of peripheral arterial disease (PAD), and were classified according procedures, while 24 patients (4%) required three procedures and
to the International Consensus on the Diabetic Foot and Practical less than 2% required four or more procedures (Fig. 1). Fifty-five
Guidelines [13]. patients (8%) were treated with conservative management of
Data recorded included age, sex, smoking status and comor- antibiotics and wound care without any intervention.
bidities such as hypertension and PAD. An admission ankle- Revascularization via conventional bypass and/or endovascular
brachial index (ABI)  0.9 was considered as presence of PAD [14]. therapy were performed in 150 patients (23%).
Serum lower hemoglobin and higher creatinine levels during the Amputations were performed in 449 patients (69%). 314 (48%)
admission, number of previous surgical procedures, level of lower were minor amputations (214 toe amputation and 100 trans-
limb amputation, intra-hospital mortality and number of read- metatarsal) and 135 (21%) were major amputation (56 below the
missions were also collected. Lower limb amputation above the knee, 75 above the knee and 4 hip disarticulation). The overall limb
ankle was considered as major amputation. Digit, ray and salvage rate was 79%. The mortality rate of the amputees was
transmetatarsal were considered as minor amputations. 22.2%.
Analyses were carried out using the Statistical Package for the Sixty-one percent of the patients were admitted only once,
Social Science (SPSS) 17.0 Windows version (SPSS Inc., Chicago, IL, while 134 patients (20%) had to be readmitted only once, and 124
USA). Descriptive analysis was done for demographic character- patients (19%) were readmitted twice or more times. The total rate
istics. Categorical data were analyzed using the chi-squared (x2) of readmissions at the same hospital was 39% through the period of
test. Continuous data were expressed as means and standard the study.
deviation, and were analyzed using Student’s t-test. Predictors of The in-hospital mortality rate was 12%. Analysis of mortality
lower limb amputation and death were determined using rate by age (Table 3), showed an increase of mortality as the groups
conditional logistic regression. Multivariable analysis was per- got older. For patients younger than 30 years, there was no death.
formed by including variables selected through univariable The mortality rate for patients with 31 to 60 years was 6.1%, with 61
analysis (p < 0.10) that were eliminated with backward selection. to 80 years was 13.4%, and older than 80 years was 38.1%.

Table 1
Demographics, comorbidities, creatinine serum level, hemoglobin serum level and number of surgical procedures.

General (%) (n = 654) Amputees (n = 135)a Deceased (n = 78)

Age, mean (SD) 63.08 (12.19) 65.97 (12.17) 70.04 (10.77)
Sex (male) n (%) 441 (67.4) 91 (67.4) 48 (61.5)
Hypertension n (%) 258 (39.4) 73 (54.7) 42 (53.8)
Active Smoking n (%) 214 (32.7) 43 (31.8) 24 (30.7)
PAD n (%) 160 (24.5) 50 (37.0) 23 (29.4)

ABIb
<0.4 63 (43) 26 (52) 10 (43.5)
0.4–0.59 53 (33) 12 (24) 8 (34.8)
0.6–0.9 28 (17) 6 (12) 4 (17.4)
Incompressible 11 (7) 6 (12) 1 (4.3)
Highest serum creatinine, median (min-max)c 1.29 (0.47–11.73) 1.34 (0.47–9.39) 1.40 (0.54–11.73)
Lowest serum hemoglobin, median (min-max)c 9.50 (4.0–17.0) 7.50 (4.1–14.0) 7.05 (4.1–16.2)
Number of surgical procedures per patient, mean (SD) 1.15 (0.69) 1.32 (0.76) 1.04 (0.74)
Amputation n (%) 135 (20.6) 135 (100) 30 (38.4)
Mortality n (%) 78 (11.9) 30 (22.2) 78 (100)

SD = Standard deviation PAD = Peripheral arterial disease ABI = Ankle-brachial index.

a
Amputees: patients who underwent major amputation.
b
n = 155.
c
n = 629
 R.H.R. Costa et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 11S (2017) S583–S587 S585

[15]. In Brazil, amputation rate may be as high as 47.7% [10]. In

600 Guiana, close to Brazil, prior to the development of a structured
487 national program for diabetic patients, the amputation rate was
500
42%. After the implementation of the program, it was lowered in
two thirds [16]. In Portugal, the outpatient amputation rate
400
reported was 5.8%, but we can assume that as outpatients, they had
less severe disease [6]. In Germany, the amputation rate ranged
300
from 4.7% inside a structured health program to 21.7% outside the
200
program [9]. Amputation rates of 42.3% were also surprisingly
found in the US (NYC) in a series in three hospitals (private, public
100 80 and VA), with the lowest rate in private hospital and the highest
55
24 rate at the VA [17]. In Turkey, the amputation rate found was 36.7%
4 4
0 [18]. In papers that included only diabetic foot infections, the major
No surgery 1 2 3 4 5 amputation rate ranged from 19.9% to 39% [19–22]. Lavery et al.,
2009 [23], estimated that the risk of amputation increases 154
Fig. 1. Number of procedures per patient. times with the infection of a diabetic foot ulcer. Therefore,
considering that we have no structured health system and that our
Thirty-six percent of the patients (n = 234) were discharged diabetic patients had deep infected foot ulcers (Wagner  3), a
home in good conditions. Forty-seven percent of the patients major amputation rate of 21% is quite acceptable, once we had 79%
required special home care after discharge, including the need for limb salvage rate.
parenteral antibiotics, wound care, and/or physical rehabilitation. In-hospital mortality was 12% in the present study. This rate
The association of amputation and mortality rates with age and was higher in the subgroup of patients submitted to major
serum hemoglobin level is shown in Table 2. Anemia, meaning amputation (22,2%), showing that major amputation is related to
hemoglobin level <11 g/dL was detected in 89.6% of patients mortality. Probably, the patients requiring major amputation may
submitted to amputation and in 82,1% of those who died. Risk have more severe infection, more tissue loss and less systemic
factors that predicted major amputation are shown in Table 3. organ functional reserve. Similar results were also found in another
Univariable analysis showed that hemoglobin <11 g/dL was the area of Brazil [10]. It is in accordance to the literature, which shows
most significant risk factor for major amputation (odds ratio 5.93, results ranging from 8.4% to 17% for diabetic patients with foot
p < 0.0001). This relationship was also confirmed by multivariable ulcers [10,15,22,24,25]. The main causes of death were cardiovas-
logistic regression. The presence of peripheral arterial disease and cular events and septicemia [26].
old age were also a risk for major amputation. In our sample, the mean age was 63 years, similar to other
Factors associated with increased risk for death were hemo- studies where the age ranged from a mean of 56.1 to 76.0 years
globin <11 g/dL, old age and major amputation, as confirmed by [11,19,20,22,24,25,27–29]. Ageing has been considered as a
both univariate and multivariable logistic regression (Table 4). potential predictor for lower limb amputation in diabetic patients
presenting foot ulcers [29,30] and an establish risk factor for in-
4. Discussion hospital mortality [24,29]. This old aged people usually have more
peripheral neuropathy, progressive atherosclerosis with PAD,
Our findings showed high rates of amputation and mortality carotid and coronary artery disease, and chronic renal failure
related to diabetic foot ulcers. Old age, peripheral arterial disease [24,30,31].
(ABI  0.9) and an hemoglobin level lower than 11 g/dL were PAD is an independent risk factor for subsequent ulceration and
independent predictors for major amputation. Old age, major limb loss in diabetic patient. In our study, the prevalence of PAD
amputation during any admission and hemoglobin lower than was 25.1%. In the literature, this prevalence ranged from 8% to 56%
11 g/dL were identified as risk factors for death. [27,28,32,33]. A consensus of the Italian societies of diabetes
The major amputation rate was 21% in the studied sample. In reports a prevalence up to 50% of subjects with diabetic foot ulcer
the literature, there is a wide range of amputation rates due to the [31]. In our study, patients with PAD had 2.28 times higher risk for
heterogeneity of patients sample, if they were treated as limb loss. Won at al [32], in a retrospective study with 173 subjects,
outpatients or in hospital, if patients had diabetic foot ulcers or found a 2.64 times increased risk of limb loss in diabetic patients
diabetic foot infections and if the area have or not a structured with PAD. In addition, other authors have found similar results
health program. Sereday et al., in a study over 11 hospitals of [21,23,29–31,34]. This important relation between PAD and major
different regions of Argentina found a major amputation rate of amputation reinforces the importance of vascular assessment and
32,5% in diabetic patients. Infection was the most frequent treatment for diabetic foot patients, focused on evidence-based
immediate cause of amputation and PAD the underlying cause strategies to promote healing and preserve life and limb.
In this study, we identified the association of lower hemoglobin
levels with worse outcomes. More than 80% of patients who
Table 2 underwent major amputation and those who died had hemoglobin
Amputation and mortality rates according with age and serum hemoglobin level.
levels <11 g/dL, indicating anemia. The high prevalence of anemia
Variable Major amputation rate n (%) Mortality rate n (%) is well recognized in patients with diabetes and is a common
Age problem related to adverse outcomes in diabetic foot ulcer patients
Younger than 30 years 0 (0) 0 (0) [11,35–38]. An inverse correlation was found between hemoglobin
31–60 years 40 (15.4) 16 (6.2) level and diabetic foot disease progression in the study of Richards
61–80 years 79 (22.7) 46 (13.2)
et al., [39]. Desormais et al., [40], found a risk 1.44 higher for
Older than 80 years 16 (38.1) 16 (38.1)
amputation and death in patients with anemia. It is probably due to
Serum Hemoglobin Level diminished delivery of oxygen to the tissues and the impairment in
<11 g/dL 121 (89.60) 64 (82.10) the compensatory response to reduced circulating hemoglobin
11 g/dL 14 (10.40) 14 (17.90) levels found in patients with diabetes [39], leading to impairment
in healing and poor infection control. Kengne et al., in an
S586 R.H.R. Costa et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 11S (2017) S583–S587

Table 3
Risk Factors associated with major amputation.

Univariate Analysis Multivariate Analysis

OR 95% CI p-value* OR 95% CI p-value

Age, per year 1.026 1.009–1.043 0.002** 1.020 1.002–1.038 0.028
Gender, Male 1.001 0.669–1.500 0.995
Hypertension 0.714 0.488–1.047 0.085 0.667 0.445–1.002 0.051
Active Smoking 0.951 0.634– 1.427 0.809
PAD 2.187 1.455–3.289 <0.0001 1.841 1.183–2.866 0.007
Multiple surgical procedures (3 or more) 2.104 0.988–4.478 0.054 1.480 0.675–3.245 0.328
Multiple Readmissions (2 or more) 0.964 0.593–1.568 0.883
Creatinine >1.8md/dL 0.989 0.642–1.524 0.960
Hemoglobin <11 g/dL 5.936 3.118–11.299 <0.0001 5.574 2.906–10.691 <0.0001

PAD = Peripheral arterial disease.

Table 4
Risk Factors associated with mortality.

Univariate Analysis Multivariate Analysis

OR 95% CI p-value* OR 95% CI p-value

Age, per year 1.061 1.038–1.085 <0.0001** 1.059 1.034–1.084 <0.0001
Gender, Male 1.342 0.823–2.188 0.238
Hypertension 0.732 0.455–1.177 0.198
Active Smoking 0.903 0.542–1.506 0.695
PAD 1.340 0.794–2.261 0.273
Multiple surgical procedures (3 or more) 0.754 0.224–2.538 0.649
Multiple Readmissions (2 or more) 1.565 0.902–2.715 0.111
Creatinine >1.8md/dL 1.166 0.694–1.957 0.562
Hemoglobin <11 g/dL 4.643 2.092–10.308 <0.0001 4.046 1.776–9.215 <0.0001
Major Amputation 2.804 1.696–4.635 <0.0001 1.797 1.046–3.086 0.034

PAD = Peripheral arterial disease OR = Odds Ratio CI = Confidence interval.

epidemiological study, demonstrated that presence of diabetes, this high readmittance rate was not associated with higher
anemia and cardiovascular disease doubled the absolute risk of amputation and mortality rates, it is important to highlight that
mortality [35]. These results reinforce diabetic patients must be it increases morbidity to the patient and is associated with a higher
routinely screened and treated for anemia. Considering multiple burden.
factors contribute to the presence of anemia in these patients as This study has some limitations. First, missing data was
nutrition and diet, drug therapy, systemic inflammation, renal inevitable considering the fact that it was a retrospective study
disease, peripheral arterial disease and cardiovascular disease, a and the data were extracted from the patients’ medical records.
specific protocol treatment of anemia in these patients could Second, other variables, such as type of revascularization (if open
potentially reduce the high rate of these devastating events. surgery or endovascular) and C reactive protein serum levels,
Although a question exists with regard to the benefits of treatment were not collected because they were not of interest at the
of anemia in diabetic foot patients. beginning of the studied period. In addition, there was lack of
The presence of hypertension and/or active smoking was not information in the medical records regarding relevant aspects such
associated with lower limb amputation or death in this diabetic as heart status, respiratory and previous functional deficit as
population. Our prevalence of systemic hypertension was 60,5% deambulation and measures of patient’s quality of life.
and 32,7% of the subjects were active smokers. There is a wide Therefore, we are in need of an aggressive approach to such
range in prevalence of these conditions in diabetic patients with patients who are referred late in the course of the disease to our
foot lesions. For hypertension, prevalence of 48% to 91% was found, hospital. Based on the data collected and identification of ours
and the proportion of active smokers ranged from 20 to 49% patients profile, we have made some improvements in the
[22,25,27,28]. Although known as important risk factors for stratification of the patients. We adopted the SVS-WIfI classifica-
cardiovascular disease, these conditions do not appear to have tion system [26], which provides better assessment of the wound,
an impact on amputation or mortality rates in our sample the infection and the ischemia of the limb, allowing us to predict
[21,25,27,31]. the likelihood of the need for a revascularization procedure and/or
In this study, 92% of patients underwent one or more surgical major amputation. Alongside this system, we have established a
interventions. Mostly were debridement and minor amputations, better registry of the patients’ heart, lung and renal functions and
which were performed in 48% of the subjects. This express that other regular blood tests through adoption of a standardized
diabetic foot problems are a surgical condition, therefore requiring protocol, so we will be able to a better categorization of the
an evaluation by a specialized surgeon. patients. Finally, we are better assessing the patient’s functionality
Other important aspect was the high re-admission rate (39%). and quality of life through a multidisciplinary protocol designed in
First, the foot ulcer develops mostly in subjects with peripheral conjunction with physical therapists and nurses.
neuropathy. So, even after discharge with good wound care, the In conclusion, diabetic foot ulcer is associated with high
foot conditions for a relapse are maintained. Second, once we have amputation and mortality rates. Risk factors for major amputation
no structured heath program, there is a deficiency of adequate were old age, presence of peripheral arterial disease and low
primary and secondary medical care in our region [41], which hemoglobin level. Old age, major amputation and low hemoglobin
impairs the preventive measures for a new foot lesion. Although level were risk factors for death. The findings from the present
 R.H.R. Costa et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 11S (2017) S583–S587 S587

study add evidences on risk factors for major amputation and [20] Alvarsson A, Sandgren B, Wendel C, Alvarsson M, Brismar K. A retrospective
mortality associated to diabetic foot ulcer patients, with implica- analysis of amputation rates in diabetic patients: can lower extremity
amputations be further prevented? Cardiovasc Diabetol 2012;11:18.
tions for daily practice. Efforts to prevent major amputation should [21] Sun J-H, Tsai J-S, Huang C-H, Lin C-H, Yang H-M, Chan Y-S, et al. Risk factors for
be targeted at elderly patients especially those with PAD and lower lower extremity amputation in diabetic foot disease categorized by Wagner
hemoglobin levels. classification. Diabetes Res Clin Pract 2012;95(3):358–63.
[22] Setacci C, Sirignano P, Mazzitelli G, Setacci F, Messina G, Galzerano G, et al.
Diabetic foot: surgical approach in emergency. Int J Vasc Med 2013;2013.
[23] Lavery LA, Armstrong DG, Wunderlich RP, Mohler MJ, Wendel CS, Lipsky BA.
References Risk factors for foot infections in individuals with diabetes. Diabetes Care
2006;29(6):1288–93.
[1] Aguiree F, Brown A, Cho NH, Dahlquist G, Dodd S, Dunning T, et al. IDF Diabetes [24] Nirantharakumar K, Saeed M, Wilson I, Marshall T, Coleman JJ. In-hospital
Atlas. . mortality and length of stay in patients with diabetes having foot disease. J
[2] Frykberg RG, Zgonis T, Armstrong DG, Driver VR, Giurini JM, Kravitz SR, et al. Diabetes Complications 2013;27(5):454–8.
Diabetic foot disorders: a clinical practice guideline (2006 revision). J Foot [25] Gershater MA, Löndahl M, Nyberg P, Larsson J, Thörne J, Eneroth M, et al.
Ankle Surg 2006;45(5):S1–S66. Complexity of factors related to outcome of neuropathic and neuroischaemic/
[3] Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of ischaemic diabetic foot ulcers: a cohort study. Diabetologia 2009;3:398–407.
diabetic foot disease. Lancet 2005;366(9498):1719–24. [26] Mills JL, Conte MS, Armstrong DG, Pomposelli FB, Schanzer A, Sidawy AN, et al.
[4] Nabuurs-Franssen M, Huijberts M, Kruseman AN, Willems J, Schaper N. The Society for Vascular Surgery lower extremity threatened limb
Health-related quality of life of diabetic foot ulcer patients and their classification system: risk stratification based on Wound, Ischemia, and foot
caregivers. Diabetologia 2005;48(9):1906–10. Infection (WIfI). J Vasc Surg 2014;59(1)220–34 e222.
[5] Iversen MM, Tell GS, Riise T, Hanestad BR, Ostbye T, Graue M, et al. History of [27] Brownrigg JRW, Griffin M, Hughes CO, Jones KG, Patel N, Thompson MM, et al.
Foot Ulcer Increases Mortality Among Individuals With Diabetes Ten-year Influence of foot ulceration on cause-specific mortality in patients with
follow-up of the Nord-Trøndelag Health Study, Norway. Diabetes Care 2009;32 diabetes mellitus. J Vasc Surg 2014;60(4)982–6 e3.
(12):2193–9. [28] Lawrence SM, Wraight PR, Campbell DA, Colman PG. Assessment and
[6] Martins-Mendes D, Monteiro-Soares M, Boyko EJ, Ribeiro M, Barata P, Lima J, management of inpatients with acute diabetes-related foot complications:
et al. The independent contribution of diabetic foot ulcer on lower extremity room for improvement. Intern Med J 2004;34(5):229–33.
amputation and mortality risk. J Diabetes Complications 2014;28(5):632–8. [29] Moulik PK, Mtonga R, Gill GV. Amputation and mortality in new-onset diabetic
[7] Nouvong A, Armstrong DG. Diabetic foot ulcers. In: Cronenwett JL, Johnston foot ulcers stratified by etiology. Diabetes Care 2003;26(2):491–4.
KW, editors. Rutherford’s vascular surgery. 8th ed. Philadelphia: Elsevier [30] Nather A, Bee CS, Huak CY, Chew JL, Lin CB, Neo S, et al. Epidemiology of
Saunders; 2014. p. 1816–35. diabetic foot problems and predictive factors for limb loss. J Diabetes
[8] Hobizal KB, Wukich DK. Diabetic foot infections: current concept review. Complications 2008;22(2):77–82.
Diabetic Foot Ankle 20123:. [31] Aiello A, Anichini R, Brocco E, Caravaggi C, Chiavetta A, Cioni R, et al. Treatment
[9] Weck M, Slesaczeck T, Paetzold H, Muench D, Nanning T, Von Gagern G, et al. of peripheral arterial disease in diabetes: a consensus of the Italian Societies of
Structured health care for subjects with diabetic foot ulcers results in a Diabetes (SID, AMD), Radiology (SIRM) and Vascular Endovascular Surgery
reduction of major amputation rates. Cardiovasc Diabetol 2013;12(1):45. (SICVE). Nutr Metab Cardiovasc Dis 2014;24(4):355–69.
[10] Rezende KF, Nunes MA, Melo NH, Malerbi D, Chacra AR, Ferraz MB. In hospital [32] Won SH, Chung CY, Park MS, Lee T, Sung KH, Lee SY, et al. Risk factors associated
care for diabetic foot: a comparison between the estimated cost and the SUS with amputation-free survival in patient with diabetic foot ulcers. Yonsei Med
reimbursement. Arquivos Brasileiros Endocrinol Metabol 2008;52(3):523–30. J 2014;55(5):1373–8.
[11] Ekpebegh CO, Iwuala SO, Fasanmade OA, Ogbera AO, Igumbor E, Ohwovoriole [33] Prompers L, Schaper N, Apelqvist J, Edmonds M, Jude E, Mauricio D, et al.
AE. Diabetes foot ulceration in a Nigerian hospital: in-hospital mortality in Prediction of outcome in individuals with diabetic foot ulcers: focus on the
relation to the presenting demographic, clinical and laboratory features. Int differences between individuals with and without peripheral arterial disease.
Wound J 2009;6(5):381–5. The EURODIALE Study. Diabetologia 2008;51(5):747–55.
[12] (9) Microvascular complications and foot care. Diabetes Care 2015;38(Suppl) [34] Gregg EW, Li Y, Wang J, Burrows NR, Ali MK, Rolka D, et al. Changes in diabetes-
S58–66 United States. related complications in the United States, 1990–2010. N Engl J Med 2014;370
[13] Apelqvist J, Bakker K, Van Houtum W, Nabuurs-Franssen M, Schaper N. (16):1514–23.
International consensus and practical guidelines on the management and the [35] Kengne AP, Czernichow S, Hamer M, Batty GD, Stamatakis E. Anaemia,
prevention of the diabetic foot. Diabetes/Metab Res Rev 2000;16(S1):S84–92. haemoglobin level and cause-specific mortality in people with and without
[14] Norgren L, Hiatt WR, Dormandy Ja, Nehler MR, Harris KA, Fowkes FGR, et al. diabetes. PloS One 2012;7(8):e41875.
Inter-society consensus for the management of peripheral arterial disease [36] Harwant S, Doshi H, Moissinac K, Abdullah B. Factors related to adverse
(TASC II). Eur J Vasc Endovasc Surg 2007;33(1):S1–S75. outcome in inpatients with diabetic foot. Med J Malaysia 2000;55(2):236–41.
[15] Sereday M, Damiano M, Lapertosa S, Cagide A, Bragagnolo J. Amputaciones de [37] Wright JA, Oddy MJ, Richards T. Presence and characterisation of anaemia in
Miembros Inferiores en diabéticos y no diabéticos en el ámbito hospitalario. diabetic foot ulceration. Anemia 20142014:.
Asociacion latinoamericana de diabetes 2009;17(1):9–15. [38] Xie Y, Zhang H, Ye T, Ge S, Zhuo R, Zhu H. The geriatric nutritional risk index
[16] Lowe J, Sibbald RG, Taha NY, Lebovic G, Rambaran M, Martin C, et al. The independently predicts mortality in diabetic foot ulcers patients undergoing
Guyana diabetes and foot care project: improved diabetic foot evaluation amputations. J Diabetes Res 2017;2017:5797194.
reduces amputation rates by two thirds in a lower middle income country. Int J [39] Richards T, Loukogeorgakis S, Wright J, Hurel S. Anaemia, inflammation, renal
Endocrinol 2015;2015. function, and the diabetic foot: what are the relationships? Diabetic Foot J
[17] Blumberg SN, Warren SM. Disparities in initial presentation and treatment 2012;15(4):150–8.
outcomes of diabetic foot ulcers in a public, private, and Veterans [40] Desormais I, Aboyans V, Bura A, Constans J, Cambou J-P, Messas E, et al.
Administration hospital. J Diabetes 2014;6(1):68–75. Anemia, an independent predictive factor for amputation and mortality in
[18] Gürlek A, Bayraktar M, Savaş C, Gedik O. Amputation rate in 147 Turkish patients hospitalized for peripheral artery disease. Eur J Vasc Endovasc Surg
patients with diabetic foot: the Hacettepe University Hospital experience. Exp 2014;48(2):202–7.
Clin Endocrinol Diabetes 1997;106(5):404–9. [41] Rezende KF, Ferraz MB, Malerbi DA, Melo NH, Nunes MP, Pedrosa HC, et al.
[19] Hadadi A, Omdeh Ghiasi H, Hajiabdolbaghi M, Zandekarimi M, Hamidian R. Predicted annual costs for inpatients with diabetes and foot ulcers in a
Diabetic foot infections and outcomes in iranian admitted patients. developing country—a simulation of the current situation in Brazil. Diabetic
Jundishapur J Microbiol 2014;7(7):e11680. Med 2010;27(1):109–12.