Diabetic foot: clinical aspects
(Portuguese PDF version)

José Lacerda Brasileiro,1 Wagner Tadeu Pereira Oliveira,2 Leandro Borges Monteiro,2 Juliana Chen,3 Erasmo Lima Pinho Jr.,3 Sérgio Molkenthin,2 Maldonat Azambuja Santos,4

1. Assistant professor, Angiology and Vascular Surgery Service, Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande, MS, Brazil.
2. Resident physician, Vascular Surgery, Hospital Universitário de Mato Grosso do Sul, Campo Grande, MS, Brazil.
3. Medical student, UFMS, Campo Grande, MS, Brazil.
4. Chief of Angiology and Vascular Surgery Service, Hospital Universitário de Mato Grosso do Sul, Campo Grande, MS, Brazil.

Correspondence:
José Lacerda Brasileiro
Rua João Rosa Pires,641/1002, Amambaí
CEP 79008-050 - Campo Grande, MS, Brazil
Phone: +55 (67) 325.5599
E-mail: jlbras@terra.com.br


ABSTRACT

Objective: To study the clinical aspects of the diabetic foot, once it is a chronic complication of a frequently multifactorial etiology, including vascular, neural, articular, and infectious involvement.

Method: Retrospective analysis of 56 cases of diabetic foot examined by the Angiology and Vascular Surgery Service at the Hospital Universitário de Mato Grosso do Sul (NHU/UFMS) from 1998 to 2002.

Results:
The disease was predominant in males, between 51 to 70 years old, who suffered from diabetes type II for less than 10 years and were taking oral hypoglycaemic agents. Clinical manifestations most commonly found were the swelling of limbs, pain, and hyperemia. Amputations were performed in 71.4% of the cases. Of these, 55% were minor amputations (distal to the ankle), and 45% were major amputations (proximal to the ankle). The most common cause of diabetic foot was neuropathy (48.2%), and the peripheral arterial disease was the main cause of amputation. The prevalence of amputations in patients with diabetic foot was 73.2%.

Conclusion:
Peripheral neuropathy was the predominant etiology in the diabetic foot. Vasculopathy was the most frequent cause of amputation. Guidance on how to prevent foot complications is a major aid in reducing disabilities and deformities due to the diabetic foot.

Key-words: diabetic foot, diabetes mellitus, amputation.

J Vasc Br 2005;4(1):11-22


Diabetes mellitus is a chronic and complex metabolic disorder, characterized by a compromised metabolism of glucose and other energy-producing substances, associated to a range of complications in essential organs for life maintenance.1,2

It constitutes a major public health problem, due to the high prevalence and morbidity/mortality, besides the risk of development of disabling chronic complications (such as retinopathy, nephropathy, neuropathy, and vasculopathy) and the high cost of the treatment and the reduction of work capacity in individuals at a productive age.3,4

Its prevalence is estimated to be around 120 million individuals worldwide. Of these, between 4% to 10% develop foot injuries. In Brazil, a multicenter study performed in nine capitals found a prevalence of 7.6% among people between 30 to 69 years old. Almost half of them were unaware of the disease, and approximately 25% of the previously diagnosed diabetic patients were not under any kind of treatment. A projective analysis estimated that, between 1995 and 2025, the number of diabetic individuals will grow 42% in developed countries, and 170% in developing countries.5-7

Concerning its chronic complications, the diabetic foot is the most frequent cause of complications, with a high level of amputations, prolonged hospitalization, and hospital cost in our environment. In the United States, diabetes is responsible for almost half of the non-traumatic lower limb amputations.8,9

The diabetic foot often has a multifactorial etiology and is characterized by a variety of abnormalities resulting from the combination of neuropathy and/or vasculopathy in patients with diabetes mellitus.10

The neuropathy, whose most accepted pathogenic mechanism is the polyol pathway, can present itself under three forms: 1) motor, characterized by the alteration in the foot architecture that displaces the sites of plantar pressure, and by alterations of collagen, keratin, and fat pad; 2) autonomic, in which there is a sympathetic dysfunction, resulting in the reduction of sweating and the alteration of microcirculation; 3) sensorial, the most common of all, in which there is a loss of protective sensation of pressure, heat, and proprioception, in such a way that minor repetitive traumas and even major damages are not noticed by the patients.11-17

Regarding diabetic vasculopathy, studies showed that age and duration of the diabetes mellitus, as well as its neuropathy, were also correlated to its prevalence. Vasculopathy can present itself under two forms: 1) microangiopathy, which, according to LoGerfo & Coffman,18 is not considered a major factor in the injury pathogenesis, since it does not compromise the reduction of blood flow to the foot of the diabetic patient, despite the thickening of the capillary basal membrane; 2) macroangiopathy, resulting in an atherosclerotic process, which, in the diabetic patient, is more frequent, premature, progressive, and more distal, therefore, more severe. In the lower limb, the most commonly affected vessels by arteriosclerosis are the tibial arteries. The fibular and feet arteries are generally preserved. Artery calcification can be present, being observed in 94% of the patients suffering from diabetes for 35 years.12,19-21

There is also the combined form (neuro-ischemic), in which both the neuropathy and the angiopathy contribute to the development of foot injuries.

Moreover, the loss of sensitivity in the lower limbs may result in the formation of neurogenic osteoarthropathy (diabetic neuroarthropathy or Charcot arthropathy). It is a complication that affects approximately 0.2% of the diabetic patients, generally between 50 and 60 years old, with the disease for at least 10 years. It results in acute fractures, subluxations or displacement that cause permanent deformity in the foot, generally associated to the reduction or loss of the protective and selective sensation of the thermal and vibratory perception, presenting an asymptomatic clinical course, with progressive bone and articular degeneration.22-24

Concerning the development of the diabetic foot ulceration, neuropathy and peripheral vasculopathy are the most important factors. However, neural involvement is the main cause of most injuries in the diabetic foot. In general, patients go to the hospital due to ulcerations or necrosis secondary to the painless trivial trauma. The most important fact about the peripheral neuropathy in the diabetic foot is the loss of sensitivity, making it vulnerable to trivial traumas, driving bacteria into the wound, and causing silent and severe infections in case they are not treated in an early stage.

Thus, for a successful ulcer treatment, it is important to determine, in the initial assessment, the etiologic factor (ischemic, neuropathic or neuro-ischemic), which can be done through clinical data and complementary exams.25,26

The presence of infection should also be verified early, through the foot exam (location of flogistic signals) or in case of a systemic disorder (such as fever and poor glycemic control), since it represents a major factor of morbidity and mortality in patients with ulcers. The highest susceptibility of the diabetic patient to the infection is a consequence of the loss in the inflammatory response and in the antioxidizing system, the alteration of migration, phagocytosis and chemotaxis of leucocytes, and the lower production of cytokines. Hyperglycemia is the earliest sign of infection, while fever, leucocytosis, chills, and signs of inflammation can be absent in up to 2/3 of the cases, due to the concurrent presence of neuropathic and/or vascular alterations. Thus, the severity of the infection is not related to the causal pathogen and the decision for the therapy should not be based on it.17,27-29

The culture of an infected injury can identify the etiologic agents, but only if it is collected and processed appropriately. The curettage or grattage of the base of a debrided ulcer and the surgical material obtained from the tissue constitute reliable pieces for the culture, being the infection generally of a polymicrobial nature, involving aerobic and anaerobic microorganisms.30,31

Concerning radiological exams, the helical computerized tomography offers a quick assessment of the limbs, although it has a high cost. Magnetic resonance, besides being an expensive exam, does not offer an assessment of the direct physical density, despite Gefen et al.32 having considered such exam to be effective in showing the tissues damaged by ulceration. Ultrasound has little efficiency due to bone shadows and because it does not penetrate effectively in the presence of air. On the other hand, digital and conventional radiography generate loss of tridimensional information, geometric distortion, and relative poor soft tissue contrast, although they are useful in diagnosing Charcot arthropathy and osteomyelitis.33

For the vascular assessment, the anatomical level of the artery stenosis can be obtained through pulse palpation in lower limbs. Contrast arteriography is considered the gold standard, but the measurement of the ankle/brachial pressure index remains an essential assessment tool, except in the presence of lower limb artery calcification.34

Regarding neuropathy assessment, the whole nerve biopsy or skin puncture associated to immunohistochemistry, electrophysiological and tactile and vibratory sensitivity tests are some of the existing methods. However, in the daily clinical practice, the physical examination with monofilament or tuning fork is the most used method.16,35

The treatment of the diabetic foot is based on the reduction in tissue pressure of the foot, infection control, ischemic correction, and cares with the injury. Rest and limb elevation must be started immediately. Ideally, all weight from the lower limbs should be removed. Concerning the infection, despite the fact that the culture and the antibiogram aid in choosing antimicrobial regimens, most of the times the empirical technique with wide spectrum drugs is necessary before the results of the culture become available. The vascular involvement should be verified in the first physical examination and also in case of a poor therapeutic response, making the correction of the vascular occlusive disease necessary, since it makes difficult to provide nutrients and antibiotics to the injured area.30,36

Concerning surgical intervention, the debridement is an important auxiliary method, since it removes devitalized tissue, helps to control the infection, and stimulates the proliferative healing stage. The metatarsal head resection aims at reducing the high focal pressure peak around the affected metatarsal heads. Nevertheless, Edmonds37 observed a reulceration rate of 52% after 35 months of follow-up.15,38

Depending on the clinical evolution and the involvement level, the lower limb amputation, despite its individual and social implications, can be necessary. It is classified into two forms: minor (when performed distal to the ankle), and major (when performed proximal to the ankle).39

Thus, the present study aims at analyzing the cases of diabetic foot at the Hospital Universitário de Mato Grosso do Sul (NHU/UFMS), estimate the prevalence of amputations, as well as assessing the clinical evolution of the diabetic foot.

MATERIAL AND METHOD

We performed a retrospective assessment of patients with diabetic foot examined by the Angiology and Vascular Surgery Service at the Hospital Universitário de Mato Grosso do Sul (NHU/UFMS) from January, 1998 to December, 2002.

RESULTS

Of the 56 patients studied, 33 (58.9%) were male and 23 (41.1%) were female, while white was the predominant race (69.6%), followed by mulatto (28.6%) and black (1.8%).

Concerning the age group, most patients (60.8%) were between 51 and 70 years old, 10 (17.8%) were between 31 and 50 years old, 10 (17.8%) were older than 70 years old, and only two (3.6%) were younger than 30 years old.

Regarding origin, most (57.1%) were from Campo Grande (state of Mato Grosso do Sul, Brazil), while 39.3% were from other cities in Mato Grosso do Sul, and 3.6% were from other Brazilian states.

Diabetes mellitus type II (or non-insulin-dependent) was the most common (94.6%), while only 5.4% were type I (or insulin-dependent).

Concerning the diagnosis period of the diabetes mellitus until the hospitalization due to the diabetic foot, only in 11 cases (19.6%) it was not possible to assess the duration of the disease, because in seven cases this information was not in the patients' records, and four patients did not know the diagnosis at the time of hospitalization. In the cases whose duration was known, in 24 patients (53.3%) the duration was less than 10 years, and in 21 cases (46.7%) it was more than 10 years. .

Concerning the treatment of the diabetes mellitus, 47 patients (83.9%) were under treatment, while nine (16.1%) were not, either because they were unaware of the disease, or by their own behavior (four and five cases, respectively). Of those under treatment, 29 patients (61.7%) were taking oral hypoglycaemic drugs, 16 (34%) were taking insulin, and two (4.3%) were taking insulin and oral hypoglycaemic drugs concurrently.

Regarding the diabetic complications, retinopathy was present in 16 cases (28.6%). Regarding nephropathy, nine patients (16.1%) presented varying degrees of renal dysfunction, and three (33.3%) were already in need of dialysis periodically. Episodes of previous hyperglycaemic condition were reported in six diabetic patients (10.7%). Of these, 50% had only one episode, 33.3% had from two to five episodes, and 16.7% had more than five episodes. Diabetic gastroparesis was found in one patient (1.8%).

In seven patients (12.5%), there was a history of previous amputation. Of these, six (85.7%) were minor amputations, and one (14.3%) was a major amputation, with a period range between 1 month and 7 years.

The diseases associated to diabetes mellitus were present in 35 individuals (62.5%). The systemic artery hypertension was the predominant disease (91.2%), followed by the cerebral vascular accident (23.5%), the cardiac congestive insufficiency (14.7%), and dyslipidemia (5.9%). Other diseases found in a smaller proportion were gastritis, benign prostatic hyperplasia, obesity, chronic obstructive pulmonary disease, heart disease, anemia, venous insufficiency, and psychiatric alterations. However, 21 patients (37.5%) did not present other diseases than diabetes mellitus.

In the initial assessment, through reported clinical data or previous diagnosis, 27 patients (48.2%) presented a neuropathic foot, 26 (46.4%) presented an ischemic foot, and three (5.4%) presented a combined foot (neuro-ischemic). Volume increase (57.1%), pain (50%), and hyperemia (48.2%) were the most commonly observed complaints, followed by the presence of purulent secretion (41.1%), heat (26.8%), and gangrene (19.6%). Other clinical manifestations observed were: necrosis, trophic alterations, cyanosis of the extremities, and paresthesia (Figure 1). Signs of infection were present in 36 cases (64.3%).

click hereFigure 1 - Clinical manifestations observed in patients with diabetic foot, NHU/UFMS, 1998-2002.

Concerning the evolution (that is, the period from the initial manifestation until hospitalization), 31 cases (55.4%) had from 8 to 30 days of evolution, 11 (19.6%) had up to 7 days, eight (14.3%) had from 30 to 60 days, and six (10.7%) had more than 60 days. The mean evolution time was 37.9 days.

Concerning the anatomical extension of the diabetic foot injury, 32.1% were restricted to the toes, 28.6% to the forefoot, 16.1% to the leg, 10.7% presented an injury of the whole foot, 7.1% were restricted to the rearfoot, and 5.4% to the forefoot and hindfoot. Considering only the digital injury, the first toe was the most affected (50%), followed by the second toe with 44.4%, while the third toe was affected in 27.8% of cases, the fourth toe in 16.7%, and the fifth toe in 5.5%. Regarding the quantity of affected toes by case, most (66.7%) presented only one affected toe, 22.2% two affected toes, and 11.1% three affected toes.

The most affected limb was the left one (51.8%), while in 44.6% of cases the right side was affected, and 3.6% of cases presented a bilateral involvement.

Radiological exams were requested in 43 cases (76.8%). Of these, simple radiography of the affected foot was performed in 31 patients (73.8%), and 24 patients (55.8%) were submitted to lower limb angiography. Varying degrees of arteriopathy were shown in all patients submitted to the angiography. Iliac artery occlusion was detected in two cases (Leriche syndrome).

Culture was performed in 24 cases (42.8%). Of these, gram-negative species were predominant (62.5%), followed by gram-positive species in 41.7% of cases; anaerobes were not shown. Negative results were observed in three cases (12.5%), and in one case (4.2%), the culture indicated contamination. Only gram-negative species were seen in 41.7% of cases, only gram-positive species were found in 20.8%, and the presence of both types was seen in 20.8% of the results. Only one species was found in 41.6% of cases, while 33.3% presented two species, and the presence of three or four species was seen in 4.2% of cases.

The most commonly isolated germ was the Proteus (29.2%), followed by the Enterococcus and Klebsiella (both with 20.8%).

Regarding the surgical procedures performed, 44.7% of patients were submitted to debridement, 71.4% to amputation (55% minor amputations, 25% transtibial amputations, and 20% transfemoral amputations), 21.4% to peripheral revascularization, and 5.3% to other procedures (namely, thromboembolectomy and lumbar sympathectomy) (Figure 2).

click hereFigure 2 - Surgical procedures performed in cases of diabetic foot, NHU/UFMS, 1998-2002.

In 13 patients (23.2%), debridement was the only surgical treatment, while 20 patients (35.7%) needed to undergo amputation, and in 10 patients (17.9%) both procedures were performed. Considering all surgical interventions and reinterventions, 105 procedures were performed, with an average of 1.87 procedures/patient.

The ischemic diabetic foot was the main cause of amputation in the present study. Of the 26 patients with vasculopathy, 23 (88.5%) were submitted to amputation, being 12 major amputations and 11 minor amputations (Tables 1 and 2). Nine individuals had to undergo amputation after the peripheral revascularization, being seven minor amputations and two major amputations.

click hereTable 1 - Amputation and variables of gender, age, characteristics related to diabetes mellitus, type of foot, and history of previous amputation, NHU/UFMS, 1998-2002

Variables Categories n Amputation
n %
Gender Male 33 25 75.7
Female 23 15 65.2
Age < 30 years old 2 1 50.0
31-50 years old 10 7 70.0
51-70 years old 34 25 73.5
> 70 years old 10 7 70.0
Diabetes Type I 3 2 66.7
Type II 53 38 71.7
Duration < 10 years 24 17 70.8
Duration > 10 years 21 14 66.7
Medication: insuline 16 08 50.0
Medication: oral hypoglycaemic agents 29 22 75.9
Medication: insuline + oral hypoglycaemic agents 2 - -
Type of
diabetic foot
Neuropathic 27 16 59.2
Ischemic 26 23 88.5
Combined 3 1 33.3
Previous amputation Present 7 5 71.4
Absent 49 35 71.4

 

click hereTable 2 - Type of amputation related to gender, age group, and type of diabetic foot, NHU/UFMS, 1998-2002

Variables Categories n Amputation
Minor amputation Major amputation
n % n %
Gender Male 33 12 36.4 13 39.4
Female 23 10 43.5 5 21.7
Age < 30 years old 2 - - 1 50.0
31-50 years old 10 4 40.0 3 30.0
51-70 years old 34 16 47.0 9 26.5
> 70 years old 10 2 20.0 5 50.0
Type of diabetic foot Neuropathic 27 11 40.7 5 18.5
Ischemic 26 11 42.3 12 46.1
Combined 3 - - 1 33.3

 

Two patients died (3.6%), one by septic shock, and one by pulmonary embolism during hospitalization. The other patients had hospital discharge without intercurrences. Nevertheless, eight patients (14.8%) had to be hospitalized again after a short period (less than 1 month) due to infectious complications, mainly in the amputation stump. However, there was one case of infectious complication in the vascular prosthesis. As a consequence, among the eight patients hospitalized again, 50% were submitted to debridement and amputation, 25% only debridement, 12.5% only amputation, and 12.5% to vascular prosthesis removal. In these cases, amputations were minor in two cases, and major in three cases.

Regarding the evolution of the diabetic foot, there was a recurrence in a period of less than 1 year in two cases (3.7%) since the last hospitalization. One of them was submitted to a minor amputation (of a toe), while the other one was submitted to a major amputation (in a supracondylar region).

Assessing the total hospitalization period per diabetic foot, we found an average of 30.7 days, with an average of about 32 days for patients submitted to amputation. Based on the anatomical level of the lower limb injury at the time of hospitalization, the average was 33.8 days for cases restricted to the toes, 30.3 days for those restricted to the foot, and 25.9 days for those with leg injury.

Regarding the sequels of the diabetic foot, considering patients with a previous amputation (who did not need a new amputation in the period of the study) as well as the amputations performed during the study, of the 54 patients who had hospital discharge, 41 individuals (75.9%) underwent amputations. Of these, 23 (56.1%) were minor amputations, and 18 (43.9%) were major amputations. In the same group, in six individuals (11.1%) there was further death - five of them (83.3%) had been submitted to lower limb amputation in a period varying from 2 to 38 months (average of 13.8) after the last hospitalization, due to etiology unrelated to the diabetic foot.

DISCUSSION

The diabetic foot is a complication of a frequently multifactorial etiology, in which there can be a neural, articular, vascular, and infectious involvement. Moreover, it can cause mutilation, creating suffering, disability, and work absence.26

As observed by El-Shazly et al.,40 lower limb complications in patients with diabetes mellitus were more common in males (58.9%) and in the age group between 51 and 70 years old (60.8%).

According to Milman et al.,8 the diabetic foot was more frequent in the diabetes mellitus type II. However, this study diverges when observed that the group of patients with a higher prevalence of lower limb injuries was the group with diabetes mellitus with a period of less than 10 years (53.3%).

Although El-Shazly et al.40 report that insulin-dependent diabetes types I and II (which represents an advanced stage) can predict lower limb complications, we have observed that the type II under oral hypoglycaemic agents was predominant (61.7%).

The presence of retinopathy and nephropathy, which are chronic complications of the diabetes mellitus, is important, since, as in the diabetic foot, the duration of the base disease is the longest determining time for their occurrence, being found in 28.6% and 16.1% of cases, respectively. Diabetic gastroparesis, an alteration in the gastrointestinal motility as a consequence of neuropathy, also occurs late in the diagnosis of diabetes mellitus, being found in only one patient.19,41

Among the diseases associated to the diabetes, systemic artery hypertension was the most common (91.2%), once these patients presented high levels of cardiovascular risk factors. Besides, the occurrence of the association of these two diseases multiplies the risk factors for the micro and macrovascular disease, resulting in an increase of cardiovascular mortality risk, coronary disease, cardiac congestive insufficiency, cerebro-vascular disease, and peripheral vascular disease.7,42

Delay of appropriate treatment of the diabetic foot increases the occurrence of complications and the need for amputation. In this study, the evolution average was 37.9 days. In some cases, the duration was more than 2 months (10.7%).

In the initial assessment it is important to determine the etiologic factor (ischemic, neuropathic or neuro-ischemic) in order to decide the diagnostic and therapeutical behavior, which can be deducted from the patient's clinical history and physical examination.

High pressure is usually the cause of the neuropathic ulcer, due to alterations in the plantar distribution, although it can also occur in the absence of such factor through a constant pressure or a repetitive moderate pressure, being commonly located in the metatarsal head. Other types of ulcer have a chemical, thermal origin, and are caused by poor hygienic conditions.43,44

Concerning the ischemic ulcer, the use of shoes, especially new ones, is a significant cause of ulceration, besides contributing to the foot deformity. The most common locations are the first and fifth metatarsal heads. There is no tendency to develop in plantar regions, where blood supply is relatively more preserved.12,37

The purely ischemic ulcers are relatively uncommon. Such patients, due to the associated neuropathy, can present tissue loss or gangrene as a first severe sign of the peripheral vascular disease, and the symptoms can be absent despite the presence of severe ischemia.17,45

It is estimated that between 70% and 100% of foot injuries present clear signs of neuropathy. Thus, the diabetic neuropathy represents a factor frequently associated to ulcerations, which makes us highlight the fact that the absence of clinical status does not exclude its presence or the risk of foot ulceration.16,45

Regarding complementary exams, contrast angiography was performed in 24 patients. All of them presented varying degrees of arteriopathy, which was expected, since arteriosclerosis is statistically more frequent in diabetic patients. However, although there is a characteristic involvement of the infra-popliteal vessels, it can also involve, as in the cases of Leriche syndrome observed, the abdominal aorta, iliac, and femoral arteries.20,21

Arteriography, despite being the gold standard for assessing the peripheral arterial disease, is an invasive procedure. Patients with limited renal function can have contrast-induced nephrotoxity. Thus, arteriography should only be indicated for patients who will be submitted to surgery.34

The simple radiography of the affected area was requested in 31 patients, being the easiest, most accessible, and less expensive method to detect bone involvement, although the computerized tomography and the nuclear magnetic resonance, whose limiting factor is the high cost, have better accuracy.30,38

Regarding the culture results, gram-negative species were predominant (62.5%). Most of them isolated one or two species (74.9%). The presence of species from both gram groups only occurred in 20.8% of the results. However, studies report that gram-positive species are the predominant pathogens, and usually the infection is polymicrobial with four to five organisms involved.12,17,25,46

Anaerobic germs were not shown in the exam. Steed,38 however, estimates that they are found in around 25% of diabetic injuries, and, due to the difficulty in the appropriate processing of anaerobic cultures, they can be present even when not identified in the culture.

The diabetic foot infection can be classified into no risk (or mild) and risk of limb loss. The first one, being superficial, with no systemic toxicity and with a low degree of ischemia, is usually caused by streptococcus and staphylococcus sensitive to oxacillin and to most beta-lactamic antibiotics. Anaerobic gram-positive coccus can be found. In the second group, due to the presence of major ischemia, lymphangitis and a higher extension and depth of the injury, aerobic gram-positive coccus are predominant (staphylococcus, streptococcus, and enterococcus), besides the presence of aerobic gram-negative bacili (such as E. coli and Enterobacter) being more frequent. However, in more severe infections, it is necessary to take therapeutic measures for gram-negative anaerobes (such as Bacteroides) and non-fermenter gram-negative bacilli (such as Pseudomonas and Acinetobacter).47

Moreover, it is important to highlight that it is currently being observed an increase in the number of infection cases due to multiresistant pathogens, mainly involving gram-negative bacilli (such as Enterobacter, Serratia, Providencia, Citrobacter, Morganella, E. coli and Klebsiella pneumoniae).48

Regarding the surgical treatment, the debridement is a useful method, since it aids the diagnosis through assessment of injury extension and depth, besides having a part in the therapeutic process, because it reduces the bacterial load in the location, removes the necrotic tissue, and stimulates healing. There are cases in which its use, associated to parenteral antibiotics and local cares (such as dressing, rest, and limb protection) and the base disease are enough to heal the ulceration, in order to avoid amputation.38

On the other hand, amputations were performed in more than half of the cases of diabetic foot (71.4%), which shows that lower limb amputations are still necessary in many cases, despite the improvement in the treatment of ulcers and the severe implications for the functional status, well-being, and survival of the individuals. The triad of peripheral neuropathy, vasculopathy, and infection susceptibility is a classic high-risk scenario for its use.12,36,49

Statistical data from the United States and Sweden showed that 50% and 32% of non-traumatic lower limb amputations are related to diabetes. Another study made in Rio de Janeiro and in the Baixada Fluminense found an incidence about 13 times higher of amputation comparing to individuals without diabetes.45 Moreover, although most amputations were performed in individuals around 50 years old, young patients can also be submitted to amputation, as it was shown in this study and by Levin.25

Although neuropathy is the most common etiologic factor in the diabetic foot, the peripheral vascular disease was the predominant cause of amputation in this study. The importance of its association to diabetes relies in the fact that it contributes to ulceration, gangrene, and healing delay, since it reduces the defense ability against infections, jeopardizing the supply of nutrients and antibiotics to the affected area. Thus, the treatment of vasculopathy should be assessed after the control of the injury and/or infection, since the possibility of improving blood flow is an important factor in order to avoid a major amputation.17,19

However, even after the peripheral revascularization, there may be necessary to perform a further amputation, especially of a minor type, as it was also observed by Calle-Pascual et al.50

The cause of hospitalization after a short period of discharge was related to the presence of infection, mainly in the amputation stump. The treatment is dramatic, since there is a possibility of more proximal amputations if the debridement alone is not efficient.

There was a recurrence of ulceration in two patients (both in a period less than 1 year and both underwent amputation). Nevertheless, it is important to notice that such value may not correspond to reality, since around half of the patients (42.9%) were not from Campo Grande, making the periodic follow-up difficult.

As it has been observed in other studies, diabetic foot is associated to major rates of hospitalization, with repeated surgical interventions and annual hospitalizations. Besides, success in healing of diabetic foot ulcer demands a long period of treatment, involving clinical visits, hospitalizations, and dressing changes.8,51,52

It is estimated that the prevalence of ulcer is in 4% to 10% of the diabetic patients. Its presence precedes around 85% of lower limb amputations. Therefore, several studies observed that the identification of risk factors for ulceration and early treatment, as well as a good glycemic control, periodic assessment (at least annually) of levels of glycosylated hemoglobin, besides proper foot care (through therapeutical shoes, daily inspection, trauma protection, regular visits to the doctor, and handling of nails and calluses by professionals) are directly associated to a lower incidence of amputation in patients with diabetes.45,53

As a consequence, the importance of its prevention has currently increased, despite recent improvements in the knowledge and in the treatment of the diabetic foot, since it is observed that the time and costs generated are lower comparing to major hospital and medication expenses caused by the treatment, besides a better physical, social and psychological condition of the patients and their family. It was also observed that diabetic patients who follow a diabetic foot care program have a risk of ulceration eight to 22 times lower.44,54

Finally, it is observed that the last and most important assistance is based on guidance in order to prevent ulcerations. However, diabetes mellitus is a disease difficult to manage. Besides the continuity of the medication therapy, it also involves a series of changes in the individual's life habits. Patience and strictness are needed in order to have a good glycemic control, as well as proper foot care, through daily inspection, regular visits to the specialist, adequate shoes that do not generate pressure, attention when cutting the nails and to the occurrence of calluses, proper hygiene with substances that do not provoke skin irritation or injuries. Thus, awareness and cooperation, both from the patients and from their family, are essential for the success of ulceration prevention and diabetic foot complications, besides a multidisciplinary team able to guide, early diagnose, and treat the diabetic disease.45,55

CONCLUSION

The diabetic foot was predominant in males, between 51 to 70 years old, who suffered from diabetes type II for less than 10 years and were taking oral hypoglycaemic agents.

Peripheral neuropathy was the predominant etiology in the diabetic foot, while vasculopathy was the most frequent cause of amputation.

Despite the implications in the well-being and survival of the patients, amputation is still needed and it was performed in 71.4% of cases.

Preventive measures are essential in the diabetic foot treatment. Control of the diabetes mellitus, guidance in order to avoid ulcerations through proper foot care, and regular visits to the doctor, as well as the cooperation of the patient and their family are fundamental in preventing disabilities and deformities caused by the diabetic foot.

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