A Survey of the Presence of Lower Limb Arterial Insufficiency in Diabetic Patients Attending the Surgery Department of Golestan Hospital for Reasons other than Vascular Diseases

Diabetic ulcer is the commonest reason of lower limb amputation. When atherosclerosis progressed, lower limb ischemia occurred. We also know diabetes is one of the effective risk factors in atherosclerosis, for this reason lower limb ischemia is one of the commonest long term complications of diabetes. Chronic lower limb ischemia could be asymptomatic or occur with intermittent claudication with pain and cramp in legs muscles. Pain begins with activity and relieves with rest. First, ischemia associated with intermittent claudication and then painful ulcer with gangrene was observed. The other symptoms such as muscles atrophy, cutaneous atrophy, hair loss on dorsal surface of fingers, and increase in the thickness of toenails are associated to chronic ischemia. This study was conducted on diabetic patients admitted to the surgery department for reasons other than vascular diseases. We designed the Pro forma to record the patients’ history including personal information, duration of suffering from diabetes. In addition, the symptoms of arterial insufficiency such as intermittent claudication, atrophic changes, cutaneous atrophy, muscles atrophy, hair loss on dorsal surface of fingers and increased thickness of toenails as well as pulse status other physical examinations were performed. The collected data were analyzed with SPSS package. Our study conducted on 120 diabetic patients that 52 (43.3%) patients were men. And 68 (56.7%) patients were women. Mean age in men and women had been 60.8 ±10, 56.8± 8.8. Based on our results 26 (21.7%) patients arterial pulse was not palpated and in 41 (34.2%) patients we found weak arterial pulses and in 53 patients (44.2%) arterial pulses were normal. Variance analysis test showed that the mean of the duration of suffering from diabetes had significant difference in these three groups (P= 0.018). In other tests, pallor was observed in 49.2% of patients. Intermittent claudicating was found in 32.5%of patients and impaired capillary filling test were seen in 60% of patients. Results of the rubor of dependency test were positive in 43.5% of patients and venous filling time test in 60% of patients was abnormal. And in 65% of patients coldness of extremities was positive. Our findings showed that the performed clinical tests facilitate the diagnosis of ischemia and therefore it seems necessary to perform these tests for all diabetic patients especially when admitted for surgery operation.


INTRODUCTION
Several studies have shown that there is a direct relationship between arterial disorders and foot ulcers. In fact, we can say that arterial diseases might be a risk factor for the impairment of wound healing and consequently amputation (1).
Peripheral arterial disease (PAD) is the chronic arterial occlusive disease in lower limbs due to atherosclerosis. Only half of the elderly patients with confirmed peripheral arterial disease are symptomatic. Patients with peripheral arterial disease might not be able to walk long distances or move fast enough due to comorbid conditions such as lung disease or arthritis. Ulcers caused by chronic arterial insufficiency are formed commonly in the ankle, heel or leg. The case of fingers turned blue, dried away, and mummified or soft tissue lacking life covered with scabs is the gangrene caused by ischemic infarction. As time goes by, the lesion becomes purulent and dry gangrene turns into wet gangrene (1,3,4,2). PAD is very common in patients with diabetes and is considered one of the causes of diabetic foot ulcers especially in men. PAD causes impairment in wound healing followed by amputation. Arterial disorder is one of the most important risk factors of diabetic foot. The lower limb ischemia occurs as a result of the progression of arterial atherosclerosis and since diabetes is the most effective risk factor for atherosclerosis, therefore, it is one of the most common long-term complications of diabetic lower limb ischemia (5). Besides intermittent claudication other symptoms that can be seen in chronic ischemia include cutaneous atrophy, muscle atrophy, loss of hair on the dorsal surface of foot, and thickness of toenails (6,7,5), which in the case of the change of foot form, this problem can cause unusual pressure to the leg (8). Among the symptoms of lower limb ischemia lack of arterial pulse, cold extremities, and color changes in foot along with position change could be mentioned (7,9). In mild to moderate ischemia the lack of pulse is the only clinical finding that is an indication of the presence of the disease in the examined position or proximal to it, which are expressed as three cases: it is not palpated at all (0), it is palpated decreased (1+) or normally (2+) (10,5,7). Conventional tests in vascular examinations include: 1) measuring the ABI (anklebrachial index) index, 2) measuring the (blood?) pressure, 3) venous filling time test, and 4) capillary filling test, (9,1,6). The most important risk factors for PAD in diabetic patients that can be noted include old age, gender (in men the risk of the disease is higher), the duration of suffering from diabetes, high blood pressure, high HbA1c, high FPg (fasting plasma glucose), and higher BMI (14). In patients with diabetes PAD is diagnosed too late, which results in an increased incidence of complications and increased severity of infections and this leads to foot ulcers, gangrene, and amputation (2,9). The early diagnosis of PAD, in addition to changing and transforming risk factors and decreasing their dangerous complications, causes the improvement of the quality of vascular reconstruction treatment methods (angioplasty and bypass) and enhances the effectiveness of the treatments (13,12). To diagnose the infection and its causes, culture, and antibiogram of the wound different methods are used including antibiogram from the wound, biopsy from the deep parts of the wound, X-ray of the foot, bone scan with labelled leukocytes, and MRI (14).
Diabetic patients are more vulnerable to various injuries than non-diabetic patients, thus, surgery is generally a risky operation for these patients, especially for the ones with ischemia. Therefore, this study was aimed at determining the prevalence of the symptoms of ischemia in diabetic patients that are candidate of a surgery.

MATERIALS AND METHODS
This is a cross-sectional study conducted in 2010 in Golestan Hospital. The study population consisted of 120 diabetic patients not suffering vascular diseases, who were hospitalized in the above-mentioned hospital for various reasons. The patient's history including personal information, duration of suffering from diabetes and symptoms of arterial insufficiency including intermittent claudication, cold extremities, trophic changes including cutaneous atrophy, muscle atrophy, loss of hair on the dorsal surface of the fingers and toes and thickness of fingernails were taken from patients. Then, they were placed under examination and other tests. Examinations and tests included the examination of pulses for three modes: pulse does not palpate at all (0+), pulse has reduced (1+) and/or it is palpated normally (2+), rubor of dependency test, capillary filling test, venous filling time test, and occurrence of pallor test.
The pulses were examined for three conditions: pulse does not palpate at all (0+), pulse has reduced (1+), and/or pulse is palpated normally (2+). In the time method, the leg was elevated for 20 seconds, if the venous filling time takes less than 15 seconds after lowering the leg there is no problem (0), if it takes between 15-30 seconds it is (1+), if it takes between 30-40 seconds it is (2+), between 45-60 seconds it is (3+), and if it takes more than 60 seconds it is (4+). In the occurrence of pallor test, the leg was elevated for 60 seconds and grading was done based on the pallor induction period. It was considered (0+) for absence of pallor, (1+) for occurrence after 60 seconds, (2+) for between 30-60 seconds, (3+) for less than 30 seconds, and (4+) when pallor occurs quickly.
After taking patient's history and performing abovementioned examinations and tests, the obtained results were recorded in a special checklist that was prepared for this purpose. The data were then entered into the computer and were analyzed by SPSS 18 software. Statistical tests used for data analysis included ANOVA test, student's t-test, chi-square test, and Fisher's exact test.

RESULTS
In this study, 120 patients, who had no history of vascular diseases and had been admitted to the surgery department of Golestan hospital for various reasons, were investigated. The mean age of these patients was 58.6 ± 9.5. The minimum and maximum observed ages were 38 and 80 respectively. 18 (15%) of these patients were under 50, 49 patients (40.8%) were in the age range of 59-50, 35 (29.2%) were in the age group of 69-60 , and 18 (15%) were in the age group of 60 years and older (Figure 1).
Fifty-three (44.3%) patients were female and 67 (55.8%) male (Fig. 2). The mean age of these men and women were 60.8 ± 10 and 56.8 ± 8.8 years respectively, and according to student's t-test the mean age of women and men had a significant difference (p = 0.02) ( Table 1).
The mean of the duration of suffering from diabetes in these patients were 9.3 ± 4.15 years. The minimum and maximum duration of suffering from the disease were 6 and 25 years, respectively. In addition, 16 (13.3%) patients had been suffering from diabetes for less than 10 years. 16 (13.3%) had diabetes for 10-14 years, 74 patients (61.7%) for 15-19 years, and 14 (11.7%) 20 for years or more ( Figure 3).
According to the examinations carried out, 26 patients (21.7%) had no arterial pulse, in 41       patients (34.2%) there was a reduction in pulse rate, and also in 53 patients (44.2%) the arterial pulse was normal ( Figure 4). The analysis of variance (ANOVA) test showed that the mean of the duration of suffering from diabetes in these three age groups had significant difference (p = 0.018) ( Table 2).
According to the results of this study, 67 (55.8%) of the patients were male and 53 (44.2%) were female. Arterial insufficiency was observed in 24 females and 43 males (46.2% vs. 63.2%), but according to chi-square test, there was no significant difference between the frequency of arterial insufficiency and gender (p = 0.07) ( Table  3).
The mean age of patients with lower extremities arterial insufficiency was 57.4 ± 8.1 and in patients without arterial insufficiency it was 60 ± 10.9 years and according to student's t-test the mean age of the two abovementioned groups had no significant difference (p = 0.13) ( Table 4).
The mean of the duration of suffering from diabetes in patients with arterial insufficiency was 16.3 ± 3.8 years and in patients without failure was 14.2 ± 3.8 years and according to the student's ttest the mean disease duration in the two groups were significantly different (p = 0.005) ( Table 5).  Out of the 120 patients studied, 79 (65.8%) did not suffer from hypertension and hyperlipidemia diseases, 14 (11.7%) suffered from hyperlipidemia, and 27 (22.5%) had high blood pressure (figure 5).
The clinical examination of the patients showed that of 120 patients, 39 (32.5%) suffered from claudication (Fig. 7). Duration of suffering from diabetes in patients with claudication was 17.1 ± 3.4 and in patients without claudication it was 14.5 ± 3.9 years, and according to student's t-test the duration of suffering from diabetes in the two groups had significant difference (p = 0.001) ( Table 6).
The result of the above-mentioned test in 52 patients (43.3%) was positive and in 68 patients (56.7%) was negative (Figure 11). The duration of suffering from diabetes in patients who had a positive test result was 16.7 ± 4.2 and in patients who had a negative test result was 14.3 ± 3.4 years  and according to student's t-test the duration of suffering from diabetes in these two groups was statistically significant (p = 0.001) ( Table 7).

DISCUSSION AND CONCLUSION
The overall objective of this study was to study the presence of arterial insufficiency of the lower extremities in diabetic patients admitted to the surgery department of Golestan Hospital. In this study, those patients were investigated who suffered diabetes but did not suffer any kind of vascular diseases, and have been hospitalized in Golestan Hospital for various reasons such as different surgeries. The minimum and maximum ages observed were 38 and 80. Therefore, in this study, a collection of diabetic patients who are in different age ranges have been examined and there will be no confounding effect of the age on the generalization of the results. Fifty two (43.3%) of the patients were female and 68 of them (56.7%) were male.
The mean age of the above-mentioned men and women were 60.8 ± 10 and 56.8 ± 8.8 years respectively, the mean age of men and women were significantly different. The results of various researches have showed that being male is an effective risk factor for lower extremities ischemia in diabetic patients (11).
The mean duration of suffering from diabetes in these patients was 15.4 ± 3.9 years. Duration of suffering from diabetes is also one of the important risk factors in lower extremities ischemia (1,6, 9,5 and 11). So given that more than 80% of studied patients have been suffering diabetes for more than 10 years, the risk of ischemia and its complications in these patients is very high.
According to the examination performed, 26 patients (21.7%) were without arterial pulse and in 41 patients (34.2%) there was a reduction in pulse rate and in 53 patients (44.2%) arterial pulse was normal. The mean duration of suffering from diabetes in these three groups were significantly different, therefore, according to the results the pulse rate at extremities in more than 55% of patients was abnormal indicating a high percentage of them are probably suffering from ischemia.
Arterial insufficiency in 24 females and 43 males (46.2% vs. 63.2%) was observed. The frequency distributions of the arterial insufficiency had no significant difference with gender.
The arterial insufficiency in diabetic patients had no relationship with their age and gender in this study but it had a significant relationship with the duration of suffering from diabetes. Therefore, the duration of suffering from diabetes can be considered one of the effective factors in the development of vascular lesions and ischemia in patients who have been suffering diabetes for a long time (usually more than 10 years).
Of 120 studied patients, 11.7% suffered hyperlipidemia and 22.5% had high blood pressure. In performing pallor test 49.2% of patients were normal, 32.5% had claudication, and in performing capillary refill test 60% were abnormal. The result of rubor of dependency test in 43.5% of cases was positive and the result of venous filling time test was abnormal in 60% of patients. Cold extremities test was also positive in 65% of patients. Findings of this study can be used to develop pharmaceutical and non-pharmaceutical treatments for different diabetes associated disorders such as wound, neuropathic pains (14)(15)(16)(17).
Given the high prevalence of ischemia in diabetic patients undergoing various surgical procedures, the necessary measures should be taken when performing surgical procedures on these patients. On the other hand, given that chronic lower limb ischemia can be totally asymptomatic and/or be in the form of intermittent claudication, these symptoms may not be fully noticed by the patient or those around them. Therefore, it is necessary for diabetic patients undergoing various surgical procedures, to be considered and investigated regarding vascular problems and the possibility of the presence of ischemia prior to the surgery (5,6). According to the results of this study, tests used in the examination of patients, have been positive in a significant portion of patients, which all of these tests are somewhat helpful in detecting ischemia. Therefore, taking the history of patients and applying these tests in the examining diabetic patients, especially those who are candidates for various surgeries, are very practical and should be performed.

ACKNOWLEDGMENT
The present study was financially supported by Ahvaz Jundishapur University of Medical Sciences (Grant No.: U-88264).