Foot ulcer is a common complication of diabetes. Prognostic Value of Systolic Ankle and Toe Blood Pressure Levels in Outcome of Diabetic Foot Ulcer

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1 Prognostic Value of Systolic Ankle and Toe Blood Pressure Levels in Outcome of Diabetic Foot Ulcer Jan Apelqvist, MD an Castenfors, MD, PhD Jan Larsson, MD Anders Stenstrom, MD, PhD Carl-David Agardh, MD, PhD The prognostic value of distal blood pressure measurements has been studied in 314 consecutive diabetic patients with foot ulcers. Systolic toe blood pressure was measured with a strain-gauge technique, and ankle pressure was measured with strain-gauge or Doppler techniques. Wound healing was defined as intact skin for at least 6 mo. One hundred ninety-seven patients healed primarily, 11 had amputations, and 40 died before healing had occurred. In 294 of 300 patients, it was possible to measure either ankle or toe pressure. Fourteen patients were not available for pressure measurements. Of these, 10 patients healed primarily, and 4 died before healing occurred. Both ankle and toe pressures were higher (P <.001) among patients who healed without amputation compared with those who underwent amputation or died before healing. No differences were seen in ankle or toe pressure levels among those who had amputations or died. No patient healed primarily with an ankle pressure <40 mmhg. An upper limit above which amputation was not required could not be defined. Primary healing was achieved in 139 of 164 patients (85%) with a toe pressure level >45 mmhg, whereas 43 of 117 patients (36%; P <.001) healed without amputation when toe pressure was ^45 mmhg. In conclusion, a combination of ankle and toe pressure measurements is a useful tool to predict primary healing in diabetic foot ulcers. Diabetes Care 12:373-78, 1989 Foot ulcer is a common complication of diabetes mellitus (1-3). In addition to being a devastating situation for the individual, treatment of diabetic foot ulcers is a huge economic burden for the health-care system (1,2,4). Thus, it is of great importance to be able to predict the possibility of primary healing in diabetic patients with foot ulcers. Accelerated atherosclerosis, leading to impaired circulation in the legs, is one of the most important causes of diabetic gangrene, which leads to amputation (1). To evaluate this, measurements of systolic blood pressure have been used with different techniques at different levels of the lower extremity. Ankle blood pressure, with strain-gauge or Doppler technique, is most commonly used. Previous studies have shown that ankle pressure levels <50-80 mmhg indicate poor wound healing or healing only after major amputation (5-15). The predictive value of ankle pressure has, however, not been confirmed by others (16-20). An ischemic index between blood pressure levels in the ankle and brachial arteries has also been used. An index >0.45 was necessary to heal minor amputations in some studies (11,21), but in another study, an index >0.60 was necessary to heal most foot ulcers (2). The most important limitation for the use of ankle pressure measurements, especially in patients with diabetes, is an overestimate of the intra-arterial pressure due to calcification of the medial arterial wall (13,24). This can be avoided when systolic toe pressure is used. Toe pressure levels and up to mmhg have been found to indicate a good prognosis for wound healing, whereas healing did not occur with pressures <20 to mmhg(5,6,8,9,17,23,24). Inotherstudies, however, toe pressure did not predict wound healing (7,19). The results for predictive value of ankle and toe blood pressure in diabetic foot ulcers have thus been conflicting. The aim of this study was to evaluate whether ankle and toe blood pressure could predict primary healing in a large group of diabetic patients with foot ulcers. From the Departments of Internal Medicine, Clinical Physiology, and Orthopedic Surgery, University Hospital, Lund, Sweden. Address correspondence and reprint requests to Jan Apelqvist, MD, University Hospital, S-221, 85 Lund, Sweden. DIABETES CARE, VOL. 12, NO. 6, JUNE

2 ANKLE AND TOE PRESSURE IN DIABETIC FOOT MATERIALS AND METHODS Patients. In a prospective study (planned and implemented 1 July 1983 and continued to 30 June 1987), 314 consecutive patients with diabetes mellitus (156 men, 158 women) referred to the Department of Internal Medicine because of foot ulcers were investigated. Patient characteristics are shown in Table 1. The mean ± SD duration of foot ulcers before the first admission was 14.5 ± 26.1 wk. Ulcer definition. Each patient is represented by one lesion below the ankle. In all cases, the most severe ulcer occurring during the observation period is described. Patients with several concurrent lesions are represented by the lesion with the worst outcome. Wound healing is defined as intact skin for at least 6 mo or, for cases when the patient died within that period, as intact skin at the time of death. On admission, the type of lesion was characterized by the same team of physicians. Lesions are classified according to Wagner (11). In addition, necrosis through the full thickness of the dermis is included in superficial ulcers (Wagner grade 1), which is the most superficial lesion included in the study. Also, minor gangrene (Wagner grade 4) is defined as continuous necrosis of the skin and underlying structures (muscle, tendon, joint, or bone) mainly located on the forefoot. Major gangrene (Wagner grade 5) is defined as continuous necrosis described above but involving most of the foot. Medical treatment. Patients were treated by a foot-care team consisting of a diabetologist, an orthopedic surgeon, an orthotist, a podiatrist, and a diabetes nurse. When necessary, a vascular surgeon was consulted. TABLE 1 Patient characteristics at enrollment Healed primarily Amputated Died n Age (yr) 60 ± ± 13* 74 ± 13* Sex(M/F) 96/101 44/33* 16/24 Duration of diabetes (yr) 12 ± ± ± 10 Treatment Diet Oral agents Insulin Glycosylated hemoglobin (%) 9.0 ± ± ± 2.0 Smoking habits Smokers or exsmokers Never smoked Systolic blood pressure (mmhg) 156 ± ± ± 33 Diastolic blood pressure (mmhg) 84 ± ± Neuropathy * 27 Values are means ± SD. *P <.001 compared with primary healing. Metabolic control was improved when possible (e.g., changing to insulin treatment). Peripheral edema was usually treated with diuretics. Antibiotics were used to treat infection. Proper ulcer dressing was used, foot wear was corrected when required, and external pressure on the lesion was relieved. All patients were scheduled to attend an education program by a podiatrist in preventive foot care. Surgical treatment. Surgical debridement of lesions was performed when required. Amputation was conducted in cases of progressive gangrene, intolerable pain despite analgesic treatment, and toxic or septic conditions not responding to medical treatment. The level of amputation was chosen on clinical grounds as the most distal level possible where healing could be anticipated, minimal requirement being intact skin with no signs of local infection or severe ischemia. Amputation below the ankle is referred to as minor and above the ankle as major amputation. Vascular surgery or angioplasty was performed in 14 patients. Systolic ankle and toe blood pressure measurements. Systolic ankle and toe blood pressure was measured at the patient's first visit and every 6 mo until healing had occurred. In the case of amputation, a preoperative measurement was performed when the previous measurement was 3 mo old, according to Holstein and Lassen (9). In 10 patients, blood pressure measurements were repeated before amputation (n = 5) and because healing had not occurred during the preceding 6 mo (n = 5). In the remaining patients, the pressure measured at entry was used for the evaluation. Patients were investigated in the supine position at room temperature (21-25 C). Systolic blood pressure in the brachial artery was measured in both arms with a conventional mercury sphygmomanometer after a 5- to 10-min rest. Korotkoff phase 1 was used as the systolic blood pressure, and the highest value was used for calculation. Systolic toe pressure was measured with individually fitted occluding cuffs placed around the base of the first toe. In 11 patients, occluding cuffs were placed on the second toe, and in 4 patients, occluding cuffs were placed on the third or fourth toe due to ulcer or previous amputation of the other toes. A thin tube of rubber filled with mercury was placed around the distal part of the toe, and cuff pressure was raised above the systolic pressure. When cuff pressure was lowered, the start of systolic inflow (sensed as a volume increase by the rubber tube) was used as an indicator of the systolic pressure level (strain-gauge technique). Absence oi visible increase in toe volume was assigned a value of 0 mmhg. Toe pressure was measured simultaneously in both legs. Systolic ankle pressure was measured with occluding cuffs measuring 12 x 35 cm and placed around both ankles. When possible, the systolic pressure level was measured with the same rubber tube around a toe as described above. In 65 patients with slow or inconclusive inflow curves, the appearance of Doppler sounds in the tibial or dorsal pedal arteries was used. The artery 374 DIABETES CARE, VOL. 12, NO. 6, JUNE 1989

3 . APELQVIST AND ASSOCIATES HEALED 173 p< p<0.001 AMPU- TATED 65 ANKLE DECEASED 30 HEALED 162 p<0.001 p<0.001 AMPU- TATED 68 TOE DECEASED FIG. 1. Systolic ankle and toe blood pressure levels in patients who healed primarily (O), had amputations ( ), or died before healing occurred ( ). N indicates number of patients. Values are given as means ± SD. NS, not significant. with the best audible sound was used for calculation. For both ankle and toe, the approximate mean of three measurements was used for the calculation. Ischemic ankle and toe indexes are defined as the ratio between ankle or toe piessure and brachial artery pressure, respectively. The occurrence of peripheral neuropathy was measured with vibration-perception threshold with a biothesiometer (Bio-Medical, Newbury, OH). The mean of three measurements in Fig. 1 was used. Values >30 arbitrary units (scale 1-50) was considered indicative of neuropathy. Stable glycosylated hemoglobin (HbA 1c ) was measured with ion-exchange chromatography with microcolumns (Bio-Rad, Richmond, CA). Statistics. Differences were calculated with the Mann- Whitney U test (two tailed) and x 2 -test. RESULTS The type of lesion was characterized according to Wagner as superficial (grade 1, n = 150), deep (grade 2, n = 50), abscess and/or osteomyelitis (grade 3, n = 46), minor gangrene (grade 4, n = 39), or major gangrene (grade 5, n = 29). Primary healing occurred in 63% of patients (n = 197). In some patients, surgical debridement (n = 30), minor bone resection (n = 3), 31 or skin transplantation (n = 7) was performed to achieve healing. Twenty-four percent of patients (n = 77) healed after amputation. The type of lesions that lead to amputation were deep ulcer (n = 2), abscess and/or osteomyelitis (n = 16), minor gangrene (n = 34), or major gangrene (n = 25). The levels of amputation were below the ankle (16 toes and 11 midtarsals), below the knee (n = 45), and above the knee (n = 5). No amputations were performed through the ankle joint. Thirteen percent of patients (n = 40) died before healing had occurred. Of these patients, 8 had amputations before they died. Fourteen patients included in the study were not available for pressure measurements. Of these patients, 10 healed primarily, and 4 died before healing occurred. Sixteen patients who healed primarily (n = 9) or who healed after amputation (n = 7) died within 6 mo after healing had occurred (1-6 mo, median 4 mo). The influence of possible confounding factors on the outcome is shown in Table 1. As expected, patients who had amputations or died were older than those who healed primarily and more often had signs of peripheral neuropathy. Furthermore, there was a male predominance in the amputated group. Otherwise, no differences were seen regarding duration of diabetes, treatment mode, metabolic control as assessed by HbA 1c levels, smoking habits, or blood pressure levels between the three groups. Healing in relation to systolic ankle pressure. Systolic ankle pressure was measured in 268 patients. It was not possible to measure ankle pressure in 22 patients because arteries were incompressible even at a pressure level of >300 mmhg and in 10 cases because of ulcers at the ankles. On a group basis, there was a difference (P <.001) in ankle pressure among patients where primary healing occurred compared with patients where healing occurred after amputation or who died (Fig. 1). No differences were seen in ankle pressure between the two latter groups. There was considerable interindividual variation within each group of patients. As shown in Fig. 2, only 1 patient achieved primary healing with an initial ankle pressure <40 mmhg (P <.001 compared with values >40 mmhg). In this patient, angioplasty was performed before any healing occurred. (Ankle pressure before and after surgery was 30 and 170 mmhg, respectively.) In another patient, reconstructive vascular surgery was performed with ankle pressure before and after surgery 50 and 150 mmhg, respectively. No upper limit of ankle pressure was seen above which amputation was not performed. However, below 80 mmhg, most patients (65%, P <.001) either had amputations or died before healing had occurred. Only 9 of 22 patients with incompressible arteries and 5 of 10 patients with nonmeasurable pressure due to ulcer at the ankle healed primarily (Fig. 2). Healing in relation to systolic toe pressure. Systolic toe pressure was measured in 281 patients. In the other patients, toe pressure could not be measured because the arteries could not be compressed (n = 1) or because DIABETES CARE, VOL. 12, NO. 6, JUNE

4 ANKLE AND TOE PRESSURE IN DIABETIC FOOT ANKLE PRESSURE I- mm Hg INCOMPRESSIBLE ULCER HEALING RATE (%) FIG. 2. Systolic ankle blood pressure in patients who healed primarily (open area), had amputations (hatched area), or died before healing occurred (solid area). Bottom bars indicate patients with incompressible arteries (n = 22) and patients with nonmeasurable pressure because of ulcer at ankle (n = 10). N indicates number of patients. of ulcer (n = 16) or previous amputation (n = 2). Only 5 of 19 healed primarily. In 6 of 300 patients, neither ankle nor toe pressure could be measured. In the remaining patients, there was a difference (P <.001) in pressure levels between the group of patients with primary healing compared with those who underwent amputation or died (Fig. 1). No difference was seen between patients who had amputations or died (Fig. 1). As shown in Fig. 3, primary healing occurred in 9 patients with toe pressure <15 mmhg. Of these patients, 2 underwent vascular surgery or angioplasty before healing occurred. Toe pressure before surgery was 15 and 15 mmhg compared to 90 and 60 mmhg after surgery, respectively. In the remaining 7 patients, primary healing occurred without any surgical or medical u TOE PRESSURE h mm Hg H % N HEALING RATE (%] FIG. 3. Systolic toe blood pressure levels in patients who healed primarily (open area), had amputations (hatched area), or died before healing occurred (solid area). N indicates number of patients. Index > >1.20 ANKLE lllilllliii^^b m H % FIG. 4. Ischemic toe and ankle indexes in patients who healed primarily (open area), had amputations (hatched area), or died before healing occurred (solid area). N indicates number of patients. treatment other than that described above. On the other hand, primary healing was achieved in 85% (n = 164) of patients when toe pressure was >45 mmhg, whereas only 43 of 117 patients (36%, P <.001) healed without amputation when toe pressure was <45 mmhg. Neither ankle nor toe pressure was predictive for the length of time to heal. Ischemic ankle and toe index in relation to primary healing. Ankle and toe indexes showed the same pattern for primary healing as absolute blood pressure levels (Fig. 4; for comparison, see Figs. 2 and 3). Mean ± SD ischemic ankle index was 0.87 ± 0.29 in patients with primary healing (n = 179) compared to 0.55 ± 0.28 in the amputated group (n = 65, P <.001). However, a considerable overlap was seen, with the lowest index being 0.19 in 1 patient with primary healing (after reconstructive vascular surgery). Likewise, a difference in the toe index was seen between patients with primary healing (0.55 ± 0.30, n = 182) and amputation (0.20 ± 0.18, n = 68, P <.001). The lowest toe index with primary healing was zero because 3 patients healed with a toe pressure of 0 mmhg. Systemic blood pressure did not change during the observation period, thus it did not influence the ischemic index. 376 DIABETES CARE, VOL. 12, NO. 6, JUNE 1989

5 ). APELQVIST AND ASSOCIATES DISCUSSION Few studies describe distal blood pressure levels predicting primary healing in diabetic foot ulcers (8,13), whereas most studies have been designed to predict healing after minor amputations (5-7,9-12,14-21,23). Some authors consider ankle pressure valuable (5-15), but others find it to be less useful (16-23). The conflicting results are probably because patients with and without diabetes have been studied (5,7-9,12-15,17-19,23,25); few patient materials are available, especially in the case of low pressure levels (6,7,11,12,14,17,19-22,24,25); and different types of lesions were included (11,16,17,20). Incomplete healing is not infrequent at higher ankle pressure levels. However, in this study, ankle pressure still seems to be a valuable prognostic parameter, because ankle pressure of <40 mmhg was inconsistent with primary healing unless macrocirculation was improved by vascular surgery. Note, however, that nonmeasurable ankle pressure due to incompressible arteries was seen in 22 of our patients, of which only 41% healed primarily. Ankle pressure was measured with the strain-gauge technique, usually on the first toe. Similar pressures are recorded with this technique and inflow measurement with the Doppler technique (26). However, due to local variation in the degree of atherosclerosis often seen in diabetic patients, ankle pressure may differ between the two arteries in the foot (1,2,14). This was the reason why the strain-gauge technique was used to measure ankle pressure in this study. The strain-gauge technique is most often used to measure systolic toe pressure (5-7,9,24,25). The occluding cuff is almost always applied around the first toe. However, in this study and the studies of Holstein and Lassen (5,9), other toes were used. Most patients healed with a toe pressure >30 mmhg, which is in agreement with other studies (5,9,23-25,27). However, in this study, no lower limit for healing was found, and pressure >45 mmhg was necessary for a primary healing rate of 85%. Fifteen patients had amputations with toe pressure >45 mmhg. Only 7 of these were caused by gangrene. Fiftythree amputations were performed in patients with toe pressure <45 mmhg; 45 of the amputations were due to gangrene. Other studies have shown somewhat different results that may be explained by differences in study design, materials, and the fact that primary healing in this study did not include minor amputations (6-8,1 7,19,23). In this study, only 4 of 31 patients with ankle pressure <80 mmhg and in 1 of 21 patients with toe pressure ^15 mmhg healed after an amputation below the ankle. This indicates that different pressure levels have to be used to predict primary healing compared to healing after minor amputations. Many authors have used ischemic ankle and/or toe indexes (10, 11,14,15,21,22,24,25,27). However, it is questionable to use this index to predict healing in diabetic patients with foot ulcers because incompressible arteries might give false high values both in the arm and ankle. Furthermore, compared with absolute pressure levels, which especially in the toe give additional information of the perfusion pressure level in the foot, neither the ankle nor toe index contributed any additional information to assist physicians in medical decision making. When comparing ankle and toe pressure in predicting primary healing, ankle pressure provided a certain level below which no primary healing was found. Toe pressure also provided valuable information, because an upper level was found above which amputation seldom was required. In conclusion, a combination of ankle and toe pressure measurements give valuable information to predict primary healing in diabetic foot ulcers. ACKNOWLEDGMENTS This work was supported by the Swedish Medical Research Council Grant REFERENCES 1. 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