Ankle Brachial Index and Transcutaneous Partial Pressure of Oxygen as predictors of wound healing in diabetic foot ulcers
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1 The Journal of Diabetic Foot Complications Ankle Brachial Index and Transcutaneous Partial Pressure of Oxygen as predictors of wound healing in diabetic foot ulcers Authors: Lalithambika CV 1, Nisha B 2, Saraswathy L 1, Ajit Kumar Varma 3, Amrutha Jose 4, Sundaram KR 4 The Journal of Diabetic Foot Complications, 2014; Volume 6, Issue 2, No. 4, Pages All rights reserved. Abstract: Peripheral Occlusive Vascular Disease impairs the healing process in diabetic foot ulcers. Ankle Brachial Index is the conventional method of assessing POVD and Transcutaneous Partial Pressure of Oxygen. It is a relatively new measure of assessing microvascular circulation. Our aim was to compare and contrast the utility of ABI and in predicting wound healing in diabetic foot ulcers. The study included 118 diabetic foot ulcer patients who had their ABI and measured. A handheld doppler device measured the ABI, and an electrochemical transducer measured the. Wound outcome was classified as either healed or not healed. The mean ABI in the healed group was 0.96±0.24 and 0.61±0.27 (p<0.001) in the not healed group. The mean in the healed group was 33.77±15.51 and 23.29±14.77 (p=0.002) in the not healed group. The agreement rate of ABI with was 59.3%. More than 90% of ulcers with normal ABI and/or healed. With aggressive management of POVD a good percent of wounds with abnormal ABI and/or also healed. By plotting the ROC curve, in our population, an ABI value of 0.77 was found to have 80% sensitivity and 75% specificity, and a value of 22.5 mm Hg was found to have 74.4% sensitivity and 53.6% specificity in predicting wound healing. Both ABI and measured different aspects of POVD and were complementary in predicting wound healing in diabetic foot ulcers. The optimal cut-off values for both measures for our population were also defined. Key words: Ankle Brachial Index, Diabetic Foot Ulcer, Peripheral Occlusive Vascular Disease, Transcutaneous Partial Pressure of Oxygen Corresponding author Dr. CV Lalithambika MD Resident Department of Physiology PIN cvlalithambika@aims.amrita.edu INTRODUCTION Affiliations 1 Department of Physiology 2 Department of Endocrinology 3 Department of Podiatry 4 Department of Biostatistics Having a diabetic foot ulcer is a major cause of morbidity for diabetic patients. Almost 50% of diabetic ulcers are ischemic in origin. 1 Peripheral Occlusive Vascular Disease (POVD) impairs the healing process in diabetic foot ulcers. Ankle Brachial Index (ABI) is the conventional method of assessing POVD and its influence on wound healing; 2,3 however, it has certain limitations. Diabetic patients have microvascular and small vessel diseases which are not reliably measured by ABI. ABI can be unreliable in patients with calcification of the walls of arteries, which make vessels incompressible and can result in abnormally high values. 4 is a noninvasive measure of local arterial blood flow and skin oxygenation that predicts chances of wound healing. values identify patients with subclinical microvascular impairment. 5 Since wound healing depends on an adequate supply of oxygen to the tissues, measurement of, which is a direct measure of the tissue oxygen partial pressure, may be a more reliable method 6,7,8 to predict wound healing. measurements have also been used to determine the amputation risk in non-healing ulcers 9 and the amputation levels. 10 It also helps to heal surgical wounds. 11,12 54
2 The Journal of Diabetic Foot Complications, 2014; Volume 6 Issue 2, No. 4, Pages Studies have shown that is related to the degree of ischemia. 13 Some studies have shown that ABI has significant limitations for diagnosing and treating critical limb ischemia patients compared with. 14 Studies have defined different cut-off minimum values for ABI and in predicting POVD and wound healing. The cut-off which best predict wound healing in our population is unknown. The primary study objectives were to identify 1) the association of ABI and, with wound outcomes (healed and not healed) in diabetic foot ulcers and 2) the comparative utility of using ABI and as a marker in predicting wound healing in diabetic ulcers. The secondary study objective was to attempt to define ABI and cut-off values which predict wound healing in our population. PATIENTS AND METHODS This was a retrospective cross-sectional study. Based on the results of the association between ABI and with wound healing 15 and with 99% confidence and 90% power, the minimum sample size computed was highest in the case of the ABI (40 patients). However, we also included 118 Type 2 diabetic patients with diabetic foot ulcers who visited the podiatry outpatient department of a tertiary referral university teaching hospital in South India. Study participants ABI and were measured. If patients were thought to have POVD, by either ABI or, an angiogram was performed. If possible, revascularization was also performed. In addition, all patients underwent routine treatment for diabetic foot ulcers including antibiotic treatment, surgical and chemical debridement, off-loading, and management of diabetes and co-morbid conditions. A handheld doppler device measured the ABI. A blood pressure cuff was placed on the upper arm and inflated until the doppler device detected no brachial pulse. The cuff was then slowly deflated until a doppler-detected pulse, systolic pressure, returned. This maneuver was repeated on the leg, with the cuff wrapped around the distal calf and the doppler device placed over the dorsalis pedis or posterior tibia artery. The ankle systolic pressure divided by the brachial systolic pressure yielded the ABI. The highest arm pressure was used as the denominator. A normal ABI range was between 0.91 and A resting ABI of 0.9 was noted as abnormal. 2 An ABI value greater than 1.3 suggested calcification of the walls of the arteries and incompressible vessels. 16 These patients were excluded from the study. is a test that uses oxygen sensing electrodes to measure the delivery of oxygen to the skin tissue. An electrochemical transducer was fixed to the skin of the dorsum of the foot with adhesive rings and contact liquid (Figure 1). The patient refrained from smoking and drinking coffee for at least two hours before the investigation. Readings were taken in the supine position. Values greater than 40 mm Hg were defined as normal and usually associated with good healing, while 40 mm Hg was defined as low with poor chances of healing. 17 Figure 1. being recorded with electrodes Wound outcome was classified as healed or not healed. A wound was considered healed if it underwent complete epithelialization or skin grafting at the site of surgical debridement or local amputation. A wound was considered not healed if a major amputation was performed or if the patient died from an associated foot infection
3 The Journal of Diabetic Foot Complications, 2014; Volume 6, Issue 2, No. 4, Pages STATISTICAL METHODS We used the following three statistical methods to analyze the data. 1. T-test: To test the statistical significance of the difference in mean values of ABI and between the healed and not healed groups. 2. Chi-Squared with Yates Continuity Correction: To test the statistical significance of the association of ABI and, categorized as normal and abnormal with wound healing. 3. Validity Parameters: Sensitivity and specificity tests were computed for ABI and with respect to healing status. Based on the data collected using an ROC curve, an attempt was made to find appropriate cut-off points for ABI and with respect to healing status. RESULTS The study included 118 patients who satisfied the inclusion criteria. Diabetic foot ulcers healed in 90 patients and did not heal in the remaining 28 patients. Baseline characteristics were similar in the healed and not healed groups and among the co-morbidities present; the presence of nephropathy and/or renal failure alone was significantly more prevalent in the not healed group. As Table 1 shows, the mean ABI in the healed population was 0.96±0.24 and 0.61±0.27 (p<0.001) in the not healed group. The mean in the healed group was 33.77±15.51 and 23.29±14.77 (p=0.002) in the not healed group. ABI and, when cross tabulated, showed that 38.8% of people with a normal ABI had a normal, and the remaining 61.2% had an abnormal. 13.7% of patients with an abnormal ABI had a normal, and 86.3% with an abnormal ABI had an abnormal. 78.8% of patients with a normal had a normal ABI, and the remaining 21.2% had abnormal ABIs. Among those with an abnormal, 48.2% had a normal ABI and 51.8% had abnormal ABIs. Overall, in the total population, 22% had both a normal ABI and ; 37.3% had both an abnormal ABI and ; 34.8% had an abnormal with a normal ABI; and 5.9% had a normal with an abnormal ABI. Thus, the percentage agreement rate of ABI and was 59.3%, and the disagreement rate was 40.7%. Table 1. Comparison of ABI and between healed and not healed groups Variable Healed n=90 Not Healed n=28 ABI 0.96± ±0.27 <0.001* 33.77± ± * Out of 90 patients whose ulcers healed, 61 (67.8%) showed normal ABIs, and 31 (34.4%) showed a normal. Of the 28 patients whose ulcers did not heal 22 (78.6%) showed an abnormal ABI, and 26 (92.9%) showed an abnormal. In this category, only 6 (21.4%) showed a normal ABI and 2 (7.1%) showed a normal. Table 2 shows the association of ABI, normal and abnormal, with wound outcomes categorized as healed and not healed. Table 3 shows the association of, normal and abnormal, with wound outcomes categorized as healed and not healed. Ninety-one percent of wounds with a normal ABI and 93.9% with a normal healed, whereas 56.9% of those with an abnormal ABI and 69.4% with an abnormal also healed (Figures 2 and 3). Table 2. Association of ABI (normal and abnormal) with wound outcomes categorized as healed and not healed Outcome Normal ( ) n=67 ABI ( 0.9) n=51 Healed 61 (91%) 29 (57%) Not Healed 6 (9%) 22 (43%) <0.001* 56
4 The Journal of Diabetic Foot Complications, 2014; Volume 6 Issue 2, No. 4, Pages Table 3. Association of (normal and abnormal) with wound outcomes categorized as healed and not healed Outcome Normal (> 40 mm Hg) n=33 ( 40 mm Hg) n=85 Healed 31 (94%) 59 (69%) Not Healed 2 (6%) 26 (31%) =0.001* By plotting a ROC curve, in our population an ABI value of 0.77 was found to have 80% sensitivity and 75% specificity, and a value of 22.5 was found to have 74.4% sensitivity and 53.6% specificity in predicting wound healing (Figure 4). Using a cut-off of 0.77 for ABI, 91% of wounds with an ABI > 0.77 healed while the rest did not heal, whereas 46% of those with ABI 0.77 also healed. Similarly with a of >22.5, 84% healed and the remaining did not heal, whereas with a 22.5, 61% healed and 39% did not heal. Figure 2. Outcomes when ABI is normal and abnormal Figure 4. ROC curve In Table 4, multivariate logistic regression analysis showed that for an odds ratio of 6.21, an ulcer remain unhealed if ABI was abnormal and 4.44 if was abnormal. Table 4. Results of the multivariate logistic regression analysis (ABI and against the outcome of nonhealing of ulcer) Variable ABI Odds ratio (95% confidence interval) 6.21 (2.23, 17.35) <0.001* Figure 3. Outcomes when is normal and abnormal 4.44 (0.93, 21.13) = 0.061** **Borderline significant 57
5 The Journal of Diabetic Foot Complications, 2014; Volume 6, Issue 2, No. 4, Pages DISCUSSION In this study of 118 patients with diabetic foot ulcers, the utility of ABI and in predicting wound healing was assessed. The mean ABI and in the healed and not healed group were significantly different (p<0.001 and p=0.002 respectively). The agreement rate between ABI and was 59.3%. If either the ABI and/or was normal, there was more than a 90% chance of wound healing. Though 0.9 is the conventionally used cut-off value for predicting POVD by ABI, the ROC curve in our study population showed an ABI of 0.77 to have the optimal sensitivity and specificity in predicting wound healing. For, the cut-off in our population with optimal sensitivity and specificity was 22.5 mm Hg. The study by Majid Kalani et al. showed that was a better predictor for ulcer healing than toe blood pressure in diabetic patients with chronic foot ulcers. 15 The cut-off level used for in this study was 25 mm Hg. A study by Zimny et al. also emphasized to be a useful tool in screening Type 2 diabetic patients for the foot at risk. 19 A study done in the University Hospital of Tubingen, Germany evaluated whether can be used to predict the risk of non-healing and amputation in diabetic foot ulcer patients with non-palpable pedal pulses. Of the 141 patients studied, wounds associated with a of less than 20 mm Hg demonstrated a significantly decreased probability of healing compared with those associated with a greater than 40 mm Hg (p=0.008). 17 The Eurodiale study focused on outcome and determinants of outcome in diabetic foot disease. 20 This study concluded that the predictors of healing differ between patients with and without peripheral arterial disease, and infections had a negative impact on healing. Study results showed that if the ABI was abnormal there was a greater chance that the was also abnormal, whereas if the ABI was normal the may have been normal or abnormal. This was well explained by the fact that ABI measures circulation in medium sized vessels which, if low, will mostly lead to a lower capillary blood flow and low transcutaneous pressure of oxygen. Even if ABI was normal there may have been microvascular disease in diabetes, which was evident from the higher percentage of abnormal even if the ABI was normal. If ABI and/or were normal there was more than 90% chance that wounds would heal. Good healing percentages in wounds where ABI and/or was abnormal was a result of aggressive management of POVD and other aspects of the diabetic foot ulcer. This routinely occured in a highly specialized podiatry unit where the limb salvage rate was very high. The revascularization rate, and its success, were not analyzed in this study. Both ABI and were complementary and measured different aspects of POVD; therefore, both were useful in predicting wound healing. All patients with abnormal ABI and needed aggressive management of their POVD to improve the wound outcomes. An angiogram, which is the gold standard for assessing POVD, was not able to be done on all patients because of its invasive nature and cost factors. Future studies on larger populations may yield more information regarding equal or better predictability of one test over the other. CONCLUSION Both ABI and measure different aspects of POVD and are complementary in predicting wound healing in diabetic foot ulcers. In our study, the optimal cut-off values of these measures to predict wound healing was also defined. 58
6 The Journal of Diabetic Foot Complications, 2014; Volume 6 Issue 2, No. 4, Pages References 1. Gerassimidis T, Karkos CD, Karamanos D, et al: Current endovascular management of the ischaemic diabetic foot. Hippokratia. 2008Apr;12(2): Potier L, Abi Khalil C, Mohammedi K, et al. Use and utility of Ankle Brachial Index in patients with Diabetes. Eur J Vasc Endovasc Surg. 2011Jan;41(1): doi: /j.ejvs Epub 2010Nov 20. Review. 3. Chang CH, Peng YS, Chang CC, et al. Useful screening tools for preventing foot problems of diabetics in rural areas: a cross-sectional study. BMC public health. 2013Jun27;13(1):612. [Epub ahead of print] 4. Aerden D, Massaad D, von Kemp K, et al. The Ankle-Brachial index and the Diabetic foot: A Troublesome Marriage. Ann Vasc Surg. 2011Aug;25(6): doi: /j.avsg Epub2011Apr de Meijer VE, Van't Sant HP, Spronk S, et al. Reference value of transcutaneous oxygen measurement in diabetic patients compared with non diabetic patients. J Vasc Surg. 2008Aug;48(2): doi: /j.jvs Epub 2008Jun Barnikol WK, Pötzschke H: A novel, non-invasive diagnostic clinical procedure for the determination of an oxygenation status of chronic lower leg ulcers using peri-ulceral transcutaneous oxygen partial pressure measurements: results of its application in chronic venous insufficiency (CVI). Ger Med Sci. 2012;10:Doc11. doi: / Epub 2012Jun Hutchison DC, Rocca G, Honeybourne D. Estimation of arterial oxygen tension in adult subjects using a transcutaneous electrode. Thorax. 1981Jun;36(6): Lalka SG, Malone JM, Anderson GG, et al. Transcutaneous oxygen and carbon dioxide pressure monitoring to determine severity of limb ischemia and to predict surgical outcome. J Vasc Surg. 1988Apr;7(4): Carter SA, Tate RB. The relationship of the transcutaneous oxygen tension, pulse waves and systolic pressures to the risk for limb amputation in patients with peripheral arterial disease and skin ulcers or gangrene. Int Angiol. 2006Mar;25(1): Bongard O, Krähenbühl B: Predicting amputation in severe ischaemia. The value of transcutaneous PO2 measurement. J Bone Joint Surg Br. 1988May;70(3): Dowd GS. Predicting stump healing following amputation for peripheral vascular disease using the transcutaneous oxygen monitor. Ann R Coll Surg Engl. 1987Jan;69(1): Christensen KS, Klarke M. Transcutaneous oxygen measurement in peripheral occlusive disease. An indicator of wound healing in leg amputation. J Bone Joint Surg Br. 1986May;68(3): Dowd GS, Linge K, Bentley G. Measurement of transcutaneous oxygen pressure in normal and ischaemic skin. J Bone Joint Surg Br. 1983Jan;65(1): Pardo M, Alcaraz M, Bernal FL, et al. A solution to ankle-brachial index limitations in peripheral transluminal angioplasty. Radiol Med. 2013May 28. [Epub ahead of print] 15. Kalani M, Brismar K, Fagrell B, et al. Transcutaneous oxygen tension and toe blood pressure as predictors for outcome of diabetic foot ulcers. Diabetes Care. 1999Jan;22(1): Andrade JL, Schlaad SW, Koury Junior A, et al. Prevalence of lower limb occlusive vascular disease in outclinic diabetic patients. Int Angiol. 2004Jun;23(2): Ladurner R, Küper M, Königsrainer I, et al. Predictive value of routine transcutaneous tissue oxygen tension ( ) measurement for the risk of non-healing and amputation in diabetic foot ulcer patients with non-palpable pedal pulses. Med Sci Monit. 2010Jun;16(6):CR Sun JH, Tsai JS, Huang CH, et al. Risk factors for lower extremity amputation in diabetic foot disease categorized by Wagner classification. Diabetes Res Clin Pract. 2012Mar;95(3): doi: /j.diabres Epub 2011Nov Zimny S, Dessel F, Ehren M, et al. Early detection of microcirculatory impairment in diabetic patients with foot at risk. Diabetes Care. 2001Oct;24(10): Prompers L, Schaper N, Apelqvist J, et al. Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study. Diabetologia. 2008May;51(5): Epub 2008Feb
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