Performance of non-invasive bedside vascular testing in the prediction of wound healing or amputation among people with foot ulcers in diabetes: A systematic review.

amputation diabetes diabetic foot foot ulcer peripheral artery disease prognosis

Journal

Diabetes/metabolism research and reviews
ISSN: 1520-7560
Titre abrégé: Diabetes Metab Res Rev
Pays: England
ID NLM: 100883450

Informations de publication

Date de publication:
26 Jul 2023
Historique:
received: 07 07 2023
accepted: 10 07 2023
medline: 26 7 2023
pubmed: 26 7 2023
entrez: 26 7 2023
Statut: aheadofprint

Résumé

The presence of peripheral artery disease (PAD) confers a significantly increased risk of failure to heal and major lower limb amputation for people with diabetes-related foot ulcer (DFU). Determining performance of non-invasive bedside tests for predicting likely DFU outcomes is therefore key to effective risk stratification of patients with DFU and PAD to guide management decisions. The aim of this systematic review was to determine the performance of non-invasive bedside tests for PAD to predict DFU healing, healing post-minor amputation, or need for minor or major amputation in people with diabetes and DFU or gangrene. A database search of Medline and Embase was conducted from 1980 to 30 November 2022. Prospective studies that evaluated non-invasive bedside tests in patients with diabetes, with and without PAD and foot ulceration or gangrene to predict the outcomes of DFU healing, minor amputation, and major amputation with or without revascularisation, were eligible. Included studies were required to have a minimum 6-month follow-up period and report adequate data to calculate the positive likelihood ratio (PLR) and negative likelihood ratio for the outcomes of DFU healing, and minor and major amputation. Methodological quality was assessed using the Quality in Prognosis Studies tool. From 14,820 abstracts screened 28 prognostic studies met the inclusion criteria. The prognostic tests evaluated by the studies included: ankle-brachial index (ABI) in 9 studies; ankle pressures in 10 studies, toe-brachial index in 4 studies, toe pressure in 9 studies, transcutaneous oxygen pressure (TcPO Prognostic capacity of bedside testing for DFU healing and amputation is variable. A toe pressure ≥30 mmHg, TcPO

Identifiants

pubmed: 37493206
doi: 10.1002/dmrr.3701
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3701

Informations de copyright

© 2023 The Authors. Diabetes/Metabolism Research and Reviews published by John Wiley & Sons Ltd.

Références

De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol. 2000;130(5):963-974. https://doi.org/10.1038/sj.bjp.0703393
Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis. JAMA, J Am Med Assoc. 2002;287(19):2570-2581. https://doi.org/10.1001/jama.287.19.2570
Leibson CL, Ransom JE, Olson W, Zimmerman BR, O’Fallon WM, Palumbo PJ. Peripheral arterial disease, diabetes, and mortality. Diabetes Care. 2004;27(12):2843-2849. https://doi.org/10.2337/diacare.27.12.2843
Aerden D, Massaad D, Von Kemp K, et al. The ankle-brachial index and the diabetic foot: a troublesome marriage. Ann Vasc Surg. 2011;25(6):770-777. https://doi.org/10.1016/j.avsg.2010.12.025
Jude EB, Oyibo SO, Chalmers N, Boulton AJM. Peripheral arterial disease in diabetic and nondiabetic patients. Diabetes Care. 2001;24(8):1433-1437. https://doi.org/10.2337/diacare.24.8.1433
Aboyans V, Criqui MH, Abraham P, et al. Measurement and interpretation of the ankle-brachial index: a scientific statement from the American Heart Association. Circulation. 2012;126(24):2890-2909. https://doi.org/10.1161/cir.0b013e318276fbcb
van Netten JJ, Baba M, Lazzarini PA. Epidemiology of diabetic foot disease and diabetes-related lower-extremity amputation in Australia: a systematic review protocol. Syst Rev. 2017;6(1):101. https://doi.org/10.1186/s13643-017-0488-5
Kurowski JR, Nedkoff L, Schoen DE, Knuiman M, Norman PE, Briffa TG. Temporal trends in initial and recurrent lower extremity amputations in people with and without diabetes in Western Australia from 2000 to 2010. Diabetes Res Clin Pract. 2015;108(2):280-287. https://doi.org/10.1016/j.diabres.2015.02.008
Boyko EJ. Ruling out or ruling in disease with the most sensitive or specific diagnostic test: short cut or wrong turn? Med Decis Mak. 1994;14(2):175-179. https://doi.org/10.1177/0272989x9401400210
Deeks JJ. Systematic reviews in health care: systematic reviews of evaluations of diagnostic and screening tests. Bmj. 2001;323(7305):157-162. https://doi.org/10.1136/bmj.323.7305.157
Jaeschke R, Guyatt GH, Sackett DL. Users' guides to the medical literature. III. How to use an article about a diagnostic test. B. What are the results and will they help me in caring for my patients? The Evidence-Based Medicine Working Group. JAMA. 1994;271(9):703-707. https://doi.org/10.1001/jama.271.9.703
McGee S. Simplifying likelihood ratios. J Gen Intern Med. 2002;17(8):646-649. https://doi.org/10.1046/j.1525-1497.2002.10750.x
Hayden JA, van der Windt DA, Cartwright JL, Côté P, Bombardier C. Assessing bias in studies of prognostic factors. Ann Intern Med. 2013;158(4):280-286. https://doi.org/10.7326/0003-4819-158-4-201302190-00009
Harbour R, Miller J. A new system for grading recommendations in evidence based guidelines. Bmj. 2001;323(7308):334-336. https://doi.org/10.1136/bmj.323.7308.334
Huguet A, Hayden JA, Stinson J, et al. Judging the quality of evidence in reviews of prognostic factor research: adapting the GRADE framework. Syst Rev. 2013;2(1):71. https://doi.org/10.1186/2046-4053-2-71
Fujii M, Yamada A, Yamawaki K, et al. Predictive factors for limb salvage and foot ulcer recurrence in patients with chronic limb-threatening ischemia after multidisciplinary team treatment: a 6-year Japanese single-center study. Int J Low Extrem Wounds. 2021:15347346211041429. https://doi.org/10.1177/15347346211041429
Wallin L, Björnsson H, Stenström A. Fluorescein angiography for predicting healing of foot ulcers. Acta Orthop Scand. 1989;60(1):40-44. https://doi.org/10.3109/17453678909150089
Kawai M, Mihara S, Takahagi S, Iwamoto K, Hiragun T, Hide M. Evaluation of skin perfusion pressure to assess refractory foot ulcers. J Wound Care. 2017;26(5):267-270. https://doi.org/10.12968/jowc.2017.26.5.267
Apelqvist J, Castenfors J, Larsson J, Stenstrom A, Agardh CD. Prognostic value of systolic ankle and toe blood pressure levels in outcome of diabetic foot ulcer. Diabetes Care. 1989;12(6):373-378. https://doi.org/10.2337/diacare.12.6.373
Apelqvist J, Elgzyri T, Larsson J, Londahl M, Nyberg P, Thorne J. Factors related to outcome of neuroischemic/ischemic foot ulcer in diabetic patients. J Vasc Surg. 2011;53(6):1582-1588.e2. https://doi.org/10.1016/j.jvs.2011.02.006
Apelqvist J, Larsson J, Agardh CD. The importance of peripheral pulses, peripheral oedema and local pain for the outcome of diabetic foot ulcers. Diabet Med. 1990;7(7):590-594. https://doi.org/10.1111/j.1464-5491.1990.tb01454.x
Chetpet A, Dikshit B, Phalgune D. Evaluating a risk score for lower extremity amputation in patients with diabetic foot infections. J Clin Diagn Res. 2018;12(10):PC14-PC9. https://doi.org/10.7860/jcdr/2018/36712.12214
Elgzyri T, Apelqvist J, Lindholm E, Orneholm H, Annersten Gershater M. Healing below the ankle is possible in patients with diabetes mellitus and a forefoot gangrene. SAGE Open Med. 2021;9:20503121211029180. https://doi.org/10.1177/20503121211029180
Elgzyri T, Larsson J, Thorne J, Eriksson KF, Apelqvist J. Outcome of ischemic foot ulcer in diabetic patients who had no invasive vascular intervention. Eur J Vasc Endovasc Surg. 2013;46(1):110-117. https://doi.org/10.1016/j.ejvs.2013.04.013
Gershater M, Löndahl M, Nyberg P, et al. Complexity of factors related to outcome of neuropathic and neuroischaemic/ischaemic diabetic foot ulcers: a cohort study. Diabetologia. 2009;52(3):398-407. https://doi.org/10.1007/s00125-008-1226-2
Hering J, Angelkort B, Keck N, Wilde J, Amann B. Long-term outcome of successful percutaneous transluminal angioplasty of the fibular artery in diabetic foot syndrome and single-vessel calf perfusion depends on doppler wave pattern at the forefoot. Vasa. 2010;39(1):67-75. https://doi.org/10.1024/0301-1526/a000007
Larsson J, Apelqvist J, Castenfors J, Agardh CD, Stenstrom A. Distal blood pressure as a predictor for the level of amputation in diabetic patients with foot ulcer. Foot Ankle. 1993;14(5):247-253. https://doi.org/10.1177/107110079301400502
Tsai C.-Y, Chu S.-Y, Wen Y.-W, et al. The value of Doppler waveform analysis in predicting major lower extremity amputation among dialysis patients treated for diabetic foot ulcers. Diabetes Res Clin Pract. 2013;100(2):181-188. https://doi.org/10.1016/j.diabres.2013.03.017
Yang C, Weng H, Chen L, et al. Transcutaneous oxygen pressure measurement in diabetic foot ulcers: mean values and cut-point for wound healing. J Wound Ostomy Continence Nurs. 2013;40(6):585-589. https://doi.org/10.1097/won.0b013e3182a9a7bf
Lopez-Moral M, Garcia-Alvarez Y, Molines-Barroso RJ, Tardaguila-Garcia A, Garcia-Madrid M, Lazaro-Martinez JL. A comparison of hyperspectral imaging with routine vascular noninvasive techniques to assess the healing prognosis in patients with diabetic foot ulcers. J Vasc Surg. 2022;75(1):255-261. https://doi.org/10.1016/j.jvs.2021.07.123
Manu CA, Slim H, Huang D, et al. Isolated low toe-brachial index is associated with increased mortality and morbidity: a retrospective cohort study. J Wound Care. 2021;30(1):65-73. https://doi.org/10.12968/jowc.2021.30.1.65
Mennes OA, van Netten JJ, van Baal JG, Slart RH, Steenbergen W. The association between foot and ulcer microcirculation measured with laser speckle contrast imaging and healing of diabetic foot ulcers. J Clin Med. 2021;10(17):3844. https://doi.org/10.3390/jcm10173844
Padberg FT, Back TL, Thompson PN, Hobson RW, 2nd. Transcutaneous oxygen (TcPO2) estimates probability of healing in the ischemic extremity. J Surg Res. 1996;60(2):365-369. https://doi.org/10.1006/jsre.1996.0059
Castronuovo JJ, Jr., Adera HM, Smiell JM, Price RM. Skin perfusion pressure measurement is valuable in the diagnosis of critical limb ischemia. J Vasc Surg. 1997;26(4):629-637. https://doi.org/10.1016/s0741-5214(97)70062-4
Holstein P, Lassen NA. Healing of ulcers on the feet correlated with distal blood pressure measurements in occlusive arterial disease. Acta Orthop Scand. 1980;51(6):995-1006. https://doi.org/10.3109/17453678008990906
Nouvong A, Hoogwerf B, Mohler E, Davis B, Tajaddini A, Medenilla E. Evaluation of diabetic foot ulcer healing with hyperspectral imaging of oxyhemoglobin and deoxyhemoglobin. Diabetes Care. 2009;32(11):2056-2061. https://doi.org/10.2337/dc08-2246
Kalani M, Brismar K, Fagrell B, Ostergren J, Jörneskog G. Transcutaneous oxygen tension and toe blood pressure as predictors for outcome of diabetic foot ulcers. Diabetes Care. 1999;22(1):147-151. https://doi.org/10.2337/diacare.22.1.147
Ladurner R, Kuper M, Konigsrainer I, et al. Predictive value of routine transcutaneous tissue oxygen tension (tcpO2) measurement for the risk of non-healing and amputation in diabetic foot ulcer patients with non-palpable pedal pulses. Med Sci Monit. 2010;16(6):CR273-7.
Zhang S, Wang S, Xu L, He Y, Xiang J, Tang Z. Clinical outcomes of transmetatarsal amputation in patients with diabetic foot ulcers treated without revascularization. Diabetes Ther. 2019;10(4):1465-1472. https://doi.org/10.1007/s13300-019-0653-z
Brechow A, Slesaczeck T, Münch D, et al. Improving major amputation rates in the multicomplex diabetic foot patient: focus on the severity of peripheral arterial disease. Ther Adv Endocrinol Metabol. 2013;4(3):83-94. https://doi.org/10.1177/2042018813489719
Bunt TJ, Holloway GA. TcPO2 as an accurate predictor of therapy in limb salvage. Ann Vasc Surg. 1996;10(3):224-227. https://doi.org/10.1007/bf02001886
Faris I, Duncan H, Young C. Factors affecting outcome of diabetic patients with foot ulcers or gangrene. J Cardiovasc Surg. 1988;29(6):736-740.
Bishara RA, Taha W, Akladious I, Allam MA. Ankle peak systolic velocity: new parameter to predict nonhealing in diabetic foot lesions. Vascular. 2009;17(5):264-268. https://doi.org/10.2310/6670.2009.00032
Niazi K, Khan TH, Easley KA. Diagnostic utility of the two methods of ankle brachial index in the detection of peripheral arterial disease of lower extremities. Catheter Cardiovasc Interv. 2006;68(5):788-792. https://doi.org/10.1002/ccd.20906
Salaun P, Desormais I, Lapebie F.-X, et al. Comparison of ankle pressure, systolic toe pressure, and transcutaneous oxygen pressure to predict major amputation after 1 year in the COPART cohort. Angiology. 2019;70(3):229-236. https://doi.org/10.1177/0003319718793566
Sharma S, Schaper N, Rayman G. Microangiopathy: is it relevant to wound healing in diabetic foot disease? Diabetes Metab Res Rev. 2020;36(Suppl 1):e3244. https://doi.org/10.1002/dmrr.3244
Chao CY, Cheing GL. Microvascular dysfunction in diabetic foot disease and ulceration. Diabetes/Metabol Res Rev. 2009;25(7):604-614. https://doi.org/10.1002/dmrr.1004
Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Diabetic neuropathic foot ulcers: the association of wound size, wound duration, and wound grade on healing. Diabetes Care. 2002;25(10):1835-1839. https://doi.org/10.2337/diacare.25.10.1835
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. 2008;51(5):747-755. https://doi.org/10.1007/s00125-008-0940-0
Zhang Y, Cramb S, McPhail SM, et al. Factors associated with healing of diabetes-related foot ulcers: observations from a large prospective real-world cohort. Diabetes Care. 2021;44(7):e143-e5. https://doi.org/10.2337/dc20-3120
Simons JP, Goodney PP, Nolan BW, et al. Failure to achieve clinical improvement despite graft patency in patients undergoing infrainguinal lower extremity bypass for critical limb ischemia. J Vasc Surg. 2010;51(6):1419-1424. https://doi.org/10.1016/j.jvs.2010.01.083
Mills JL, Sr, Conte MS, Armstrong DG, et al. The Society for Vascular Surgery lower extremity threatened limb classification system: risk stratification based on wound, ischemia, and foot infection (WIfI). J Vasc Surg. 2014;59(1):220-234.e2. https://doi.org/10.1016/j.jvs.2013.08.003
Noronen K, Saarinen E, Albäck A, Venermo M. Analysis of the elective treatment process for critical limb ischaemia with tissue loss: diabetic patients require rapid revascularisation. Eur J Vasc Endovasc Surg. 2017;53(2):206-213. https://doi.org/10.1016/j.ejvs.2016.10.023
Elgzyri T, Larsson J, Nyberg P, Thörne J, Eriksson K.-F, Apelqvist J. Early revascularization after admittance to a diabetic foot center affects the healing probability of ischemic foot ulcer in patients with diabetes. Eur J Vasc Endovasc Surg. 2014;48(4):440-446. https://doi.org/10.1016/j.ejvs.2014.06.041
Jeffcoate WJ, Bus SA, Game FL, et al. Reporting standards of studies and papers on the prevention and management of foot ulcers in diabetes: required details and markers of good quality. lancet Diabetes and Endocrinol. 2016;4(9):781-788. https://doi.org/10.1016/s2213-8587(16)30012-2

Auteurs

Vivienne Chuter (V)

School of Health Sciences, Western Sydney University, Campbelltown, Sydney, Australia.

Nicolaas Schaper (N)

Division of Endocrinology, Department of Internal Medicine, MUMC+, Maastricht, The Netherlands.

Robert Hinchliffe (R)

Bristol Centre for Surgical Research, University of Bristol, Bristol, UK.

Joseph Mills (J)

Baylor College of Medicine, Houston, Texas, USA.

Nobuyoshi Azuma (N)

Asahikawa Medical University, Asahikawa, Hokkaido, Japan.

Christian-Alexander Behrendt (CA)

Department of Vascular and Endovascular Surgery, Asklepios Clinic Wandsbek, Asklepios Medical School, Hamburg, Germany.

Edward J Boyko (EJ)

University of Washington, Seattle, Washington, USA.

Michael S Conte (MS)

San Francisco (UCSF) Medical Centre, University of California, San Francisco, California, USA.

Misty Humphries (M)

UC Davis Medical Centre, Sacramento, California, USA.

Lee Kirksey (L)

The Cleveland Clinic, Cleveland, Ohio, USA.

Katharine C McGinigle (KC)

University of North-Carolina, Chapel Hill, North Carolina, USA.

Sigrid Nikol (S)

Clinical and Interventional Angiology, Asklepios Klinik, St. Georg, Hamburg, Germany.

Joakim Nordanstig (J)

Sahlgrenska University Hospital, Gothenburg, Sweden.

Vincent Rowe (V)

David Geffen School of Medicine, UCLA, Los Angeles, California, USA.

Russell David (R)

Leeds Teaching Hospitals NHS Trust, Leeds, UK.

Jos C van den Berg (JC)

CENTRO VASCOLARE TICINO Ospedale Regionale di Lugano, sede Civico and Universitätsinstitut für Diagnostische, Interventionelle und Pädiatrische Radiologie Inselspital, Universitätsspital, Bern, Switzerland.

Maarit Venermo (M)

Helsinki University Hospital, University of Helsinki, Helsinki, Finland.

Robert Fitridge (R)

Faculty of Health and Medical Sciences, University of Adelaide, Adelaide, South Australia, Australia.
Vascular and Endovascular Service, Royal Adelaide Hospital, Adelaide, South Australia, Australia.

Classifications MeSH