On the Cutting Edge: Wound Care for the Endovascular Specialist

Abstract

Clinical outcomes in patients with critical limb ischemia (CLI) depend not only on endovascular restoration of macrovascular blood flow but also on aggressive periprocedural wound care. Education about this area of CLI therapy is essential not only to maximize the benefits of endovascular therapy but also to facilitate participation in the multidisciplinary care crucial to attaining limb salvage. In this article, we review the advances in wound care products and therapies that have granted the wound care specialist the ability to heal previously nonhealing wounds. We provide a primer on the basic science behind wound healing and the pathogenesis of ischemic wounds, familiarize the reader with methods of tissue viability assessment, and provide an overview of wound debridement techniques, dressings, hyperbaric therapy, and tissue offloading devices. Lastly, we explore emerging technology on the horizons of wound care.

Keywords

critical limb ischemia - wound care - ulcer - debridement - peripheral arterial disease - interventional radiology

Previous Presentations

Parts of the manuscript were previously presented in an education poster entitled “On the Cutting Edge of Wound Care: What Every Interventional Radiologist Needs to Know” at the Society of Interventional Radiology Annual Meeting 2018, Los Angeles, CA.

• References

• 1 Fowkes FGR, Rudan D, Rudan I. , et al. Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis. Lancet 2013; 382 (9901): 1329-1340
• 2 Henry JC, Peterson LA, Schlanger RE. Wound healing in peripheral arterial disease: current and future therapy. J Vasc Med Surg 2014; 02 (04) 157
• 3 Yost M. PAD Costs Economics Amputation Costs Economics, Critical Limb Ischemia, Chronic Venous Disease, Venous Ulcers, Chronic Venus Insufficiency - CLI US Supplement 2016. The Sage Group. Available at: http://thesagegroup.us/pages/reports/cli-us-supplement-2016.php . Accessed August 18, 2018
• 4 Noone A, Howlander N, Krapcho M, Miller D. SEER Cancer Statistics Review, 1975–2015. National Cancer Institute; 2018 . Available at: https://seer.cancer.gov/csr/1975_2015/ . Accessed August 27, 2018
• 5 Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II) - Journal of Vascular Surgery. Available at: https://www.jvascsurg.org/article/S0741-5214(06)02296-8/fulltext . Accessed August 18, 2018
• 6 Menke NB, Ward KR, Witten TM, Bonchev DG, Diegelmann RF. Impaired wound healing. Clin Dermatol 2007; 25 (01) 19-25
• 7 Yost ML. Cost-benefit analysis of critical limb ischemia in the era of the Affordable Care Act: is it fiscally responsible to perform primary amputation as treatment?. Endovascular Today 2014; (05) 29-36
• 8 Goodney PP, Travis LL, Nallamothu BK. , et al. Variation in the use of lower extremity vascular procedures for critical limb ischemia. Circ Cardiovasc Qual Outcomes 2012; 5 (01) 94-102
• 9 Eurobarometer Qualitative Study on Patient Involvement in Healthcare - European Innovation Partnership - European Commission. Available at: https://ec.europa.eu/eip/ageing/library/eurobarometer-qualitative-study-patient-involvement-healthcare_en . Published May 21, 2012 . Accessed August 18, 2018
• 10 Corbett LQ, Ennis WJ. What do patients want? Patient preference in wound care. Adv Wound Care (New Rochelle) 2014; 3 (08) 537-543
• 11 Náfrádi L, Nakamoto K, Schulz PJ. Is patient empowerment the key to promote adherence? A systematic review of the relationship between self-efficacy, health locus of control and medication adherence. PLoS One 2017; 12 (10) e0186458
• 12 Koenigsberg MR, Corliss J. Diabetes self-management: facilitating lifestyle change. Am Fam Physician 2017; 96 (06) 362-370
• 13 Kavitha KV, Tiwari S, Purandare VB, Khedkar S, Bhosale SS, Unnikrishnan AG. Choice of wound care in diabetic foot ulcer: a practical approach. World J Diabetes 2014; 5 (04) 546-556
• 14 Koenigsberg MR, Bartlett D, Cramer JS. Facilitating treatment adherence with lifestyle changes in diabetes. Am Fam Physician 2004; 69 (02) 309-316
• 15 Mills Sr JL. The application of the Society for Vascular Surgery Wound, Ischemia, and foot Infection (WIfI) classification to stratify amputation risk. J Vasc Surg 2017; 65 (03) 591-593
• 16 Mills Sr JL, Conte MS, Armstrong DG. , et al; Society for Vascular Surgery Lower Extremity Guidelines Committee. 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 (01) 220-34.e1 , 2
• 17 Martin P. Wound healing--aiming for perfect skin regeneration. Science 1997; 276 (5309): 75-81
• 18 Gonzalez Ade O, Costa TF, Andrade ZA, Medrado AR. Wound healing - a literature review. An Bras Dermatol 2016; 91 (05) 614-620
• 19 Tidball JG. Mechanisms of muscle injury, repair, and regeneration. Compr Physiol 2011; 1 (04) 2029-2062
• 20 Mendonça RJ, Coutinho-Netto J. Cellular aspects of wound healing. An Bras Dermatol 2009; 84 (03) 257-262
• 21 Qadura M, Terenzi DC, Verma S, Al-Omran M, Hess DA. Concise review: cell therapy for critical limb ischemia: an integrated review of preclinical and clinical studies. Stem Cells 2018; 36 (02) 161-171
• 22 Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro-oncol 2005; 7 (04) 452-464
• 23 Sood A, Granick MS, Tomaselli NL. Wound dressings and comparative effectiveness data. Adv Wound Care (New Rochelle) 2014; 3 (08) 511-529
• 24 Midwood KS, Williams LV, Schwarzbauer JE. Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 2004; 36 (06) 1031-1037
• 25 Stadelmann WK, Digenis AG, Tobin GR. Physiology and healing dynamics of chronic cutaneous wounds. Am J Surg 1998; 176 (2A, Suppl): 26S-38S
• 26 Gould LJ, Leong M, Sonstein J, Wilson S. Optimization and validation of an ischemic wound model. Wound Repair Regen 2005; 13 (06) 576-582
• 27 Medina A, Scott PG, Ghahary A, Tredget EE. Pathophysiology of chronic nonhealing wounds. J Burn Care Rehabil 2005; 26 (04) 306-319
• 28 Penn JW, Grobbelaar AO, Rolfe KJ. The role of the TGF-β family in wound healing, burns and scarring: a review. Int J Burns Trauma 2012; 2 (01) 18-28
• 29 Mustoe TA, O'Shaughnessy K, Kloeters O. Chronic wound pathogenesis and current treatment strategies: a unifying hypothesis. Plast Reconstr Surg 2006; 117 (7, Suppl): 35S-41S
• 30 Hirsch AT, Treat-Jacobson D, Lando HA, Hatsukami DK. The role of tobacco cessation, antiplatelet and lipid-lowering therapies in the treatment of peripheral arterial disease. Vasc Med 1997; 2 (03) 243-251
• 31 Jonason T, Bergström R. Cessation of smoking in patients with intermittent claudication. Effects on the risk of peripheral vascular complications, myocardial infarction and mortality. Acta Med Scand 1987; 221 (03) 253-260
• 32 Lassila R, Lepäntalo M. Cigarette smoking and the outcome after lower limb arterial surgery. Acta Chir Scand 1988; 154 (11-12): 635-640
• 33 Faulkner KW, House AK, Castleden WM. The effect of cessation of smoking on the accumulative survival rates of patients with symptomatic peripheral vascular disease. Med J Aust 1983; 1 (05) 217-219
• 34 2011 ACCF/AHA Focused Update of the Guideline for the Management of Patients With Peripheral Artery Disease (Updating the 2005 Guideline). Available at: http://circ.ahajournals.org/content/124/18/2020.full . Accessed January 13, 2016
• 35 Spangler EL, Goodney PP. Smoking cessation strategies in vascular surgery. Semin Vasc Surg 2015; 28 (02) 80-85
• 36 Cahill K, Stevens S, Perera R, Lancaster T. Pharmacological interventions for smoking cessation: an overview and network meta-analysis. Cochrane Database Syst Rev 2013; 5 (05) CD009329
• 37 Stead LF, Koilpillai P, Lancaster T. Additional behavioural support as an adjunct to pharmacotherapy for smoking cessation. Cochrane Database Syst Rev 2015; 10 (10) CD009670
• 38 Rooke TW, Hirsch AT, Misra S. , et al. 2011 ACCF/AHA Focused Update of the Guideline for the Management of Patients With Peripheral Artery Disease (Updating the 2005 Guideline). Available at: http://circ.ahajournals.org . Published February 5, 2016 . Accessed February 5, 2016
• 39 Adler AI, Stevens RJ, Neil A, Stratton IM, Boulton AJM, Holman RR. UKPDS 59: hyperglycemia and other potentially modifiable risk factors for peripheral vascular disease in type 2 diabetes. Diabetes Care 2002; 25 (05) 894-899
• 40 Zhou Z-Y, Liu Y-K, Chen H-L, Yang H-L, Liu F. HbA1c and lower extremity amputation risk in patients with diabetes: a meta-analysis. Int J Low Extrem Wounds 2015; 14 (02) 168-177
• 41 Christman AL, Selvin E, Margolis DJ, Lazarus GS, Garza LA. Hemoglobin A1c predicts healing rate in diabetic wounds. J Invest Dermatol 2011; 131 (10) 2121-2127
• 42 Mohler III ER, Hiatt WR, Creager MA. Cholesterol reduction with atorvastatin improves walking distance in patients with peripheral arterial disease. Circulation 2003; 108 (12) 1481-1486
• 43 Kumbhani DJ, Steg PG, Cannon CP. , et al; REACH Registry Investigators. Statin therapy and long-term adverse limb outcomes in patients with peripheral artery disease: insights from the REACH registry. Eur Heart J 2014; 35 (41) 2864-2872
• 44 Schanzer A, Hevelone N, Owens CD, Beckman JA, Belkin M, Conte MS. Statins are independently associated with reduced mortality in patients undergoing infrainguinal bypass graft surgery for critical limb ischemia. J Vasc Surg 2008; 47 (04) 774-781
• 45 Westin GG, Armstrong EJ, Bang H. , et al. Association between statin medications and mortality, major adverse cardiovascular event, and amputation-free survival in patients with critical limb ischemia. J Am Coll Cardiol 2014; 63 (07) 682-690
• 46 Stone NJ, Robinson JG, Lichtenstein AH. , et al; American College of Cardiology/American Heart Association Task Force on Practice Guidelines. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 2014; 129 (25) (Suppl. 02) S1-S45
• 47 Soga Y, Iida O, Hirano K. , et al. Impact of cilostazol after endovascular treatment for infrainguinal disease in patients with critical limb ischemia. J Vasc Surg 2011; 54 (06) 1659-1667
• 48 Soga Y, Iida O, Kawasaki D, Hirano K, Yamaoka T, Suzuki K. Impact of cilostazol on angiographic restenosis after balloon angioplasty for infrapopliteal artery disease in patients with critical limb ischemia. Eur J Vasc Endovasc Surg 2012; 44 (06) 577-581
• 49 Stewart KJ, Hiatt WR, Regensteiner JG, Hirsch AT. Exercise training for claudication. N Engl J Med 2002; 347 (24) 1941-1951
• 50 Tompra N, Foster C, Sanchis-Gomar F, de Koning JJ, Lucia A, Emanuele E. Upper versus lower limb exercise training in patients with intermittent claudication: a systematic review. Atherosclerosis 2015; 239 (02) 599-606
• 51 Wound Debridement Options. The 5 Major Methods. WoundSource. Available at: http://www.woundsource.com/blog/wound-debridement-options-5-major-methods . Published April 19, 2018 . Accessed August 14, 2018
• 52 Chambers L, Woodrow S, Brown AP. , et al. Degradation of extracellular matrix components by defined proteinases from the greenbottle larva Lucilia sericata used for the clinical debridement of non-healing wounds. Br J Dermatol 2003; 148 (01) 14-23
• 53 Mumcuoglu KY, Miller J, Mumcuoglu M, Friger M, Tarshis M. Destruction of bacteria in the digestive tract of the maggot of Lucilia sericata (Diptera: Calliphoridae). J Med Entomol 2001; 38 (02) 161-166
• 54 Gottrup F, Jørgensen B. Maggot debridement: an alternative method for debridement. Eplasty 2011; 11: e33
• 55 Advisor WC. Debridement options: BEAMS made easy. Wound Care Advisor. Available at: https://woundcareadvisor.com/debridement-options-beams-made-easy_vol2-no/ . Published March 25, 2013. Accessed August 17, 2018
• 56 Mechanical Debridement | Wound Debridement Techniques. WoundEducators.com | Online Wound Care Certification Courses. Available at: https://woundeducators.com/wound-debridement-techniques-3-mechanical-debridement/ . Published June 16, 2012 . Accessed August 17, 2018
• 57 Ayello EA, Cuddigan J, Kerstein MD. Skip the knife: debriding wounds without surgery. Nursing 2002; 32 (09) 58-63, quiz 64
• 58 Utsunomiya M, Nakamura M, Nakanishi M. , et al. Impact of wound blush as an angiographic end point of endovascular therapy for patients with critical limb ischemia. J Vasc Surg 2012; 55 (01) 113-121
• 59 Khan MUN, Lall P, Harris LM, Dryjski ML, Dosluoglu HH. Predictors of limb loss despite a patent endovascular-treated arterial segment. J Vasc Surg 2009; 49 (06) 1440-1445 , discussion 1445–1446
• 60 Meyer A, Goller K, Horch RE. , et al. Results of combined vascular reconstruction and free flap transfer for limb salvage in patients with critical limb ischemia. J Vasc Surg 2015; 61 (05) 1239-1248
• 61 Blevins Jr WA, Schneider PA. Endovascular management of critical limb ischemia. Eur J Vasc Endovasc Surg 2010; 39 (06) 756-761
• 62 Rother U, Lang W. Noninvasive measurements of tissue perfusion in critical limb ischemia. Gefasschirurgie 2018; 23 (Suppl. 01) 8-12
• 63 HyperMed Imaging, Inc. Announces CE Mark for New HyperViewTM Product. Available at: https://www.businesswire.com/news/home/20180402005574/en/HyperMed-Imaging-Announces-CE-Mark-New-HyperView%E2%84%A2 . Published April 2, 2018. Accessed August 21, 2018.
• 64 Neville R, Gupta S. Establishment of normative perfusion values using hyperspectral tissue oxygenation mapping technology. Vascular Disease Management 2009; 6 (06) 156-161
• 65 Chiang N, Jain JK, Sleigh J, Vasudevan T. Evaluation of hyperspectral imaging technology in patients with peripheral vascular disease. J Vasc Surg 2017; 66 (04) 1192-1201
• 66 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
• 67 Smith AM, Mancini MC, Nie S. Bioimaging: second window for in vivo imaging. Nat Nanotechnol 2009; 4 (11) 710-711
• 68 Marshall MV, Rasmussen JC, Tan I-C. , et al. Near-infrared fluorescence imaging in humans with indocyanine green: a review and update. Open Surg Oncol J 2010; 2 (02) 12-25
• 69 Bajwa A, Wesolowski R, Patel A. , et al. Assessment of tissue perfusion in the lower limb: current methods and techniques under development. Circ Cardiovasc Imaging 2014; 7 (05) 836-843
• 70 Braun JD, Trinidad-Hernandez M, Perry D, Armstrong DG, Mills Sr JL. Early quantitative evaluation of indocyanine green angiography in patients with critical limb ischemia. J Vasc Surg 2013; 57 (05) 1213-1218
• 71 Settembre N, Kauhanen P, Albäck A, Spillerova K, Venermo M. Quality control of the foot revascularization using indocyanine green fluorescence imaging. World J Surg 2017; 41 (07) 1919-1926
• 72 Patel HM, Bulsara SS, Banerjee S. , et al. Indocyanine green angiography to prognosticate healing of foot ulcer in critical limb ischemia: a novel technique. Ann Vasc Surg 2018; 51: 86-94
• 73 Igari K, Kudo T, Toyofuku T, Jibiki M, Inoue Y, Kawano T. Quantitative evaluation of the outcomes of revascularization procedures for peripheral arterial disease using indocyanine green angiography. Eur J Vasc Endovasc Surg 2013; 46 (04) 460-465
• 74 Igari K, Kudo T, Uchiyama H, Toyofuku T, Inoue Y. Intraarterial injection of indocyanine green for evaluation of peripheral blood circulation in patients with peripheral arterial disease. Ann Vasc Surg 2014; 28 (05) 1280-1285
• 75 Benitez E, Sumpio BJ, Chin J, Sumpio BE. Contemporary assessment of foot perfusion in patients with critical limb ischemia. Semin Vasc Surg 2014; 27 (01) 3-15
• 76 Eneroth M, Larsson J, Apelqvist J. Deep foot infections in patients with diabetes and foot ulcer: an entity with different characteristics, treatments, and prognosis. J Diabetes Complications 1999; 13 (5-6): 254-263
• 77 Hill SL, Holtzman GI, Buse R. The effects of peripheral vascular disease with osteomyelitis in the diabetic foot. Am J Surg 1999; 177 (04) 282-286
• 78 Giurato L, Meloni M, Izzo V, Uccioli L. Osteomyelitis in diabetic foot: a comprehensive overview. World J Diabetes 2017; 8 (04) 135-142
• 79 Grayson ML, Gibbons GW, Balogh K, Levin E, Karchmer AW. Probing to bone in infected pedal ulcers. A clinical sign of underlying osteomyelitis in diabetic patients. JAMA 1995; 273 (09) 721-723
• 80 Lee YJ, Sadigh S, Mankad K, Kapse N, Rajeswaran G. The imaging of osteomyelitis. Quant Imaging Med Surg 2016; 6 (02) 184-198
• 81 Palestro CJ. FDG-PET in musculoskeletal infections. Semin Nucl Med 2013; 43 (05) 367-376
• 82 Lavery LA, Armstrong DG, Peters EJG, Lipsky BA. Probe-to-bone test for diagnosing diabetic foot osteomyelitis: reliable or relic?. Diabetes Care 2007; 30 (02) 270-274
• 83 Braddock M. Euroconference on tissue repair and ulcer/wound healing: molecular mechanisms, therapeutic targets and future directions. Expert Opin Investig Drugs 2005; 14 (06) 743-749
• 84 Snyder RJ. Treatment of nonhealing ulcers with allografts. Clin Dermatol 2005; 23 (04) 388-395
• 85 Taylor JE, Laity PR, Hicks J. , et al. Extent of iron pick-up in deforoxamine-coupled polyurethane materials for therapy of chronic wounds. Biomaterials 2005; 26 (30) 6024-6033
• 86 Sheehan P, Jones P, Caselli A, Giurini JM, Veves A. Percent change in wound area of diabetic foot ulcers over a 4-week period is a robust predictor of complete healing in a 12-week prospective trial. Diabetes Care 2003; 26 (06) 1879-1882
• 87 Snyder RJ, Cardinal M, Dauphinée DM, Stavosky J. A post-hoc analysis of reduction in diabetic foot ulcer size at 4 weeks as a predictor of healing by 12 weeks. Ostomy Wound Manage 2010; 56 (03) 44-50
• 88 Gist S, Tio-Matos I, Falzgraf S, Cameron S, Beebe M. Wound care in the geriatric client. Clin Interv Aging 2009; 4: 269-287
• 89 Edwards JV, Howley P, Cohen IK. In vitro inhibition of human neutrophil elastase by oleic acid albumin formulations from derivatized cotton wound dressings. Int J Pharm 2004; 284 (1-2): 1-12
• 90 Schönfelder U, Abel M, Wiegand C, Klemm D, Elsner P, Hipler U-C. Influence of selected wound dressings on PMN elastase in chronic wound fluid and their antioxidative potential in vitro. Biomaterials 2005; 26 (33) 6664-6673
• 91 Snyder RJ, Ead J, Glick B, Cuffy C. Dehydrated human amnion/chorion membrane as adjunctive therapy in the multidisciplinary treatment of pyoderma gangrenosum: a case report. Ostomy Wound Manage 2015; 61 (09) 40-49
• 92 Vazales R, Constant D, Snyder RJ. A rare case of aggressive digital adenocarcinoma of the lower extremity, masquerading as an ulcerative lesion that clinically favored benignancy. Healthcare (Basel) 2014; 2 (03) 315-323
• 93 Tang JC, Vivas A, Rey A, Kirsner RS, Romanelli P. Atypical ulcers: wound biopsy results from a university wound pathology service. Ostomy Wound Manage 2012; 58 (06) 20-22 , 24, 26–29
• 94 Forrest RD. Early history of wound treatment. J R Soc Med 1982; 75 (03) 198-205
• 95 Wodash AJ. Wet-to-dry dressings do not provide moist wound healing. J Am Coll Clin Wound Spec 2013; 4 (03) 63-66
• 96 Dale BA, Wright DH. Say goodbye to wet-to-dry wound care dressings: changing the culture of wound care management within your agency. Home Healthc Nurse 2011; 29 (07) 429-440
• 97 Khan T, Shin L, Woelfel S, Rowe V, Wilson BL, Armstrong DG. Building a scalable diabetic limb preservation program: four steps to success. Diabet Foot Ankle 2018; 9 (01) 1452513
• 98 Kinlay S. Management of critical limb ischemia. Circ Cardiovasc Interv 2016; 9 (02) e001946
• 99 Boghossian JA, Miller JD, Armstrong DG. Offloading the diabetic foot: toward healing wounds and extending ulcer-free days in remission. Chronic Wound Care Management and Research 2017; 4: 83-88
• 100 Fernando ME, Crowther RG, Lazzarini PA. , et al. Plantar pressures are higher in cases with diabetic foot ulcers compared to controls despite a longer stance phase duration. BMC Endocr Disord 2016; 16 (01) 51
• 101 Crews R. Diabetes: Improving foot care compliance. Lower Extremity Review Magazine. October 2009. Available: http://lermagazine.com/article/diabetes-improving-foot-care-compliance . Accessed August 20, 2018
• 102 Bus SA, van Deursen RW, Armstrong DG, Lewis JE, Caravaggi CF, Cavanagh PR. ; International Working Group on the Diabetic Foot. Footwear and offloading interventions to prevent and heal foot ulcers and reduce plantar pressure in patients with diabetes: a systematic review. Diabetes Metab Res Rev 2016; 32 (Suppl. 01) 99-118
• 103 Armstrong DG, Boulton AJ. Activity monitors: should we begin dosing activity as we dose a drug?. J Am Podiatr Med Assoc 2001; 91 (03) 152-153
• 104 Cavanagh PR, Bus SA. Off-loading the diabetic foot for ulcer prevention and healing. Plast Reconstr Surg 2011; 127 (Suppl. 01) 248S-256S
• 105 Brem H, Sheehan P, Boulton AJM. Protocol for treatment of diabetic foot ulcers. Am J Surg 2004; 187 (5A): 1S-10S
• 106 Peters EJG, Armstrong DG, Lavery LA. Risk factors for recurrent diabetic foot ulcers: site matters. Diabetes Care 2007; 30 (08) 2077-2079
• 107 Uccioli L, Faglia E, Monticone G. , et al. Manufactured shoes in the prevention of diabetic foot ulcers. Diabetes Care 1995; 18 (10) 1376-1378
• 108 Wrobel JS, Ammanath P, Le T. , et al. A novel shear reduction insole effect on the thermal response to walking stress, balance, and gait. J Diabetes Sci Technol 2014; 8 (06) 1151-1156
• 109 Healy A, Naemi R, Chockalingam N. The effectiveness of footwear and other removable off-loading devices in the treatment of diabetic foot ulcers: a systematic review. Curr Diabetes Rev 2014; 10 (04) 215-230
• 110 Najafi B, Mohseni H, Grewal GS, Talal TK, Menzies RA, Armstrong DG. An optical-fiber-based smart textile (Smart Socks) to manage biomechanical risk factors associated with diabetic foot amputation. J Diabetes Sci Technol 2017; 11 (04) 668-677
• 111 Ventola CL. Medical applications for 3D printing: current and projected uses. P&T 2014; 39 (10) 704-711
• 112 Sunkari VG, Lind F, Botusan IR. , et al. Hyperbaric oxygen therapy activates hypoxia-inducible factor 1 (HIF-1), which contributes to improved wound healing in diabetic mice. Wound Repair Regen 2015; 23 (01) 98-103
• 113 Gill AL, Bell CNA. Hyperbaric oxygen: its uses, mechanisms of action and outcomes. QJM 2004; 97 (07) 385-395
• 114 Gabb G, Robin ED. Hyperbaric oxygen. A therapy in search of diseases. Chest 1987; 92 (06) 1074-1082
• 115 Bhutani S, Vishwanath G. Hyperbaric oxygen and wound healing. Indian J Plast Surg 2012; 45 (02) 316-324
• 116 Tibbles PM, Edelsberg JS. Hyperbaric-oxygen therapy. N Engl J Med 1996; 334 (25) 1642-1648
• 117 Leach RM, Rees PJ, Wilmshurst P. Hyperbaric oxygen therapy. BMJ 1998; 317 (7166): 1140-1143
• 118 Knighton DR, Halliday B, Hunt TK. Oxygen as an antibiotic. The effect of inspired oxygen on infection. Arch Surg 1984; 119 (02) 199-204
• 119 Mader J, Adam K, Couch L. Potentiation of tobramycin by hyperbaric oxygen in experimental Pseudomonas aeruginosa osteomyelitis (Abstract 1331). Presented at the: American Society for Microbiology: the 27th Interscience Conference on Antimicrobial Agents and Chemotherapy. Washington, DC; 1987
• 120 Fedorko L, Bowen JM, Jones W. , et al. Hyperbaric oxygen therapy does not reduce indications for amputation in patients with diabetes with nonhealing ulcers of the lower limb: a prospective, double-blind, randomized controlled clinical trial. Diabetes Care 2016; 39 (03) 392-399
• 121 Santema KTB, Stoekenbroek RM, Koelemay MJW. , et al; DAMO2CLES Study Group. Hyperbaric oxygen therapy in the treatment of ischemic lower- extremity ulcers in patients with diabetes: results of the DAMO₂CLES multicenter randomized clinical trial. Diabetes Care 2018; 41 (01) 112-119
• 122 Huang E. Comment on Santema et al. Hyperbaric oxygen therapy in the treatment of ischemic lower-extremity ulcers in patients with diabetes: results of the DAMO₂CLES multicenter randomized clinical trial. diabetes care 2018;41:112-119. Diabetes Care 2018; 41 (04) e61
• 123 Moran PS, Teljeur C, Harrington P, Ryan M. A systematic review of intermittent pneumatic compression for critical limb ischaemia. Vasc Med 2015; 20 (01) 41-50
• 124 Fetterolf DE, Snyder RJ. Scientific and clinical support for the use of dehydrated amniotic membrane in wound management. Wounds 2012; 24 (10) 299-307
• 125 Kesting MR, Wolff K-D, Hohlweg-Majert B, Steinstraesser L. The role of allogenic amniotic membrane in burn treatment. J Burn Care Res 2008; 29 (06) 907-916
• 126 Koob TJ, Lim JJ, Zabek N, Massee M. Cytokines in single layer amnion allografts compared to multilayer amnion/chorion allografts for wound healing. J Biomed Mater Res B Appl Biomater 2015; 103 (05) 1133-1140
• 127 Angiogenic properties of dehydrated human amnion/chorion allografts: therapeutic potential for soft tissue repair and regeneration | Vascular Cell. Available at: https://vascularcell.com/index.php/vc/article/view/10.1186-2045-824X-6-10 . Accessed August 28, 2018
• 128 Serena TE, Carter MJ, Le LT, Sabo MJ, DiMarco DT. ; EpiFix VLU Study Group. A multicenter, randomized, controlled clinical trial evaluating the use of dehydrated human amnion/chorion membrane allografts and multilayer compression therapy vs. multilayer compression therapy alone in the treatment of venous leg ulcers. Wound Repair Regen 2014; 22 (06) 688-693
• 129 Zelen CM, Snyder RJ, Serena TE, Li WW. The use of human amnion/chorion membrane in the clinical setting for lower extremity repair: a review. Clin Podiatr Med Surg 2015; 32 (01) 135-146
• 130 Zelen CM, Serena TE, Denoziere G, Fetterolf DE. A prospective randomised comparative parallel study of amniotic membrane wound graft in the management of diabetic foot ulcers. Int Wound J 2013; 10 (05) 502-507
• 131 Loots MA, Lamme EN, Mekkes JR, Bos JD, Middelkoop E. Cultured fibroblasts from chronic diabetic wounds on the lower extremity (non-insulin-dependent diabetes mellitus) show disturbed proliferation. Arch Dermatol Res 1999; 291 (2-3): 93-99
• 132 Berlanga J, Fernández JI, López E. , et al. Heberprot-P: a novel product for treating advanced diabetic foot ulcer. MEDICC Rev 2013; 15 (01) 11-15
• 133 Marx RE. Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg 2004; 62 (04) 489-496
• 134 Massara M, Barillà D, De Caridi G. , et al. Application of autologous platelet-rich plasma to enhance wound healing after lower limb revascularization: a case series and literature review. Semin Vasc Surg 2015; 28 (3-4): 195-200
• 135 Serra R, Buffone G, Dominijanni A, Molinari V, Montemurro R, de Franciscis S. Application of platelet-rich gel to enhance healing of transmetatarsal amputations in diabetic dysvascular patients. Int Wound J 2013; 10 (05) 612-615
• 136 Fernández-Montequín JI, Valenzuela-Silva CM, Díaz OG. , et al; Cuban Diabetic Foot Study Group. Intra-lesional injections of recombinant human epidermal growth factor promote granulation and healing in advanced diabetic foot ulcers: multicenter, randomised, placebo-controlled, double-blind study. Int Wound J 2009; 6 (06) 432-443
• 137 Sridharan K, Sivaramakrishnan G. Growth factors for diabetic foot ulcers: mixed treatment comparison analysis of randomized clinical trials. Br J Clin Pharmacol 2018; 84 (03) 434-444
• 138 Caporali A, Emanueli C. MicroRNA regulation in angiogenesis. Vascul Pharmacol 2011; 55 (04) 79-86
• 139 Neale JPH, Pearson JT, Katare R, Schwenke DO. Ghrelin, MicroRNAs, and critical limb ischemia: hungering for a novel treatment option. Front Endocrinol (Lausanne) 2017; 8: 350
• 140 Lu D, Chen B, Liang Z. , et al. Comparison of bone marrow mesenchymal stem cells with bone marrow-derived mononuclear cells for treatment of diabetic critical limb ischemia and foot ulcer: a double-blind, randomized, controlled trial. Diabetes Res Clin Pract 2011; 92 (01) 26-36
• 141 Gupta PK, Chullikana A, Parakh R. , et al. A double blind randomized placebo controlled phase I/II study assessing the safety and efficacy of allogeneic bone marrow derived mesenchymal stem cell in critical limb ischemia. J Transl Med 2013; 11: 143
• 142 Andersen CA, Roukis TS. The diabetic foot. Surg Clin North Am 2007; 87 (05) 1149-1177 , x
• 143 Ramirez AT, Soroff HS, Schwartz MS, Mooty J, Pearson E, Raben MS. Experimental wound healing in man. Surg Gynecol Obstet 1969; 128 (02) 283-293
• 144 Flanagan M. Improving accuracy of wound measurement in clinical practice. Ostomy Wound Manage 2003; 49 (10) 28-40
• 145 Günes UY. A prospective study evaluating the Pressure Ulcer Scale for Healing (PUSH Tool) to assess stage II, stage III, and stage IV pressure ulcers. Ostomy Wound Manage 2009; 55 (05) 48-52
• 146 Margolis DJ, Berlin JA, Strom BL. Which venous leg ulcers will heal with limb compression bandages?. Am J Med 2000; 109 (01) 15-19