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perative Debridement of Diabetic Foot Ulcersichael S Golinko, MD, MA, Renta Joffe, MD, Jason Maggi, MD, Dalton Cox, BA,

ashwar B Chandrasekaran, MS, R Marjana Tomic-Canic, PhD, Harold Brem, MD, FACS

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very year, the incidence of diabetes increases, and an esti-ated 366 million people worldwide will be affected by

030.1 Because of multiple physiologic impairments2 suchs decreased angiogenesis or other microcirculatory condi-ions3,4 and neuropathy, routinely treatable wounds in pa-ients without diabetes often become chronic, nonhealingounds in patients with diabetes, posing serious risk for

nfection, sepsis, and amputation.5 Diabetic foot ulcersDFUs) occur in approximately 15% of patients with dia-etes, and of these, 14% to 24% of ulcers will end inmputation.6 Amputations in patients with diabetes aressociated with a high morbidity and a 5-year survival ratef 31%.7

Sharp debridement of the diabetic foot ulcer stimulateshe nonmigratory edge epithelium, releases growth factors,nd reduces the local inflammatory and proteolyticnvironment.8-10 The goal of operative debridement is toemove all hyperkeratotic tissue (ie, callus), necrotic tissue,unctionally abnormal senescent cells, and infected tissue,ll of which inhibit wound healing.10-12 In this manner, theemaining tissue, although physiologically impaired, canespond to exogenous topical treatment, (ie, growth factorsr cell therapy).

Debridement is widely accepted as the most definitivereatment for the diabetic foot ulcer,13,14 and although its mentioned in guidelines, protocols, and consensustatements,13,15-17 there remain few established descriptionsf the procedure.18-20 Inadequate debridement may lead torolonged infection, increasing risk for limb amputation.he objective of this study and accompanying video was toetail an operative procedure for debridement of diabeticoot ulcers based on biologic principles.

isclosure Information: Nothing to disclose.his work was carried out at Columbia University Medical Center, and NYUangone Medical Center, New York City, New York with financial supporthrough: National Institute of Health: NLM 5R01LM008443.

eceived May 21, 2008; Revised August 18, 2008; Accepted September 12,008.rom the Department of Surgery, Division of Wound Healing and Regener-tive Medicine, New York University School of Medicine (Golinko, Maggi,ox, Chandrasekaran, Brem), the Department of Pathology, Columbia Col-

ege of Physicians and Surgeons (Joffe, Tomic-Canic), and the Hospital forpecial Surgery, Tissue Engineering, Repair and Regeneration Program, Nework, NY (Tomic-Canic).orrespondence address: Harold Brem, MD, FACS, New York Universitychool of Medicine, Division of Wound Healing and Regenerative Medicine,

(epartment of Surgery, 462 First Ave, NBV 15W16, NY NY 10016.

e12008 by the American College of Surgeons

ublished by Elsevier Inc.

ETHODShe technique described represents the key steps we

ound after reviewing 280 operative debridements,hich were performed on 178 consecutive patients.nce a patient is admitted for surgery, an interdiscipli-

ary team of surgeons, primary care physicians, nurses,ocial workers, nurse practitioners, and physician assistantsmplement published protocols and guidelines.15,16,21-25

he wounds are also examined, photographed, mea-ured, and documented in the Wound Electronic Med-cal Record (WEMR) database. Patients were identifiedsing the Wound Electronic Medical Record and oper-tive notes for each operation reviewed.

ESULTSperative techniquexcision of callus and skin edge, routine pathologyallus refers to nonviable, hyperkeratotic tissue, and is

ommon to diabetic foot ulcers. The presence of callus canrevent healing and can also create increased pressure fromootwear or improper gait in the neuropathic diabetic foot,ltimately leading to further ulceration.26 The entire callus

s resected with a sharp scalpel and further debridementhould extend to the soft tissue adjacent to the callus (Fig.A). The clinical margin of debridement should be con-irmed by pathology and should not include epidermisith significant hyperkeratosis or parakeratosis as is seen inigure 1B. The solid line in Figure 1E represents the mar-in of callus, but debridement should extend to the dashedine, soft normal appearing skin.

ssessment of undermining and removalf the overlying tissuelthough most commonly associated with pressure ulcers,ndermining may also occur in diabetic foot ulcers. Al-hough assessment for undermining before debridement issually done, occasionally undermining is not apparentntil after the initial callus has been removed. Undermin-

ng is the destruction of tissue or ulceration extending un-er the skin edges so that the ulcer is larger at its base thant the skin surface. A sterile cotton swab can be used toently examine the wound for evidence of undermining

Fig. 1C). Undermining should be exposed by surgically

ISSN 1072-7515/08/$34.00doi:10.1016/j.jamcollsurg.2008.09.018

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e2 Golinko et al Operative Debridement of Diabetic Foot Ulcers J Am Coll Surg

esecting the overlying tissue. It is important to remove theeast amount of healthy tissue needed to expose the under-ying wound bed (Fig. 1D). By using a triangular incision,ith the apex of the triangle at the deepest point of under-

Figure 1. (A) The gross appearance of the callusVideo 1. (B) A routine hematoxylin and eosin staicorneum. Parakeratosis is noted by the presence(C) After removal of the callus, 2 cm of underminiby the depth of the cotton swabs. (D) Preparationexcision of a triangular portion of undermined tissulcer and the apex, toward the normal appearingdebridement should be extended to soft epidermiline.

ining, the entire wound bed can be exposed. F

emoval of clinically infected soft tissue and bonerom the wound and routine pathology

ebridement of the wound should proceed from super-icial to deep in a fashion parallel to the wound bed.

r excision using the technique demonstrated inhe callus, which is histologic, thickened stratumclei (small purple dots) in the stratum corneum.s discovered in the operating room, as indicatedcision of undermined tissue. (E) The wound aftere base of the triangle is toward the center of the

e. The solid lines represent the border of callus;t beyond this border, represented by the dashed

aften of tof nu

ng wafor exue. Thtissus, jus

irst, the necrotic skin should be removed. Next is the

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e3Vol. 207, No. 6, December 2008 Golinko et al Operative Debridement of Diabetic Foot Ulcers

ubcutaneous layer, including fat and connective tissue.djacent fascia, tendon, and muscle should be examined

or any evidence of spreading disease and infection, andan be easily excised, as demonstrated in Video 1. Aiopsy of the tissue left after this primary debridement isent for both pathologic and microbiologic analysis. Theptimal margin of debridement is where the tissue leftehind after removal of all clinically infected and ne-rotic tissue is free of infection and scar. Routine hema-oxylin and eosin (H&E) staining of wound specimens isseful to identify cellular granulation tissue (Fig. 2A)ersus the acellular, woven collagen fibers typical of fi-rosis (Fig. 2B). Debridement should go down to bone ifecessary, as Video 2 demonstrates in the metatarsalound. A earlier debridement on the patient had shown

cute osteomyelitis (Fig. 2C), but after further treat-ent with antibiotics and sharp debridement, nonin-

Figure 2. (A) Hematoxylin and eosin (H&E) staevidenced by numerous cells in addition to newpatient’s wound at a different level showing fibcollagen. This tissue should be surgically remgranulation tissue seen in Figure 2A. (C) Acute oregion on a previous debridement. The top arroexudate of inflammatory cells, including neutrshould include further debridement after antibiotbone is confirmed by pathologic analysis. (D) Rewoven bone with osteoclastic or osteoblastic acis considered healing bone.

ected bone, ie, reactive bone, was seen (Fig. 2D). t

ressing and postoperative followuphe remaining wound bed is treated with a primary hemo-

tatic agent, such as fibrin sealant and collagen, which haseen shown to reduce intraoperative and postoperativeleeding.31 Because minimal drainage is expected, theound is dressed in Kerlix gauze (Covidien), which is leftp to 7 days. In the presence of infection (ie, increasedhite blood cell count, cellulitis, or drainage), the patient is

reated with broad spectrum systemic antibiotics, whichre then tailored to the microbiology results. Once dis-harged, the patient is followed weekly in the outpatientetting to assess healing rates.

In preliminary studies, we found a generalized decreasen wound area and amputation rate in our case series of 178atients. These data endpoints are currently the subject of aulticenter study and further review will be needed to

etermine if the data will indeed significantly reflect the

the wound bed showing granulation tissue asmed blood vessels. (B) H&E stain of the same, characterized by acellular woven strands of

d, with the goal of reaching and stimulatingyelitis: H&E stain of bone from the metatarsal

ints to viable bone; the lower arrow points tos, lymphocytes, and plasma cells. Treatmentatment to ensure that either healthy or reactivee bone, which is characterized histologically by, depending on the stage of the remodeling and

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ISCUSSIONlinical judgment in itself is often not sufficient to deter-ine if all abnormal tissue has been removed from a foot

lcer in a person with diabetes. The margin of debridementf the skin edge should extend to the soft tissue beyond theallus. The depth of debridement of the wound bed shouldxtend to tissue that is free of fibrosis and infection, eg,steomyelitis, as confirmed by pathology and microbiology.

The accompanying figures and video illustrate the keyortions of operative debridement of diabetic foot ulcers.lthough the concept of debridement of a wound untilnly normal, soft tissue remains and culture and pathologynalysis has been advocated,13 precisely how this is achievedas not been described exclusively in foot ulcers in personsith diabetes. Saap and Falanga12 developed a debridementerformance index that includes callus, undermining, andound bed necrotic tissue. Falanga27 noted the importancef the goal of debridement down to well-vascularized tissueree of scar. In this report, we have built on these ideas toresent practical, biologically based techniques of diabeticoot ulcer debridement.

Clinical judgment has traditionally defined the marginf debridement, which is recognized as tissue with punctu-te bleeding.13 Although pathology has been advocated inound care,28 specific abnormal histopathologic findingsave not been a focus of intensive discussion.Excision of the skin edge to the point where clinically

iable tissue is reached should be confirmed by routine&E staining. Figure 1 highlights Mr X, a 74-year-oldan with type 2 diabetes, coronary artery disease, and hy-

ertension. He presented with nonpurulent drainage of aight great toe ulcer, had chronic osteomyelitis based on

RI and x-ray findings, and was growing methicillin-esistant Staphylococcus aureus on culture, so operative de-ridement was indicated. The technique described for cal-

us removal is regularly included in protocols as a measuref adequate debridement.12 The excised callus revealed hy-erkeratotic squamous epithelium with mildly inflamedermal tissue (Fig. 2). The outer edge, clinically normalppearing skin, was sent for pathologic analysis, revealingenign squamous epithelium and underlying dermal tis-ue. Any area of tissue that contains hyperkeratosis or par-keratosis likely represents incomplete keratinocyte differ-ntiation, so is pathologic and should be excised.29

athologically, hyperkeratosis is defined as an increase inhe thickness of the stratum corneum. Hyperkeratosis maye either orthokeratotic or parakeratotic in nature. Or-hokeratotic hyperkeratosis is an exaggeration of the nor-al pattern of keratinization (ie, no nuclei are seen in the

tratum corneum). In parakeratotic hyperkeratosis, nuclei i

re pathologically retained in the stratum corneum.30 Ex-mples of parakeratosis are visible in Figure 1B.

Pathologic specimens are examined by the surgeon tollow correlation between clinically appearing negativeargin and definitive pathologic analysis. To gain the pro-

iciency necessary to differentiate between parakeratosis,yperkeratosis, and normal epithelium, a strong relation-hip between the surgeon and the pathology department isssential. Repetition of this correlation will allow surgeonso more adequately assess the margins of resection clini-ally, with anticipation that this will allow definitive de-ridement in one operation. Secondarily, analysis of theathologic specimens does provide the necessary informa-ion to define an adequate debridement and allow the sur-eon to determine if a second debridement is necessary. Buthe primary objective is to gain the experience to provide aomplete debridement in one operation using a combina-ion of pathologic analysis and clinical judgment. In ourxperience, it is estimated that for a surgeon with no expe-ience in skin pathology, it would be necessary to performpproximately 50 procedures and pathologic analyses be-ore gaining clinical proficiency. Once attained, the sur-eon will gain the ability to perform a thorough and ade-uate debridement with fewer operative interventions.

Although assessment of undermining may be clinicallyncountered more often in pressure ulcers and is part ofoutine physical examination, it can be occasionally en-ountered in diabetic foot ulcers, particularly if clinicaluspicion is high for osteomyelitis. Armstrong and col-eagues18,19 stress the importance of removing underminedissue, and they describe a circumferential technique ofxcision. Although this technique certainly removes skinver undermining, it may also remove excess normal tissue.he case of Mr X illustrates the triangular technique of

emoval of undermining. He had an area of undermininglong the wound edge of the right toe, extending approxi-ately 2 cm. A triangular excision planned with the base of

he triangle on the wound edge and the apex extending intoormal tissue, is useful to minimize the amount of normalissue resected, but at the same time expose any under-ined area (Fig. 1C). Without excising this overlying skin,

ccess to the wound bed is limited, so healing may beelayed. Further study is needed to evaluate the efficacy ofhis technique.

It is apparent that there are several clinical scenarios inhich such an operative technique may appear to be lessesirable, such as in patients with severe peripheral vascularisease. This technique of operative debridement would beontraindicated without evaluation by a vascular surgeonnd assessment for possible intervention. In such cases, it is

mportant to note that there is not only one specific defin-

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e5Vol. 207, No. 6, December 2008 Golinko et al Operative Debridement of Diabetic Foot Ulcers

tive debridement, and this technique can be tailored to theatients’ medical condition while still removing all patho-

ogic tissue. As previously noted, by removing all patho-ogic tissue, the wound is increasingly stimulated to heal.o perform a lesser debridement and leave pathologic tis-ue would only further impair an already susceptible pa-ient’s ability to heal a very complex wound. A key to thisechnique is first identifying patients with ischemia or oth-rwise complicating medical factors and discussing withhem in detail the risks associated with such a procedure.he primary risk with this technique is postoperativeleeding. Although potential complications in addition toleeding, such as risk of infection or progression to ampu-ation, are always present, especially with a larger wound, its our experience that providing these patients with a widend deep debridement will give them the best possiblehance of healing.

Soft tissue and bone debridement techniques are fea-ured in the video. Mrs Y is a 46-year-old woman with typediabetes mellitus who presented with bilateral large blis-

ering plantar ulcers. Her past medical history was relevantor congestive heart failure, hypertension, and chronic re-al insufficiency. Her initial wounds each measured morehan 12 cm2 in area. Her wounds were debrided in theperating room on multiple occasions using the techniquesescribed earlier, until complete closure was achieved. Softissue cultures from the right foot grew Proteus mirabilis,taphylococcus aureus, and Morganella morganii. Quantita-ive cultures of the right fifth metatarsal bone revealedore than 10 million gram-negative rods and more than

0 million gram-positive cocci in clusters.Mr Y’s pathology illustrates two key findings in the

one. Normally, bone is surrounded by adipose and con-ective tissue. Osteomyelitis should be distinguished clin-

cally from reactive bone. Histologically and microscopi-ally, osteomyelitis is characterized by an admixture ofnflammatory cells (including neutrophils, lymphocytes,nd plasma cells surrounding what is often viable bone.he term reactive bone pertains to new bone formation orone remodeling, which histologically is characterized byoven bone with osteoclastic or osteoblastic activity de-ending on the stage of the remodeling.30 Bone debride-ent should extend until there is an absence of infection

nd fibrosis as confirmed by pathology.In the field of surgical oncology, surgeons have tradition-

lly used multiple histopathologic and molecular markerso identify a “negative margin.” In the future, surgeons maye able to use molecular markers of chronic wounds such ashe oncogenes c-myc and �-catenin to identify impairedells and guide debridement.29 Because the goal of debride-

ent is to remove physiologically impaired cells, an assay

imilar to a frozen section to define the extent of debride-ent could accelerate healing. Similar to a Moh’s proce-

ure, wound surgery may one day be guided by the regu-ation of genes at the wound edge.

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