18
Strategies to Prevent and Heal Diabetic Foot Ulcers: A Joint Publication of APMA and SVS SPECIAL COMMUNICATION History of the Team Approach to Amputation Prevention Pioneers and Milestones Lee J. Sanders, DPM* Jeffrey M. Robbins, DPMMichael E. Edmonds, MDThis historical perspective highlights some of the pioneers, milestones, teams, and system changes that have had a major impact on management of the diabetic foot during the past 100 years. In 1934, American diabetologist Elliott P. Joslin noted that mortality from diabetic coma had fallen from 60% to 5% after the introduction of insulin, yet deaths from diabetic gangrene of the lower extremity had risen significantly. He believed that diabetic gangrene was preventable. His remedy was a team approach that included foot care, diet, exercise, prompt treatment of foot infections, and specialized surgical care. The history of the team approach to management of the diabetic foot chronicles the rise of a new health profession—podiatric medicine and surgery—and emergence of the specialty of vascular surgery. The partnership among the diabetologist, vascular surgeon, and podiatric surgeon is a natural one. The complementary skills and knowledge of each can improve limb salvage and functional outcomes. Comprehensive multidisciplinary foot-care programs have been shown to increase quality of care and reduce amputation rates by 36% to 86%. Development of distal revascularization techniques to restore pulsatile blood flow to the foot has also been a major advancement. Patients with diabetic foot complications are among the most complex and vulnerable of all patient populations. Specialized diabetic foot clinics of the 21st century should be multidisciplinary and equipped to coordinate diagnosis, off-loading, and preventive care; to perform revascularization procedures; to aggressively treat infections; and to manage medical comorbidities. (J Am Podiatr Med Assoc 100(5): 317-334, 2010) The history of the team approach to management of the diabetic foot chronicles the rise of a new health profession—podiatric medicine and surgery—and emergence of the specialties of vascular surgery and wound healing. The partnership among the diabe- tologist, vascular surgeon, and podiatric physician can be seen as a natural marriage that complements the skills and knowledge of each partner and results in more successful limb salvage and functional outcomes. Technology transfer from leprosy to diabetes has helped us understand the role of neuropathy in the pathogenesis of diabetic foot ulcers. The pathogenesis of gangrene in the diabetic foot is complex and is affected by the interaction of arterial insufficiency, neuropathy, ulceration, and infection. History has demonstrated that compre- hensive multidisciplinary foot-care programs im- prove quality of care and can reduce amputation rates by 36% to 86%. 1-12 Development of distal revascularization techniques to restore pulsatile blood flow to the foot has been a major advance- ment in limb salvage. Understanding of the pathogenesis and manage- ment of the diabetic foot has evolved from the contributions of a diverse group of individuals and teams worldwide. The goal of this historical perspec- tive is to highlight some of the pioneers, milestones, teams, and system changes that have had a major *Podiatry Service, Veterans Affairs Medical Center, Lebanon, PA. Veterans Health Administration Headquarters Podiatry Service, Louis Stokes Cleveland Veterans Affairs Medical Center, Cleveland, OH. Diabetic Foot Clinic, King’s College Hospital, London, England. Corresponding author: Lee J. Sanders, DPM, Podiatry Service, Veterans Affairs Medical Center, 1700 S Lincoln Ave, Lebanon, PA 17042. (E-mail: [email protected]) Journal of the American Podiatric Medical Association Vol 100 No 5 September/October 2010 317

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Page 1: History of the Team Approach to Amputation Prevention · care, diet, exercise, prompt treatment of foot infections, and specialized surgical care. The history of the team approach

Strategies to Prevent and Heal Diabetic Foot Ulcers:

A Joint Publication of APMA and SVS

SPECIAL COMMUNICATION

History of the Team Approach to Amputation Prevention

Pioneers and Milestones

Lee J. Sanders, DPM*Jeffrey M. Robbins, DPM†Michael E. Edmonds, MD‡

This historical perspective highlights some of the pioneers, milestones, teams, andsystem changes that have had a major impact on management of the diabetic foot duringthe past 100 years. In 1934, American diabetologist Elliott P. Joslin noted that mortalityfrom diabetic coma had fallen from 60% to 5% after the introduction of insulin, yet deathsfrom diabetic gangrene of the lower extremity had risen significantly. He believed thatdiabetic gangrene was preventable. His remedy was a team approach that included footcare, diet, exercise, prompt treatment of foot infections, and specialized surgical care.

The history of the team approach to management of the diabetic foot chronicles the riseof a new health profession—podiatric medicine and surgery—and emergence of thespecialty of vascular surgery. The partnership among the diabetologist, vascularsurgeon, and podiatric surgeon is a natural one. The complementary skills andknowledge of each can improve limb salvage and functional outcomes. Comprehensivemultidisciplinary foot-care programs have been shown to increase quality of care andreduce amputation rates by 36% to 86%. Development of distal revascularizationtechniques to restore pulsatile blood flow to the foot has also been a major advancement.

Patients with diabetic foot complications are among the most complex and vulnerable ofall patient populations. Specialized diabetic foot clinics of the 21st century should bemultidisciplinary and equipped to coordinate diagnosis, off-loading, and preventive care;to perform revascularization procedures; to aggressively treat infections; and to managemedical comorbidities. (J Am Podiatr Med Assoc 100(5): 317-334, 2010)

The history of the team approach to management of

the diabetic foot chronicles the rise of a new health

profession—podiatric medicine and surgery—and

emergence of the specialties of vascular surgery and

wound healing. The partnership among the diabe-

tologist, vascular surgeon, and podiatric physician

can be seen as a natural marriage that complements

the skills and knowledge of each partner and results

in more successful limb salvage and functional

outcomes. Technology transfer from leprosy to

diabetes has helped us understand the role of

neuropathy in the pathogenesis of diabetic foot

ulcers. The pathogenesis of gangrene in the diabetic

foot is complex and is affected by the interaction of

arterial insufficiency, neuropathy, ulceration, and

infection. History has demonstrated that compre-

hensive multidisciplinary foot-care programs im-

prove quality of care and can reduce amputation

rates by 36% to 86%.1-12 Development of distal

revascularization techniques to restore pulsatile

blood flow to the foot has been a major advance-

ment in limb salvage.

Understanding of the pathogenesis and manage-

ment of the diabetic foot has evolved from the

contributions of a diverse group of individuals and

teams worldwide. The goal of this historical perspec-

tive is to highlight some of the pioneers, milestones,

teams, and system changes that have had a major

*Podiatry Service, Veterans Affairs Medical Center, Lebanon,

PA.†Veterans Health Administration Headquarters Podiatry

Service, Louis Stokes Cleveland Veterans Affairs Medical

Center, Cleveland, OH.‡Diabetic Foot Clinic, King’s College Hospital, London,

England.Corresponding author: Lee J. Sanders, DPM, Podiatry

Service, Veterans Affairs Medical Center, 1700 S Lincoln Ave,

Lebanon, PA 17042. (E-mail: [email protected])

Journal of the American Podiatric Medical Association � Vol 100 � No 5 � September/October 2010 317

Page 2: History of the Team Approach to Amputation Prevention · care, diet, exercise, prompt treatment of foot infections, and specialized surgical care. The history of the team approach

impact on risk assessment and preservation of the

diabetic foot during the past 100 years.

Early 20th Century: New York City,Toronto, and Boston

Maurice J. Lewi, MD (1857–1957)—New York,New York

Our chronicle of the team approach to lower-limb

amputation prevention begins with Maurice J. Lewi,

MD (1857–1957), founder of The New York College

of Podiatric Medicine, formerly The School of

Chiropody of New York, the oldest college of

podiatric medicine, located in New York City. As

early as 1911, Dr. Lewi recognized the medical

establishment’s indifference toward the ‘‘minor foot

ills’’ of mankind. He was outspoken about the need

for specialized foot care and about the role of

chiropodists in providing this care. His insistence on

ethical and scientific standards formed the basis on

which modern podiatric medicine was estab-

lished.13 Dr. Lewi dedicated his 1914 publication,

The Textbook of Chiropody, to ‘‘the men and women

who were pioneers in the cause of Chiropody and

who, in the face of many and unusual obstacles,

labored to the benefit of mankind in a branch of

medical learning that had been neglected through

all the centuries.’’14(p. v) In the chapter entitled

‘‘Some Suggestive Foot Conditions,’’ Joseph P.

Solomon discusses various foot conditions that are

manifestations of systemic diseases, in particular

diabetes:

. . .so it happens oft times that the observing

chiropodist is the first to recognize signs and

symptoms on his patient’s feet and limbs which are

indicative of diabetes. . .the greatest care should be

taken not to make any incision which might cause the

flow of blood as such patients are exceedingly

susceptible to all kinds of infection, local and

otherwise. This is particularly true of those who are

advanced in years and with whom the development

of diabetic gangrene is certain if they have lesions on

the foot which are not carefully treated...14(p1086)

Dr. Lewi’s vitality, energy, and personal charm

opened the doors for the new profession of

chiropody. Little did Dr. Lewi know how epidemic

diabetes would become and how this disease would

help define the practice of podiatric medicine and

surgery.

Discovery of Insulin—Toronto, Ontario, Canada

The discovery of insulin at the University of Toronto

in 1921–1922 by Frederick G. Banting, Charles H.

Best, James B. Collip, and J. J. R. Macleod was oneof the landmark medical discoveries of the 20thcentury. Isolation of the internal secretion of the

pancreas and the subsequent therapeutic introduc-tion of insulin in the 1920s were miraculous

developments in the treatment of diabetes thatallowed individuals affected by this disease to livean almost normal life. Before 1923, the diagnosis of

diabetes in a child was a death sentence. Althoughinsulin commuted this sentence, it sadly becameapparent that insulin was not a cure for diabetes. As

people began to live longer, they experiencedcomplications that had not previously been

seen.15, 16

New England Deaconess Hospital—Boston,Massachusetts

Elliott P. Joslin, MD (1869–1962) (Fig. 1), thefamous American diabetologist, observed that the

era of coma as the central problem of diabetes hadgiven way to the era of complications. Dr. Joslinnoted that after the introduction of insulin, mortal-

ity from diabetic coma had fallen significantly from60% to 5%, yet deaths from diabetic gangrene of thefoot and leg had risen significantly.17 Through the

efforts of Dr. Joslin and members of the Massachu-setts Chiropody Association, the first hospital foot

clinic was established at the New England Deacon-ess Hospital in 1928.13 Dr. Joslin wrote: ‘‘Our Bostonchiropodists are useful allies. They have contributed

much to our reduction in gangrene.’’17(p18)

In 1933, at the George F. Baker Clinic of the NewEngland Deaconess Hospital, 16% of the deaths

were from gangrene and infection of the extremi-ties. Dr. Joslin alleged that the reason for thiscomplication was that physicians were not aggres-

sive enough in their treatment of diabetes. Hequoted the leading American diabetologist Freder-

ick M. Allen (1879–1964) by saying that ‘‘the surestway to produce gangrene is to keep patients alivebut only half treat them.’’17(p17) Dr. Joslin noted that

gangrene increased with the age of the individual,with the duration of diabetes, and in the uncon-trolled patient. In 1934, in a paper entitled ‘‘The

Menace of Diabetic Gangrene,’’ Dr. Joslin wrote,‘‘gangrene deserves more intensive study and the

investigation of the cause and type of arterioscle-rosis which is responsible for it should help to deferold age for us all.’’17(p16) He believed that diabetic

gangrene is not heaven-sent but rather earth bornand as such is preventable in most cases. Hisremedy was a team approach to diabetes care that

included foot care, medical nutrition therapy,

318 September/October 2010 � Vol 100 � No 5 � Journal of the American Podiatric Medical Association

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exercise, prompt treatment of foot infections, and,

when necessary, specialized surgical care. Dr. Joslin

remarked that ‘‘all the members of a ball team

cannot pitch the ball and no ball team wins which

tries to have each member of the nine in the

pitcher’s box. It is only common sense to provide in

a large general hospital for specialization in diabetic

surgery.’’17(p19)

Leland McKittrick, MD (1893-1978) (Fig. 2), was

recruited by Dr. Joslin to provide for the surgical

management of lower-extremity lesions in patients

with diabetes at the New England Deaconess

Hospital. In 1949, Dr. McKittrick wrote:

Chemotherapeutic agents and the antibiotics have

made it possible to control invasive infection and the

mortality rate has fallen as anticipated. . .With the

danger of ascending infection and septicemia elimi-

nated, it might now be practical to consider each foot

on the basis of its arterial supply. In selected cases,

amputation might now be performed at a more distal

level with safety and a reasonable chance of

success. . ..18(p826)

Dr. McKittrick’s contributions to surgery were

wide ranging. He recognized that amputation of a

toe, in particular the great toe, with its metatarsal

head altered weightbearing and increased suscepti-

bility of the foot (toes and metatarsals) to further

injury. As a result, he preferred the ‘‘relative

security’’ of the transmetatarsal amputation. In

1951, Dr. McKittrick was joined by the general

surgeon Frank C. Wheelock Jr, MD (1919-2006).19

Dr. Wheelock became interested in the emerging

field of vascular surgery and was the first American

surgeon to use an end-to-side femoral popliteal

bypass graft. Drs. McKittrick, Wheelock, Carl Hoar,

and John Rowbotham helped New England Dea-

coness Hospital gain an unrivaled reputation for

managing the surgical complications of diabetes,

including minor amputations and distal bypass-

es.20-22 Vascular surgeons David R. Campbell, Gary

Figure 2. Leland Sterling McKittrick, MD (1893–1978),clinical professor of surgery, New England DeaconessHospital, Boston, Massachusetts. (Courtesy of theNational Library of Medicine.)

Figure 1. Elliott Proctor Joslin, MD (1869–1962),director of the George F. Baker Clinic, InternalMedicine, New England Deaconess Hospital, Boston,Massachusetts. (Courtesy of the National Library ofMedicine.)

Journal of the American Podiatric Medical Association � Vol 100 � No 5 � September/October 2010 319

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W. Gibbons, and Frank P. Pomposelli joined thisgroup in the 1980s. In 1981, Dr. Wheelock’s surgicalgroup started an annual diabetic foot conferencethat included podiatric physicians as faculty mem-bers. This conference attracted nationwide interestand played an important role in advancing theconcept of a multidisciplinary team approach toimproving diabetic foot care. Podiatric physiciansparticipated as members of the team. This relation-ship has evolved into a long-standing successfulpartnership between vascular surgeons and podiat-ric physicians and has served as a model for thecreation of other teams across the United States.

In 1957, the ambiguous term chiropodist waschanged to podiatrist because of public confusionwith the chiropractic profession. ‘‘The term chirop-odist was fatally encumbered with unfortunateconnotations and associations.’’13(p115) The newname, podiatrist, was actually the least ambiguousand most descriptive term; ‘‘pod’’ denotes the foot,and the Greek root ‘‘iatr’’ pertains to a physician orhealer. The National Association of Chiropodistsbecame the American Podiatry Association, whichin 1984 became the American Podiatric MedicalAssociation.

Evolution of Distal Revascularization andLimb Salvage

In 1984, Frank W. LoGerfo, MD, and Jay D. Coffman,MD, dispelled the widespread misconception ofarteriolar ‘‘small-vessel’’ occlusive disease in thediabetic foot in a landmark article published in theNew England Journal of Medicine.23 As noted byGary Gibbons and colleagues, ‘‘development ofmodern distal revascularization techniques wasdependent on the rejection of the concept of anocclusive microvascular lesion in the diabeticpatient with ischemic foot ulceration and recogni-tion of the pattern of tibial vessel occlusion withpedal reconstitution typical of this patientgroup.’’24(p578) Between 1984 and 1990, the Divisionof Vascular Surgery at New England DeaconessHospital made changes in their team managementof ischemic diabetic foot ulceration, with a dedicat-ed vascular unit, routine diagnostic arteriographyfor ischemia, a multidisciplinary team approachwith all disciplines, and an expanded role ofextreme distal revascularization (pedal bypass) torestore foot perfusion.24 The development of distalrevascularization techniques, in particular the dor-salis pedis bypass graft to restore pulsatile flow tothe forefoot, is most noteworthy. Increased empha-sis on foot preservation was noted in the 1990

group, ‘‘as seen in the increase in local podiatric

procedures and wound debridements with subse-

quent skin grafting.’’24 In 1992, Dr. LoGerfo and

colleagues noted:

Our increasing success with extreme distal arterial

reconstruction has greatly reduced the need for toe

or transmetatarsal amputation. Although these pro-

cedures still play a significant role in our prac-

tice. . .restoration of foot perfusion greatly enhances

our ability to perform direct foot-sparing surgery. In

association with our podiatry colleagues, these

procedures include metatarsal head resections and

osteotomies to preserve as much foot tissue and

function as possible.25(p620)

Podiatry attendings at New England Deaconess

Hospital at this time included Drs. Robert Frykberg,

Geoffrey Habershaw, James S. Chrzan, John Giurini,

and Barry Rosenblum.26, 27

During the 1990s, 1,032 bypasses to the dorsalis

pedis artery were performed in 865 patients in the

Division of Vascular Surgery at Beth Israel Deacon-

ess Medical Center. Ninety-two percent of the

patients had diabetes, and all of the procedures

were performed for limb salvage. Limb salvage was

defined as preservation of enough of the foot to

allow ambulation of the patient without the need for

a limb prosthesis. The most common indication for

surgery was a nonhealing ischemic foot ulcer.

Primary patency, secondary patency, limb salvage,

and patient survival rates were 56.8%, 62.7%, 78.2%,

and 48.6%, respectively, at 5 years and 37.7%, 41.7%,

57.7%, and 23.8% at 10 years.28 Dr. Pomposelli

presented the analysis of outcomes from this

retrospective study at the Fifty-sixth Annual Meet-

ing of the Society for Vascular Surgery in June 2002.

His conclusion was that pedal arterial reconstruc-

tion was a safe, simple, durable, and highly effective

procedure in a large patient cohort with advanced

limb ischemia of which more than 90% had diabetes.

Dr. George Andros attended the presentation and

commented: ‘‘I am absolutely drunk with delight. . .Ithink it is probably the most important diabetic

vascular paper in the 30-plus years that I have been

coming here. It is just an amazing series.’’28(p314)

Neuropathic Foot Ulcers and LessonsLearned From Leprosy

In 1965, Paul Wilson Brand, MD, FRCS (1914–2003)

(Fig. 3), a world-renowned orthopedic surgeon,

arrived at the US Public Health Service Hospital,

National Hansen’s Disease Center, in Carville,

Louisiana, the only leprosy hospital in the conti-

320 September/October 2010 � Vol 100 � No 5 � Journal of the American Podiatric Medical Association

Page 5: History of the Team Approach to Amputation Prevention · care, diet, exercise, prompt treatment of foot infections, and specialized surgical care. The history of the team approach

nental United States. He served as chief of the

Rehabilitation Branch. Dr. Brand, a modern-day

Father Damian, was the first surgeon in the world to

use reconstructive surgery to correct the deformi-

ties of leprosy in the hands and feet.

His interest in ulceration began in India in the

1940s with leprosy. He was told by leprologists that

it would be a waste of time to attempt surgical

reconstruction because patients with leprosy had

‘‘nonhealing flesh.’’29 Fingers were known to rot

away and fall off. Ulcers on the feet did not heal,

even if they were kept clean and medicated.

Regarding nonhealing flesh, Dr. Brand found that

if his surgical patients were kept in a plaster cast

after surgery, their wounds healed almost as fast

and securely as wounds on his patients without

leprosy. It quickly became apparent to Dr. Brand

that the failure of wounds to heal was due to the

way that the injured limbs were treated once

leprosy had robbed them of the protection of pain

sensation. He so eloquently described this as loss of

‘‘the gift of pain.’’

Dr. Brand defined the pathomechanics of soft

tissue in the insensitive foot and identified the

contributory role of three levels of mechanical

stress that could result in ulceration of the foot.30

One level required a high-force disruption of the

sole of the foot, common in his Indian patients with

leprosy, who walked barefoot and were subject to

highly localized pressure from thorns and sharp

stones. The second level of causation he believed to

be the continuous application of a much lower

force, just enough to keep an area of skin deprived

of its blood supply. As little as 2.0 psi acting

continuously over several hours would be enough to

cause gangrene of a patch of skin. This could easily

be caused by a tight bandage or ill-fitting shoe, and

it was frequently seen over areas of small radius of

curvature, eg, over the first and fifth metatarsal

heads.

Dr. Brand’s experiments with a living model, the

footpads of rats, demonstrated the role of repetitive

moderate stress (20 psi) on the footpads. Histologic

analysis of the skin after 2 days of 10,000 repetitions

a day revealed edema, hyperplasia of the epidermis,

and generalized inflammation of the footpad, with

incursion of inflammatory cells. After 7 days of the

same treatment, the rat footpad ulcerated. There

was gross hyperplasia of the epidermis around it.

Dr. Brand concluded that the actual destruction of

the skin was not due directly to the external force

but must be due to the chemical action of enzymes

released by inflammatory cells at the stimulus of

repeated moderate stress. He observed that the

inflammatory state developed before skin break-

down occurred and was accompanied by a notable

rise in the local skin temperature of the affected

part. Local temperature differentials (‘‘hot spots’’)were, therefore, an index of danger.

Dr. Brand translated his experience in the rat

model to management of the insensitive hands and

feet seen in Hansen disease and diabetes. Much of

what Dr. Brand learned in India and in the US Public

Health Service proved to be transferrable to

diabetes, and, in time, more diabetic patients than

patients with leprosy were treated in the foot clinic

at Carville:

I realized that here in America in the 1960’s the

management of foot ulceration in diabetics was

hindered by some of the same misconceptions that

I had faced about leprosy in the 1940’s. Ulcers in

diabetics were still called ‘diabetic ulcers’ rather than

neuropathic ulcers. They were looked upon by

surgeons as being a reason for amputation, because

they were thought to be unlikely to heal and go on to

gangrene of the foot. Much of this was because in

diabetes, unlike leprosy, there was often a real

Figure 3. Paul Wilson Brand, MD (1914–2003),renowned orthopedic hand surgeon and leprosyspecialist. Dr. Brand spent years researching thecause and effect of the neuropathic limb. (Courtesyof John H. Bowker, MD.)

Journal of the American Podiatric Medical Association � Vol 100 � No 5 � September/October 2010 321

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vascular problem, and this did sometimes cause

gangrene, even without neuropathy.29

The opportunity for technology transfer fromleprosy to diabetes occurred when J. K. Davidson,MD, PhD (1922–2008), Director of the Diabetes Unitat Grady Hospital in Atlanta, Georgia, visited withDr. Brand. Dr. Davidson brought his whole staffdown to Carville, and for several days there was anexchange of information. There was consensus thatneuropathy was the chief villain for the foot in bothdiseases. Dr. Brand learned that Dr. Davidson hadrecruited a podiatric physician, Edwin Hobgood,DPM (1938–2009), to work in his diabetes clinic.Their team achieved a 50% reduction in theamputation rate at Grady Hospital.1

In the early 1980s, Dr. Brand was joined by WilliamColeman, DPM, James Birke, PT, PhD, and CharlesPatout, MD. Their work refined the treatment ofneuropathic ulcers through an interdisciplinarymodel involving orthopedics, podiatric medicine,physical therapy, physical medicine and rehabilita-tion, and an on-site shoe shop, which customizedshoes and insoles and shoe modifications such as the‘‘rocker sole.’’31-36 Although their mission from theUS Public Health Service was for leprosy, thenumber of patients with diabetes steadily grew andquickly overwhelmed their resources. They realizedthat a program to screen and assess foot risk wasnecessary to prioritize the management needs ofthese patients. Furthermore, Dr. Brand and his teamdeveloped the philosophical precept that patientsneeded to be managed through the entire process ofcare, which included rehabilitation after effectivetreatment, and that this rehabilitation lasted alifetime because these patients would always be atrisk for repeated ulceration.

In 1986, physical therapists James Birke andDavid Sims published a paper on plantar sensorythreshold in the ulcerated foot and helped introducethe 10-gram monofilament screening test as amethod for assessing risk of ulceration.37 This ledto establishment of the Public Health Service’sLower Extremity Amputation Prevention (LEAP)program. The LEAP program was directed atnursing assessment to identify patients at risk butlacked a sufficient mechanism for follow-up in theprivate sector.33 The responsibility to train nursingstaff fell on Robert Rolfson, who traveled exten-sively promoting use of the 10-gram monofilamentand training nurses to perform foot screening andrisk assessment of patients. One obstacle to thesuccess of this program was that once patients werescreened and assessed for risk, there was no systemin place in the private sector for treatment. An

attempt to provide preventive foot care was

initiated in nearby Baton Rouge and was quickly

overwhelmed with patients seeking care. Because

diabetes was not the primary mission of the Carville

Public Health Service Hospital, it could not support

this effort.

Orthopedic Foot and Ankle Teams

F. William Wagner, MD (1917–present), was chief

consultant to the Orthodiabetes Service at the

Rancho Los Amigos Hospital in Downey, California,

and chief of the Foot Service, Los Angeles County,

University of Southern California Medical Center,

where he assembled a very successful multidisci-

plinary team for management of the diabetic foot.

He was instrumental in raising awareness of the

dysvascular diabetic foot and for developing a

grading system for diabetic foot lesions. The

Wagner-Meggitt classification was developed

through observing the progression of diabetic foot

lesions from callus, to ulcer, to abscess, to

gangrene, and, finally, to surgical ablation. Dr.

Wagner promoted the use of Doppler ultrasound

and the ischemic index for vascular evaluation of

the diabetic foot. He was a pioneer in the emerging

specialty of foot and ankle orthopedics, and his 1981

monograph on the dysvascular foot remains a

classic reference today.38 Other successful multi-

disciplinary orthopedic teams evolved during the

1980s and 1990s headed by John H. Bowker (Miami,

Florida), Ernest Burgess (Seattle, Washington),

Richard L. Jacobs (Albany, New York), James W.

Brodsky (Dallas, Texas), Michael Pinzur (Maywood/

Chicago, Illinois), Douglas G. Smith (Seattle), Mark

S. Myerson and Lew Shon (Baltimore, Maryland),

Jeffrey E. Johnson (St. Louis, Missouri), Charles

Saltzman (Iowa), and Paul Juliano and Dane Wukich

(Pennsylvania).

Professional Education, Research, andthe Team Approach

American Diabetes Association

The American Diabetes Association has played a

pivotal role in promoting a multidisciplinary team

approach to the management of diabetes and its

complications. It is the leading voluntary health

organization in the United States dedicated to

finding a cure for diabetes, raising awareness of

the complications of diabetes, funding diabetes

research, and developing clinical practice recom-

322 September/October 2010 � Vol 100 � No 5 � Journal of the American Podiatric Medical Association

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mendations and performance measures to ensurequality diabetes care. The American DiabetesAssociation’s first technical review on preventive

foot care and its position statements on preventivefoot care, wound care, and peripheral arterial

disease have influenced clinical practice and dia-betic foot care across the United States and aroundthe globe.39-41 The American Diabetes Association’s

annual scientific sessions have provided a forum forthe exchange of information pertaining to thediabetic foot. In the 1980s and 1990s, a small and

diverse group of podiatric physicians (LawrenceHarkless, Leon Brill, John Giurini, Lee J. Sanders,

Ron Sage, Robert Frykberg, Stephen Albert, WilliamColeman, Richard Stess, and Peter Graf), endocri-nologists (Marvin Levin, Andrew J. M. Boulton,

Solomon Rosenblatt, Victor Roberts, Carl Grunfeld,Roger Pecoraro, Aris Veves, Jan Ulbrecht, Peter

Sheehan, and Leonard Pogach), orthopedists (JohnBowker and Richard Chambers), an epidemiologist(Gayle Reiber), a biomechanist (Peter Cavanagh),

pedorthist (Dennis Janisse), a rehabilitation spe-cialist (Phala Helm), a family physician (JenniferMayfield), and nurses gathered at this meeting to

attend the Council on Foot Care scientific programfor the exchange of ideas and to discuss their

research.

Lawrence B. Harkless, DPM, was elected the firstchair of the Council on Foot Care (1987–1989) andwas then appointed to the American Diabetes

Association National Board of Directors. Lee J.Sanders, DPM, followed as chair of the Council on

Foot Care (1993–1995), as a member of theAmerican Diabetes Association National Board ofDirectors (1996–2002), and as a member of the

American Diabetes Association Executive Commit-tee (1998–2001). He became the American DiabetesAssociation’s president, Health Care and Education

(2000–2001), an important milestone for the podiat-ric medicine profession.

Marvin E. Levin, MD (1924–present)—Clinicianand Educator

The collaboration between diabetologist Marvin E.

Levin, MD (Fig. 4), and endocrine surgeon LawrenceW. O’Neal, MD (1923–present), at Washington Uni-

versity, St. Louis, proved to be a very fruitfulpartnership. In the late 1960s, over lunch, Drs.Levin and O’Neal conceived the idea for a complete

and concise textbook on the care and treatment ofthe diabetic foot. Major medical textbooks at thistime had only abbreviated coverage of the subject,

consisting primarily of hygienic care of the foot. In

1973, the first edition of The Diabetic Foot was

published, with 10 chapters and 12 contributing

authors, all faculty at the Washington University

School of Medicine.42 The book contained a chapter

on podiatry and the podiatrist’s role in diabetes care

written by Oscar Lippard, DPM. This book became

the ‘‘bible’’ for an emerging generation of diabetic

foot specialists. After nearly four decades, the

seventh edition of The Diabetic Foot, published in

2008, contains 33 chapters with 58 contributing

authors and remains the most authoritative refer-

ence book on this subject.43 A dynamic lecturer,

author, and educator, Dr. Levin has truly been a

disciple for the team approach to management of

the diabetic foot and has been a role model for

many of the thought leaders in the diabetic foot

community today. He received the American Diabe-

Figure 4. Marvin E. Levin, MD (1924–present),adjunct professor of medicine and previous associatedirector of the Diabetes, Endocrinology, and Metabo-lism Clinic, Washington University School of Medicine,St. Louis, Missouri. Dr. Levin is a renowned diabetol-ogist and educator and is emeritus editor of TheDiabetic Foot.

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tes Association’s Outstanding Physician in Diabetes

Award in 1979. Dr. Levin’s pioneering efforts led to

establishment of the American Diabetes Associa-

tion’s professional section Council on Foot Care in

1987.

Lawrence B. Harkless, DPM—Clinician,Educator, and Politician

For more than 30 years, Dr. Harkless directed the

podiatric medical residency program at the Univer-

sity of Texas Health Science Center at San Antonio.

He was a professor in the Department of Orthope-

dics and the Louis T. Bogy Professor of Podiatric

Medicine and Surgery. During 3 decades, he trained

more than 165 residents and 1,000 students,

establishing his status as one of podiatric medi-

cine’s best educators. In 1984, he established The

Diabetic Foot Update: A Multidisciplinary Ap-

proach, an annual continuing medical education

program with a nationally known faculty (Fig. 5). In

2001, Dr. Harkless was honored by the American

Diabetes Association as Diabetes Educator of the

Year. In the same year, he was appointed by Texas

Governor Rick Perry to a 3-year term as chairman of

the Texas Diabetes Council, Texas Department of

Health. His success can be measured by the many

successful podiatric physicians he has trained, the

limbs he has salvaged, and the improved quality of

life he has provided to his patients. Among his many

notable alumni are David G. Armstrong, Lawrence

Lavery, and John Steinberg. In 2007, Dr. Harklessaccepted a new challenge as the founding dean ofthe College of Podiatric Medicine at the WesternUniversity of Health Sciences in Pomona, Califor-nia.

Postgraduate Training and the TeamApproach

Growth of postgraduate training programs andresearch were critical to the advancement ofpodiatric medicine during the 1980s, the 1990s,and the first decade of the 21st century. A significantadvancement in the evolution of residency trainingprograms occurred in 2003 with the Council onPodiatric Medical Education’s adoption of two newresidency categories. Podiatric medicine and sur-gery 24- and 36-month programs are now thestandard. Fellowships in limb salvage, wound care,and diabetic foot research have added additionalopportunities for postgraduate specialty training.Comprehensive standardized training has helpedclarify any ambiguity in the medical communityregarding the scope and quality of podiatric medicaleducation. Podiatric physicians and allopathicphysicians train side by side in hospitals acrossthe United States, promoting the interdisciplinarymanagement of the patient as a whole and thepodiatric physician’s role on the health-care team.

Podiatric Medicine and Research

In the past two decades, great strides in researchhave been made through the efforts of severalpodiatric physician scientists who have madesignificant contributions to our understanding ofthe pathogenesis, management, wound healing, andepidemiology of the diabetic foot. David Armstrong,DPM, MD, PhD, Lawrence Lavery, DPM, MPH,Adam Landsman, DPM, PhD, Vickie Driver, DPM,and James S. Wrobel, DPM, are among the mostrespected and prolific researchers in this field.Studies by Drs. Armstrong and Lavery include riskand wound classification systems of the diabeticfoot, risk assessment, foot pressure measurementsin off-loading, activity monitoring, prevention in adisease management model, the impact and costs oflower-extremity amputations, risk factors for footinfections, and home monitoring of foot skintemperature to prevent ulceration.44-51 Dr. Arm-strong’s ‘‘toe and flow’’ message resonates with theimportance of collaboration between podiatricphysicians and vascular surgeons to achieve suc-cessful and lasting limb salvage.

Figure 5. Some thought leaders and pioneers in theevolution of a team approach to amputation preven-tion. The Diabetic Foot Update: A MultidisciplinaryApproach, December 8–9, 1990, San Antonio, Texas,faculty: front row (left to right): Andrew J. M. Boulton,Paul W. Brand, Gayle E. Reiber, Marvin E. Levin, andRoger Pecoraro; back row (left to right): Louis T. Bogy,W. Preston Goforth, Lawrence B. Harkless, RaphaelKilcoyne, Lee J. Sanders, and F. William Wagner.

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Government Health Care, Teams, andSystem Changes

As orthopedic teams were developing across the

United States in the 1980s and 1990s, so weremultidisciplinary diabetic-foot–care teams coordi-nated by podiatric physicians and diabetes special-ists at Veterans Affairs hospitals. A nationalnetwork of podiatric physicians with a passion forlimb preservation worked diligently to meet the

needs of an aging population of veterans withchronic diseases, in particular diabetes. Thesepioneering podiatrists labored hard, often underdifficult and discriminatory conditions, to establishtheir role as members of the team. Through collab-

oration with other medical and surgical specialists,they demonstrated the value of preventive foot care,the utility of therapeutic footwear and orthoses, andthe success of local podiatric surgical procedures andlimb-sparing operations.52-59 Some of the early teams

were headed by Richard Stess, Peter Graf, and CarlGrunfeld (San Francisco [California] Veterans AffairsMedical Center); Ronald A. Sage, Rodney M. Stuck,and Michael P. Pinzur (Hines Veterans Affairs MedicalCenter Chicago); Lee J. Sanders and Terry D. Weaver

(Lebanon Veterans Affairs Medical Center Pennsylva-nia); Samuel Mason and C. Gene Wheeler (Phoenix[Arizona] Veterans Affairs Medical Center); BrentNixon and David Armstrong (Tucson [Arizona]Veterans Affairs Medical Center); Stephen Albert

(Denver [Colorado] Veterans Affairs Medical Center);and James Wrobel and William Chagares (VeteransAffairs Medical Center North Chicago). During thisperiod, seminal contributions to our understanding ofthe causal pathways of diabetic limb amputation and

ulceration were made by Roger Pecoraro and GayleReiber at the Seattle Veterans Affairs MedicalCenter.60, 61 Other members of the multidisciplinarydiabetes team at the Seattle Veterans Affairs MedicalCenter included Linda Haas, Jessie Ahroni, Margue-

rite J. McNeely, Edward Boyko, Douglas Smith, andinfectious disease specialist Benjamin Lipsky. At theCenter for Health Services Research in Primary Care,Durham (North Carolina) Veterans Affairs MedicalCenter, David Edelman and colleagues demonstratedthat a validated risk stratification foot examination for

diabetic patients was reproducible and largely accu-rate when performed by primary-care providers.54

Building on the success of the Public HealthService Hospital in Carville, the Department ofVeterans Affairs developed the Special Teams forAmputation, Mobility, and Prosthetics/Orthotics

(STAMP) program in 1985. This program estab-lished eight centers of excellence striving to

improve the quality and availability of services toveterans who had already undergone amputation.

The program focused on rehabilitation but not onprevention. The Veterans’ Medical Programs

Amendments of 1992 (PL102–405) emphasized theimportance of highest-quality amputee care and

identified veterans with amputation as a specialdisability group. The Advisory Committee on

Prosthetics and Special Disabilities Programs waschartered to oversee compliance. In 1993, under the

direction of Fred Downs (National Director of theProsthetics and Orthotics Service) and the leader-

ship of Leonard Pogach, MD (National Director ofDiabetes), the Veterans Health Administration

launched the Preservation-Amputation Care andTreatment (PACT) program through Veterans

Health Administration Directive 1993–060. Thisnational initiative was designed to meet the

changing needs of veterans with fewer traumaticamputations but with chronic disease, often with

neuropathic and ischemic complications, thatplaced them at risk for ulceration and amputation.

This directive established a model of care to prevent

or delay amputations through proactive earlyidentification of at-risk populations, primarily vet-

erans with diabetes. The major goal of the PACTprogram was to prevent amputation or repeated

amputation. The PACT program objectives included1) identifying patients at risk for amputation,

specifically veterans with diabetes, end-stage renaldisease, or peripheral vascular disease; 2) perform-

ing annual foot screening examinations; 3) assigningeach patient a risk score based on findings from foot

screening; 4) providing timely and appropriatereferral for professional foot care; and 5) tracking

patients from the date of entry through the systemof care.

There have been three additional reissues of thePACT program directive, each building on the

experiences of the preceding directive. The firstdirective established the program in 1993, and the

second, in 1996, tied performance measures toprimary-care providers to focus attention on the

need to complete foot screening on at-risk patientsand establish metrics to track compliance. The third

directive, in 2001, established a system to identifypatients and track them through the system of care

to provide some way to monitor whether patientswere getting what they needed. The latest directive

was issued in 2006 and established unique system-wide data cubes to allow individual station coordi-

nators access to data about risk factor measures,ulcers, and amputations and to provide information

to assess their systems of care.62 These data cubes

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are unique in health care because they providesystem-wide information designed to allow Veter-ans Affairs medical centers to monitor clinicalmeasures to assist them in improving their PACTprograms. The three cubes are 1) the PACT cube,which includes information about risk categoriesand the medical diagnosis of conditions that placepatients at increased risk, such as neuropathy,neurogenic arthropathy (the Charcot foot), andother foot deformities; 2) the ulcer cube, whichcollects information on ulcer type and cause; and 3)the amputation cube, which looks at major, minor,above-the-knee, and below-the-knee amputationratios. All three cubes also provide mortality data.Recent studies63, 64 have documented high mortalityrates associated with diabetic ulcers and amputa-tion, highlighting the need to promote self–foot carebehaviors. The directive also recognizes the need toallow returning Operation Enduring Freedom andOperation Iraqi Freedom veterans who have suf-fered a traumatic amputation to access the systemof care. The objective is to preserve the remaininglimb and to provide for their mental health needs inadjusting to their loss. In addition, the directiveplaced the director of the Podiatry Service aschairman of the PACT Oversight Committeecharged with overseeing the program’s continueddevelopment.

In response to a system-wide need for monofila-ments, the director of the Podiatry Service, JeffreyRobbins, DPM, partnered with Robert Rolfson todevelop a monofilament giveaway program for theVeterans Health Administration. To date, thisongoing program has provided more than onemillion monofilaments since 1999. This programwas awarded the Hammer Award for reinventinggovernment and the Scissors Award for cutting redtape in 1999. Another innovation was the develop-ment of a clinical reminder template to facilitateearly screening risk assessment and timely referralfor all patients deemed to be at risk for amputation.This includes patients with diabetes, end-stage renaldisease, and peripheral vascular disease. Thisclinical reminder is automatically added to thepatient’s electronic medical record in the VeteransHealth Administration’s Computerized Patient Re-cord System, reducing the chance of at-risk patientsbeing missed by the system.

United Kingdom and European Initiatives

Robert Daniel (R. D.) Lawrence, MD, FRCP (1892–1968), was a contemporary of Drs. Banting andJoslin. His connection to diabetes mellitus was very

personal as he himself was diagnosed as havingdiabetes at the age of 28, receiving his first injectionof insulin in May 1923. The priceless discovery ofinsulin gave him a new lease on life, which hedevoted to understanding and treating diabetes. Dr.Lawrence was the physician in charge of theDiabetic Clinic at King’s College Hospital from1931 to 1957. He recognized the importance ofdiabetes education and founded the British DiabeticAssociation and the International Diabetes Federa-tion.65-67 He considered the diabetic foot to be dueto an infected suppurative arthritis of the meta-tarsophalangeal joint, and he believed that the footcould be salvaged with limited surgical treatment,eg, partial ray resection, avoiding amputation. In1941, Dr. Lawrence approached K. C. McKeown,MD, a surgeon in the Emergency Medical Service atKing’s College Hospital, and requested that heperform a wedge resection of the affected meta-tarsophalangeal joint and related toe in a diabeticpatient. The first operation was successful, and thisprocedure was subsequently used by Dr. McKeownfrom 1941 to 1944.68 Wilfrid Oakley, R. C. F.Catterall, and M. Mencer Martin published acomprehensive report on diabetic peripheral arteri-al disease, neuropathy, infection, and gangrene in1956. They drew attention to the importance ofneuropathy alone and in association with ischemiaas a factor in the production of localized ulcerationand gangrene.69

Team Approach in Europe: 1980–2010

In 1979, Michael Edmonds, MD, began a researchfellowship with Peter Watkins at King’s CollegeHospital investigating blood flow in the neuropathicfoot. He was impressed by the overwhelmingburden of ‘‘the diabetic foot’’ in vulnerable patientswith multiple comorbidities with ischemic andneuropathic feet. Dr. Edmonds recognized the needfor coordinated intensive care of these patients withinput from several disciplines, including diabetol-ogy, podiatric medicine, orthotists, nursing, medi-cine, and orthopedic and vascular surgery. In May1981, at the invitation of podiatric physician MaryBlundell, Dr. Edmonds established a diabetic footclinic in the Podiatry Department at King’s CollegeHospital. The objective of this clinic was to managethe distinctive lesions of the neuropathic andischemic diabetic foot. This initiative led to inten-sive management of the patient with diabetic footby a multidisciplinary team and resulted in animmediate reduction in major amputations by 50%.Specific emphasis was placed on podiatric medical

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debridement, off-loading, infection control, anddiabetes care. Podiatric physician Alethea V. M.Foster joined the clinic in 1985. Aware that the

diabetic foot could deteriorate with alarmingrapidity, she emphasized an open-access service,

with the diabetic foot clinic acting as a first aidcenter, seeing emergencies on the same day orwithin 24 hours. An early report of this multidisci-

plinary service was presented at the Dublin (Ire-land) meeting of the British Diabetic Association inSeptember 1982 and at the European Association

for the Study of Diabetes meeting in London in1984.2

Following the successful outcome of reducing

amputations in the King’s College Hospital clinic,multidisciplinary diabetic-foot–care teams devel-oped throughout Europe. It was accepted that the

foot ulcer was a sign of severe systemic disease.These patients required holistic care as well as focal

treatment of their lower limbs. The presentation ofa diabetic patient with a foot ulcer was a pivotalevent in the life history of that patient. It was clear

that patients with diabetic foot disease requiredspecialized care by a multidisciplinary team work-

ing not only in a dedicated diabetic foot clinic butalso caring for the patient when admitted to thehospital. For this reason, in Europe the diabetolog-

ist has often taken a major role in direction of themultidisciplinary team, although not exclusively asvascular surgeons and orthopedic surgeons have

also been prominent. Important day-to-day care hasoften been led by podiatric physicians and some-

times by nurses. Many teams began with minimalstaff but have evolved into full multidisciplinaryteams active in research and education.

Role of Patient Education

Jean-Philippe Assal, MD, was chief of the Diabetes

Treating and Teaching Unit at the UniversityHospital in Geneva, Switzerland, a World HealthOrganization collaborating center for research in

diabetes education. Dr. Assal played an importantrole in instigating awareness of patient educationand a global integrated approach to diabetes care.

He taught that diabetes education was a fundamen-tal aspect of the management of foot ulcers in

patients with diabetes. Dr. Assal reported thatamputations of the foot were notably diminishedby more than 50% in 4 years with patient education.

He achieved this by organizing courses for diabeticpatients on the care of their feet and early detectionand treatment of lesions on the lower limbs. Each

diabetic patient attended a 2-hour course, and two

outpatient consultations were conducted for thoseat high risk with infections, plantar ulcers, andarterial insufficiency. At the time of consultation,

education on preventive measures was continued.

To determine the effect of these courses and earlyconsultations, the level of amputation of 34 diabetic

patients operated on at the orthopedic clinic duringthe previous 18 months was studied. Of 23 patientswho underwent below-the-knee amputation, 22 had

never been informed of preventive measures orearly treatment. Of 11 patients with distal (big toe ortransmetatarsal) amputation, all had benefited from

the minimal intervention as a result of the systemof information and early consultation and treat-

ment. The average hospital stay was 111 days forbelow-the-knee amputations and 26 days for distalamputations.70, 71

The 1980s

Throughout the 1980s, multidisciplinary clinics wereestablished in the United Kingdom and Europe. The

diabetic foot clinic at the City Hospital Nottingham(Nottingham, England) was set up in 1982 by WilliamJeffcoate, and in 1987, multidisciplinary clinics were

instituted at the Blackburn Royal Infirmary (Black-burn, England) by Geraint Jones and at the Man-

chester Royal Infirmary (Manchester, England) byAndrew J. M. Boulton.72 In Lund, Sweden, JanApelqvist became the director of a multidisciplinary

foot-care center with coordinated inpatient andoutpatient facilities in 1983. The team consisted ofa diabetologist, orthopedic surgeons who special-

ized in foot surgery, a vascular surgeon, a podiatricphysician, a physiotherapist, a casting technician, anorthotist, and diabetes nurse educators. The diabetic

foot clinic acted as a referral unit for severediabetes-related complications: ulcers, infection,

ischemia, osteoarthropathy, and neuropathy.5

In 1984, a diabetic foot clinic at the University ofDusseldorf, Dusseldorf, Germany, was establishedby Max Spraul and Ernst Chantelau with a minimal

model, starting with two doctors and a nurse andlater developing into a full multidisciplinary team.

Similarly, diabetologist Kristien Van Acker launchedthe first diabetic foot clinic in Belgium at theUniversity of Antwerp in 1989. She started this

clinic with two nurses; however, after 14 years, alarge multidisciplinary team was in place. EzioFaglia, working in the Diabetology Centre, Niguarda

Hospital, Niguarda, Italy, demonstrated a reductionin the major amputation rate at a multidisciplinarycenter dedicated to diabetic foot care during the

1980s.73, 74

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At the end of the decade, the St. VincentDeclaration encouraged the development of multi-disciplinary clinics in Europe. Representatives ofgovernment health departments and patient organi-

zations from all of the European countries met withdiabetes experts under the aegis of World HealthOrganization Regional Offices for Europe and theInternational Diabetes Federation, European region,

in St. Vincent, Italy, on October 10 to 12, 1989. Theyunanimously agreed on the recommendations toimprove diabetes care and urged their implementa-tion in all of the countries throughout Europe. This

included a recommendation to reduce by half therate of limb amputations for diabetic gangrenewithin 5 years, a target derived from the 50%reduction in amputations achieved by the King’s

College Hospital Foot Clinic.

The 1990s

The neuroischemic foot was becoming an increas-ing problem in the 1990s. When the diabetic footclinic at King’s College Hospital was set up in 1981,

it prevented nearly all major amputations ofneuropathic feet. At that time, it was difficult toachieve similar results with the ischemic footbecause advanced occlusive arterial disease below

the knee could not be reversed. However, with thedevelopment of modern techniques for peripheralangioplasty and distal bypass, the foot clinicachieved a further 50% reduction in major amputa-

tions of the ischemic foot.75

With the increasing use of kidney transplantation,

patients with diabetes in renal failure and with footproblems increasingly presented to diabetic footclinics. Alethea V. M. Foster, working in a specializedfoot clinic at King’s College Hospital, demonstrated a

reduction in gangrene and amputations in diabeticrenal transplantation patients (Fig. 6).76 Diabeticischemic foot patients with end-stage renal diseaseare typically the most difficult to treat because of the

presence of diffuse disease, greater involvement ofthe distal and pedal vessels, and extensive tissuenecrosis. Remarkably, it was demonstrated thatdistal bypass could be performed safely and effec-

tively with acceptable rates of limb salvage inpatients who had undergone renal transplantationand in dialysis-dependent patients.77, 78

The Rise of Multidisciplinary Diabetic FootClinics in Europe

Enthused by the St. Vincent Declaration, the teamapproach to diabetic foot care developed steadily in

the 1990s. Several major centers developed in Italy.

The unique nature of these centers was that they

were directed by endocrinologists who performed

emergency and elective foot surgery. This new

specialty of surgically trained diabetologists

evolved through the efforts of a talented and

dedicated group of physicians: Alberto Piaggesi,

Luca Dalla Paola, Carlo Caravaggi, Ezio Faglia, and

Luigi Uccioli.

In 1991, Dr. Piaggesi held the post of consultant at

the Department of Endocrinology and Metabolism,

University of Pisa, Pisa, Italy, where he was

responsible for the lower-limb complications unit

and where he set up and managed the diabetic foot

clinic that is now the referral center for Tuscany

and central Italy. The Abano Diabetic Foot Depart-

ment, directed by Dr. Paola, had 26 beds for

inpatients, with an outpatient clinic, a catheter

laboratory, four intensive care unit beds given over

to patients with diabetic foot, collaboration with the

vascular surgery department, and two operating

rooms for diabetic foot treatment. Dr. Uccioli, in his

multidisciplinary clinic in Rome, demonstrated the

value of manufactured shoes in the prevention of

diabetic foot ulcers.79

Per E. Holstein, who had been a consultant

orthopedic surgeon at the Steno Diabetes Center,

Copenhagen, Denmark, and chief vascular surgeon

at the Department of Thoracic and Vascular

Surgery, Bispebjerg Hospital, University of Copen-

hagen, founded a multidisciplinary diabetic foot

clinic in the Bispebjerg Hospital in 1993. He

demonstrated a 75% reduction in the incidence of

major amputations, which coincided with a seven-

Figure 6. The Diabetic Foot Clinic, King’s CollegeHospital, London, England, November 2001. Front row(right to left): Alethea V. M. Foster, chief podiatrist; LeeJ. Sanders, DPM, visiting professor; and MichaelEdmonds, MD, consultant physician.

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fold increase in revascularization procedures andthe establishment of a multidisciplinary diabeticfoot clinic.3

In Eastern Europe, Vilma Urbancic-Rovan startedan outpatient diabetic foot clinic at UniversityMedical Centre Ljubljana, Ljubljana, Slovenia, in

1990. Diabetic foot clinics were also set up inPrague, Czech Republic (Alexandra Jirkovska), andMoscow, Russia (Irina Gourieva). Multidisciplinaryclinics were also being organized on a national

basis. William Van Houtum reported a reduction indiabetes-related lower-extremity amputations in theNetherlands between 1991 and 2000.10

Screening and Preventive Foot Care

Most of these pioneering clinics were hospital

based and treated active foot problems; however,there was an increasing awareness of the need forscreening and preventive foot care. Programs ofpreventive care in the form of screening for high-

risk patients and then enrollment in a footprotection program achieved reductions in footulcer incidence and amputations.80, 81 The com-munity-based Integrated Diabetic Foot Care Pro-ject in Exeter, England, demonstrated that pa-

tients’ knowledge of and attitudes toward theirfoot care, as well as the knowledge and behaviorof health professionals, can be measurably en-hanced, relatively inexpensively, in a fairly short

time.82, 83

Initiatives to Support the Team Approach

There were two important European initiatives atthe end of the 1990s to support and encourage theteam approach to diabetic foot care and amputation

prevention. The Diabetic Foot Study Group of theEuropean Association for the Study of Diabetes wasset up in 1998 through the motivation of Andrew J.M. Boulton. This study group, under the leadershipof its successive chairmen (Andrew J. M. Boulton,

Michael Edmonds, Stephan Morbach, and EdwardJude) has organized annual meetings on clinical andresearch aspects of the diabetic foot.

By the mid-1990s, it was accepted that a teamapproach with a well-structured organization inappropriate facilities could reduce the risk of

development and progression of diabetic foot ulcerdisorders. However, many different strategies wereapplied in diabetes foot care. Sir Karel Bakker, MD,chairman of the successful International Symposia

on the Diabetic Foot in Noordwijkerhout, theNetherlands, in 1991 and 1995, noted that although

guidelines on the prevention, diagnosis, and man-agement of diabetic foot problems had beenformulated in several countries, the contents ofthese guidelines were sometimes inconsistent.There was a need for an international set ofdefinitions and guidelines on prevention and man-agement, and this led to formation of the Interna-tional Working Group on the Diabetic Foot, a uniquemultidisciplinary team of experts on the diabeticfoot that included general practitioners; diabetolog-ists; podiatric physicians; diabetic nurses; andgeneral, vascular, and orthopedic surgeons.Through a process of consensus, this groupproduced a document entitled the ‘‘InternationalConsensus on the Diabetic Foot.’’ This consensus,accompanied by practical guidelines, was launchedduring the Third International Symposium on theDiabetic Foot in Noordwijkerhout in 1999 and wasto motivate the team approach through the nextdecade.

Research and the Team Approach inEurope: 21st Century

The first decade of the 21st century was notable forlarge cohort studies that investigated factors relatedto diabetic foot outcomes and for multidisciplinaryclinics treating the ever-increasing number ofneuroischemic patients often in some degree ofrenal failure. Increasing interest in the Charcot footled to early intervention with casting and surgicalreconstruction for late-presenting deformed feet.The decade also saw further advances in interna-tional consensus, national frameworks of diabeticfoot care, and organization of diabetic foot clinicson a national scale.

Cohort Studies Assessing Factors Related toOutcome

In this decade, large cohort studies have describedclinical outcomes and factors related to outcomes.A collaboration of 14 European centers performeda prospective data collection study, the Eurodialestudy, in which 1,229 patients with a diabetic footulcer were followed until healing. Nicolaas Schaperwas the founding father and coordinator of thisproject and was assisted by Leonne Prompers andMaya Huijberts at the pivotal base of Maastricht,the Netherlands. Other members were Jan Apelqv-ist, Edward Jude, Alberto Piaggesi, Karel Bakker,Michael Edmonds, Per Holstein, Alexandra Jirkov-ska, Dedac Mauricio, Gunnel Ragnarson Tennvall,Heinrich Reike, Max Spraul, Luigi Uccioli, Vilma

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Urbancic, Kristien Van Acker, and Jeff Van Baal. A

further series of consecutively presenting pa-

tients with diabetes and foot ulcer (n = 2,511)

was prospectively followed and treated according

to a standardized protocol until healing was

achieved or until death.84 Data from these studies

gave a unique overview of the risk factors and

pathogenesis of diabetic foot ulcers throughout

Europe. More than 50% of diabetic patients with a

foot ulcer had signs of infection on initial exami-

nation by a hospital-based multidisciplinary foot-

care team. Fifty percent of these ulcers were of

neuroischemic origin, and one-third of the patients

with a foot ulcer had signs of peripheral arterial

disease and infection. These studies showed that

outcome was strongly related to severity of

comorbidities and confirmed that infection is a

major problem in the diabetic foot, particularly in

the presence of ischemia.

Multidisciplinary Teams, Revascularization, andLimb Salvage

Revascularization became a crucial part of the

diabetic foot service in this decade. Peripheral

angioplasty of the distal arteries down to the foot

arteries was found to be safe and effective for limb

salvage in a high percentage of diabetic patients.85

In an integrated care pathway at King’s College

Hospital, distal bypass performed by Hisham Rashid

became a vital part of the diabetic foot service.

Technical advances in revascularization, including

distal angioplasty, have been strengthened by

intensive multidisciplinary care for the management

of comorbidities and multiple diabetes complica-

tions.86 In such an integrated-care pathway, angio-

plasty and bypass were regarded not as competing

treatments but as complementary. It was important

that each intervention be applied in a timely and

appropriate manner. Coordination was accom-

plished within the organizational framework of a

weekly joint vascular clinic attended by vascular

surgeons and diabetologists and a vascular radiol-

ogy meeting also attended by the interventional

radiologist and vascular laboratory scientist. Angio-

grams were reviewed, and joint decisions were

made as to the suitability of angioplasty (often

performed as a day case procedure) or, alternative-

ly, arterial bypass after careful review of the

patient’s comorbidities. After either procedure,

patients were followed up closely in the diabetic

foot clinic to assess the clinical outcome and the

need for further intervention.87 Similar patterns of

care have now been established in many centers in

Europe.

System Changes, Research, andReduction in Amputation Rates

After initially reporting an unchanged incidence of

amputation in Leverkusen, Germany, between 1990

and 1998,88 a multidisciplinary service including an

interdisciplinary ward for inpatient treatment as

well as preoperative and postoperative care was

opened in 2001. This ward served as a central unit.

Patients would return to this unit after surgery for

integrated treatment of their wounds, infection, and

metabolic problems. As a rule, surgery was per-

formed only after common indication rounds with

the diabetologists and surgeons. After surgery, so-

called problem rounds followed regularly. Standard-

ized, phase-adapted wound care was performed

after rigorous debridement. When indicated, revas-

cularization was an integral part of treatment.

Antiseptics, antibiotics, moist semi-occlusive dress-

ings, maggots, and vacuum-assisted wound closure

therapy are all components of this treatment

scheme. When patients were discharged, they

continued to be treated by the now established

outpatient network. Overall, this standardized ap-

proach has eventually contributed to a reduction in

amputations.9

Reductions in the number of amputations have

also been reported by Gerry Rayman in Ipswich,

England,4 Ronan Canavan in Middlesborough,

England,89 Clifford Shearman in Southampton,

England,90 and Roberto Anichini in Italy.91 In

Helsinski, Finland, the emphasis on active vascular

intervention has resulted in a decrease in the

incidence of major amputation in nondiabetic and

diabetic patients,92 and in Scotland, Matthew Young

at the Edinburgh Diabetic Foot Clinic reported a

decrease in mortality in patients with diabetic foot

after aggressive treatment of vascular risk fac-

tors.93

Research has been a prominent feature of many

diabetic foot clinics, with work presented at

national and international meetings and at meetings

related to the diabetic foot, eg, the Diabetic Foot

Study Group and the biennial Malvern Diabetic Foot

Conference. In 2002, William Jeffcoate and Fran

Game set up a Foot Ulcer Trials Unit in Nottingham,

England. They recently reported the outcomes of

two studies coordinated from that center. The first

study looked at the role of education for ulcer

prevention,94 and the second study was a three-way

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investigation of the effect of dressings on diabetic

foot ulcer healing.95

International Consensus, NationalFrameworks, and Organization ofDiabetic Foot Care

In 2000, the International Working Group on the

Diabetic Foot became the International Diabetes

Federation’s consultative section on the diabetic

foot. Following the 1999 ‘‘International Consensus

on the Diabetic Foot,’’ the International Working

Group on the Diabetic Foot produced three

supplements in 2003 on infection, classification of

wounds, and wound healing. In 2007, the ‘‘Interna-

tional Consensus on the Diabetic Foot’’ was

updated and three new guidelines were issued on

wound and wound bed management, treatment of

diabetic foot osteomyelitis, and footwear and off-

loading.

In 2003, the German Working Group on the

Diabetic Foot developed certification requirements

for diabetic foot centers. These requirements

established procedures by which specialized cen-

ters for the treatment of the diabetic foot syndrome

could verify the quality of their management. The

goal was to establish comparable centers with

clearly defined treatment structures. Interested

centers submitted applications for assessment of

inpatient or outpatient diabetic foot care. Applica-

tions were then checked by a certification commit-

tee for correctness and completeness. For the

evaluation, each center documented 30 consecu-

tively seen individuals with diabetic foot lesions,

and outcome evaluations of these were performed 6

months after the initial presentation.96

A similar system of audit, certification, and

benchmarking was developed in Belgium under

the guidance of Kristien Van Acker. Diabetic foot

clinics were required to fulfill special criteria. They

had to show evidence of their management of 52

new diabetic foot ulcers with Wagner grade 2 or

Charcot foot per year. In addition, there must be

specialized centers with 24-hour availability, and

the interdisciplinary team must be present at the

outpatient clinic at least 48 weeks a year and a

minimum of half a day a week. Minimum composi-

tion of the team must include a diabetologist,

surgeon, podiatric physician, nurse/educator, and

orthotist.

In the United Kingdom, a government pledge in

2001 was published to improve diabetes care across

the board. This was called the Diabetes National

Service Framework. The Diabetes National Service

Framework called for the first ever set of national

standards for the treatment of diabetes, including 12

standards covering all aspects of diabetes care and

prevention. Together with an accompanying deliv-

ery strategy, the Diabetes National Service Frame-

work outlined a 10-year program (2003–2013) of

change and improvement to raise the quality of

services and reduce unacceptable variations. The

Diabetes National Service Framework identified

foot-care service arrangements that should be

available for people with diabetes. These fell into

two parts: 1) foot protection programs for people at

increased risk for lower-limb complications provid-

ed by a foot protection team with the aim of

reducing the risk of lower-limb complications

(typically, members of this team include podiatrists,

orthotists, and other foot-care specialists) and 2)

foot-care services for people with lower-limb

complications provided by a multidisciplinary foot-

care team with the aim of providing rapid and

effective treatment for people who develop lower-

limb complications. This team should consist of

highly trained specialist podiatrists and orthotists,

nurses with training in dressing diabetic foot

wounds, and diabetologists with expertise in low-

er-limb complications.

Conclusions

Patients with diabetic foot are among the most

complex and vulnerable of all diabetic patients with

high morbidity and mortality. Specialized diabetic

foot clinics of the 21st century should be equipped

to coordinate revascularization procedures, to

aggressively treat infections, and to manage medical

comorbidities within a multidisciplinary forum.

History has taught us that optimal management of

diabetic foot complications is best provided in a

hospital-based diabetic foot clinic. The clinic must

be available to manage emergencies and must be

equipped to perform urgent investigations and

wound debridement and to initiate immediate

parenteral antibiotic drug therapy. It must also be

able to obtain rapid vascular and orthopedic

opinions and to arrange for emergency admissions

to the hospital.

Because of the broad scope of this review, we

express our regrets in advance for any omission or

abbreviation of an event or individual’s role in the

history of the team approach to amputation

prevention in people with diabetes. Many health-

care professionals have contributed to the evolution

Journal of the American Podiatric Medical Association � Vol 100 � No 5 � September/October 2010 331

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of our understanding, care, and management of the

diabetic foot. We have attempted to highlight some

of the pioneers, milestones, teams, and system

changes that have had a major impact on risk

assessment, management, and preservation of the

diabetic foot during the past 100 years. The

inadvertent exclusion or abbreviation of an individ-

ual or team’s role in this history should in no way be

interpreted as minimizing the importance of that

person or group’s contribution.

Acknowledgment: The assistance of Kristine

Scannell, medical librarian, Veterans Affairs Medi-

cal Center, Lebanon, Pennsylvania.

Financial Disclosure: None reported.

Conflict of Interest: None reported.

References

1. DAVIDSON JK, ALOGNA M, GOLDSMITH M, ET AL: ‘‘Assessment

of Program Effectiveness at Grady Memorial Hospital-

Atlanta,’’ in Educating Diabetic Patients, ed by G

Steiner, PA Lawrence, p 329, Springer Publishing Co,

New York, 1981.

2. EDMONDS ME, BLUNDELL MP, MORRIS ME, ET AL: Improved

survival of the diabetic foot: the role of a specialized

foot clinic. Q J Med 60: 763, 1986.

3. HOLSTEIN P, ELLITSGAARD N, OLSEN BB, ET AL: Decreasing

incidence of major amputations in people with diabetes.

Diabetologia 43: 844, 2000.

4. KRISHNAN S, NASH F, BAKER N, ET AL: Reduction in diabetic

amputations over 11 years in a defined U.K. population:

benefits of multidisciplinary team work and continuous

prospective audit. Diabetes Care 31: 99, 2008.

5. LARSSON J, APELQVIST J, AGARDH CD, ET AL: Decreasing

incidence of major amputation in diabetic patients: a

consequence of a multidisciplinary foot care team

approach? Diabet Med 12: 770, 1995.

6. LITZELMAN DK, SLEMENDA CW, LANGEFELD CD, ET AL:

Reduction of lower extremity clinical abnormalities in

patients with non-insulin-dependent diabetes mellitus: a

randomized, controlled trial. Ann Intern Med 119: 36,

1993.

7. RAYMAN G, KRISHNAN ST, BAKER NR, ET AL: Are we

underestimating diabetes-related lower-extremity am-

putation rates? results and benefits of the first prospec-

tive study. Diabetes Care 27: 1892, 2004.

8. SCHOFIELD CJ, YU N, JAIN AS, ET AL: Decreasing amputation

rates in patients with diabetes: a population-based

study. Diabet Med 26: 773, 2009.

9. TRAUTNER C, HAASTERT B, MAUCKNER P, ET AL: Reduced

incidence of lower-limb amputations in the diabetic

population of a German city, 1990–2005: results of the

Leverkusen Amputation Reduction Study (LARS). Dia-

betes Care 30: 2633, 2007.

10. VAN HOUTUM WH, RAUWERDA JA, RUWAARD D, ET AL:

Reduction in diabetes-related lower-extremity amputa-

tions in The Netherlands: 1991–2000. Diabetes Care 27:

1042, 2004.

11. DRIVER VR, MADSEN J, GOODMAN RA: Reducing amputation

rates in patients with diabetes at a military medical

center: the limb preservation service model. Diabetes

Care 28: 248, 2005.

12. VAN GILS CC, WHEELER LA, MELLSTROM M, ET AL: Amputa-

tion prevention by vascular surgery and podiatry

collaboration in high-risk diabetic and nondiabetic

patients: the Operation Desert Foot experience. Diabe-

tes Care 22: 678, 1999.

13. HOLLOWAY LM: A Fast Pace Forward: Chronicles of

American Podiatry, Pennsylvania College of Podiatric

Medicine, Philadelphia, 1987.

14. LEWI MJ, ed: The Textbook of Chiropody, The School of

Chiropody NY, New York, 1914.

15. BLISS M: The Discovery of Insulin, University of Chicago

Press, Chicago, 1982.

16. SANDERS L J, AMERICAN DIABETES ASSOCIATION: The Philatel-

ic History of Diabetes: In Search of a Cure, American

Diabetes Association, Alexandria, VA, 2001.

17. JOSLIN EP: The menace of diabetic gangrene. N Engl J

Med 211: 16, 1934.

18. MCKITTRICK LS, MCKITTRICK JB, RISLEY TS: Transmetatar-

sal amputation for infection or gangrene in patients with

diabetes mellitus. Ann Surg 130: 826, 1949.

19. MCKITTRICK JB, ROOT HF, WHEELOCK FC JR: Evaluation of

the transmetatarsal amputation in patients with diabe-

tes mellitus. Surgery 41: 184, 1957.

20. GIBBONS GW, WHEELOCK FC JR, HOAR CS JR, ET AL:

Predicting success of forefoot amputations in diabetics

by noninvasive testing. Arch Surg 114: 1034, 1979.

21. GIBBONS GW, WHEELOCK FC JR, SIEMBIEDA C, ET AL:

Noninvasive prediction of amputation level in diabetic

patients. Arch Surg 114: 1253, 1979.

22. WHEELOCK FC JR: Problems of the diabetic foot: arterial

reconstruction: femoral, popliteal tibial, peroneal. Dia-

betes Educ 8: 19, 1982.

23. LOGERFO FW, COFFMAN JD: Current concepts: vascular

and microvascular disease of the foot in diabetes:

implications for foot care. N Engl J Med 311: 1615, 1984.

24. GIBBONS GW, MARCACCIO EJ JR, BURGESS AM, ET AL:

Improved quality of diabetic foot care, 1984 vs 1990:

reduced length of stay and costs, insufficient reimburse-

ment. Arch Surg 128: 576, 1993.

25. LOGERFO FW, GIBBONS GW, POMPOSELLI FB JR, ET AL:

Trends in the care of the diabetic foot: expanded role of

arterial reconstruction. Arch Surg 127: 617, 1992.

26. FRYKBERG RG, ARORA S, POMPOSELLI FB JR, ET AL:

Functional outcome in the elderly following lower

extremity amputation. J Foot Ankle Surg 37: 181, 1998.

27. ROSENBLUM BI, POMPOSELLI FB JR, GIURINI JM, ET AL:

Maximizing foot salvage by a combined approach to

foot ischemia and neuropathic ulceration in patients

with diabetes: a 5-year experience. Diabetes Care 17:

983, 1994.

28. POMPOSELLI FB, KANSAL N, HAMDAN AD, ET AL: A decade of

experience with dorsalis pedis artery bypass: analysis of

332 September/October 2010 � Vol 100 � No 5 � Journal of the American Podiatric Medical Association

Page 17: History of the Team Approach to Amputation Prevention · care, diet, exercise, prompt treatment of foot infections, and specialized surgical care. The history of the team approach

outcome in more than 1000 cases. J Vasc Surg 37: 307,

2003.

29. BRAND PW: Third Annual Roger Pecoraro, MD Lecture:

the biomechanics of ulceration. Paper presented at:

American Diabetes Association 55th Annual Meeting

and Scientific Sessions, Atlanta, Georgia, June 11, 1995.

30. BRAND PWP: ‘‘Repetitive Stress in the Development of

Diabetic Foot Ulcers,’’ in The Diabetic Foot, 4th Ed, ed

by ME Levin, LW O’Neal, p xi, Mosby, St Louis, 1988.

31. BIRKE JA, HORSWELL R, PATOUT CA JR, ET AL: The impact of

a staged management approach to diabetes foot care in

the Louisiana public hospital system. J La State Med Soc

155: 37, 2003.

32. BIRKE JA, NOVICK A, PATOUT CA, ET AL: Healing rates of

plantar ulcers in leprosy and diabetes. Lepr Rev 63: 365,

1992.

33. DORGAN MB, BIRKE JA, MORETTO JA, ET AL: Performing foot

screening for diabetic patients. Am J Nurs 95: 32, 1995.

34. DUFFY JC, PATOUT CA JR: Management of the insensitive

foot in diabetes: lessons learned from Hansen’s disease.

Mil Med 155: 575, 1990.

35. PATOUT CA JR, BIRKE JA, HORSWELL R, ET AL: Effectiveness

of a comprehensive diabetes lower-extremity amputa-

tion prevention program in a predominantly low-income

African-American population. Diabetes Care 23: 1339,

2000.

36. PATOUT CA JR, BIRKE JA, WILBRIGHT WA, ET AL: A decision

pathway for the staged management of foot problems in

diabetes mellitus. Arch Phys Med Rehabil 82: 1724,

2001.

37. BIRKE JA, SIMS DS: Plantar sensory threshold in the

ulcerative foot. Lepr Rev 57: 261, 1986.

38. WAGNER FW JR: The dysvascular foot: a system for

diagnosis and treatment. Foot Ankle 2: 64, 1981.

39. AMERICAN DIABETES ASSOCIATION: Consensus Development

Conference on Diabetic Foot Wound Care: 7–8 April

1999, Boston, Massachusetts. Diabetes Care 22: 1354,

1999.

40. American Diabetes Association: Peripheral arterial

disease in people with diabetes. Diabetes Care 26:

3333, 2003.

41. MAYFIELD JA, REIBER GE, SANDERS L J, ET AL: Preventive

foot care in people with diabetes. Diabetes Care 21:

2161, 1998.

42. LEVIN ME, O’NEAL LW, eds: The Diabetic Foot, 1st Ed, CV

Mosby Co, St Louis, 1973.

43. BOWKER JH, PFEIFER MA, eds: Levin and O’Neal’s The

Diabetic Foot, 7th Ed, Mosby Elsevier, Philadelphia,

2008.

44. ARMSTRONG DG, ABU-RUMMAN PL, NIXON BP, ET AL:

Continuous activity monitoring in persons at high risk

for diabetes-related lower-extremity amputation. JAPMA

91: 451, 2001.

45. ARMSTRONG DG, LAVERY LA, HARKLESS LB: Validation of a

diabetic wound classification system: the contribution

of depth, infection, and ischemia to risk of amputation.

Diabetes Care 21: 855, 1998.

46. ARMSTRONG DG, LAVERY LA, WUNDERLICH RP: Risk factors

for diabetic foot ulceration: a logical approach to

treatment. J Wound Ostomy Continence Nurs 25: 123,

1998.

47. ARMSTRONG DG, PETERS EJ: Classification of wounds of

the diabetic foot. Curr Diab Rep 1: 233, 2001.

48. LAVERY LA, ARMSTRONG DG, HARKLESS LB: Classification of

diabetic foot wounds. J Foot Ankle Surg 35: 528, 1996.

49. LAVERY LA, ARMSTRONG DG, MURDOCH DP, ET AL: Validation

of the Infectious Diseases Society of America’s diabetic

foot infection classification system. Clin Infect Dis 44:

562, 2007.

50. LAVERY LA, HIGGINS KR, LANCTOT DR, ET AL: Home

monitoring of foot skin temperatures to prevent

ulceration. Diabetes Care 27: 2642, 2004.

51. LAVERY LA, HIGGINS KR, LANCTOT DR, ET AL: Preventing

diabetic foot ulcer recurrence in high-risk patients: use

of temperature monitoring as a self-assessment tool.

Diabetes Care 30: 14, 2007.

52. SMITH DG, STUCK RM, KETNER L, ET AL: Partial calcanec-

tomy for the treatment of large ulcerations of the heel

and calcaneal osteomyelitis: an amputation of the back

of the foot. J Bone Joint Surg Am 74: 571, 1992.

53. PINZUR MS, MORRISON C, SAGE R, ET AL: Syme’s two-stage

amputation in insulin-requiring diabetics with gangrene

of the forefoot. Foot Ankle 11: 394, 1991.

54. EDELMAN D, SANDERS L J, POGACH L: Reproducibility and

accuracy among primary care providers of a screening

examination for foot ulcer risk among diabetic patients.

Prev Med 27: 274, 1998.

55. SANDERS L J: Diabetes mellitus: prevention of amputa-

tion. JAPMA 84: 322, 1994.

56. SANDERS L J: Transmetatarsal and midfoot amputations.

Clin Podiatr Med Surg 14: 741, 1997.

57. SANDERS L J: ‘‘Ray and Transmetatarsal Amputations,’’ in

Mastery of Surgery, 5th Ed, ed by JE Fischer, KI Bland,

p 2, Wolters Kluwer Health/Lippincott Williams &

Wilkins, Philadelphia, 2007.

58. SANDERS L J, DUNLAP G: Transmetatarsal amputation: a

successful approach to limb salvage. JAPMA 82: 129,

1992.

59. PINZUR MS, SAGE R, SCHWAEGLER P: Ray resection in the

dysvascular foot: a retrospective review. Clin Orthop

Relat Res 191: 232, 1984.

60. PECORARO RE, REIBER GE, BURGESS EM: Pathways to

diabetic limb amputation: basis for prevention. Diabetes

Care 13: 513, 1990.

61. REIBER GE, VILEIKYTE L, BOYKO EJ, ET AL: Causal pathways

for incident lower-extremity ulcers in patients with

diabetes from two settings. Diabetes Care 22: 157, 1999.

62. Preservation-Amputation Care and Treatment (PACT)

Program, Department of Veterans Affairs, Veterans

Health Administration, Washington, DC, 2006. VHA

Directive 2006–050.

63. IVERSEN MM, TELL GS, RIISE T, ET AL: History of foot ulcer

increases mortality among individuals with diabetes:

ten-year follow-up of the Nord-Trondelag Health Study,

Norway. Diabetes Care 32: 2193, 2009.

64. ROBBINS JM, STRAUSS G, ARON D, ET AL: Mortality rates and

diabetic foot ulcers: is it time to communicate mortality

Journal of the American Podiatric Medical Association � Vol 100 � No 5 � September/October 2010 333

Page 18: History of the Team Approach to Amputation Prevention · care, diet, exercise, prompt treatment of foot infections, and specialized surgical care. The history of the team approach

risk to patients with diabetic foot ulceration? JAPMA

98: 489, 2008.

65. Obituary notices: Robert Daniel Lawrence, M.A., LL.D.,

M.D., F.R.C.P. Br Med J 3: 621, 1968.

66. JACKSON JG: R.D. Lawrence and the formation of the

Diabetic Association. Diabet Med 13: 9, 1996.

67. OAKLEY WG: R.D. Lawrence, M.D., F.R.C.P., 1892–1968.

Diabetes 18: 54, 1969.

68. MCKEOWN KC: The history of the diabetic foot. Diabet

Med 12: 19, 1985.

69. CATTERALL RC, MARTIN MM, OAKLEY W: Aetiology and

management of lesions of the feet in diabetics. Br Med J

27: 953, 1956.

70. ASSAL J-P, GFELLER R, EKOE J-M: ‘‘Patient Education in

Diabetes,’’ in Recent Trends in Diabetes Research:

Symposium, September 22–24, 1981, ed by H Bostrom,

N Ljungstedt Skandiakoncernen, p 276, Almqvist &

Wiksell International, Stockholm, 1982.

71. PETER-RIESCH B, ASSAL JP: Teaching diabetic foot care

effectively. JAPMA 87: 318, 1997.

72. THOMPSON FJ, VEVES A, ASHE H, ET AL: A team approach to

diabetic foot care: the Manchester experience. Foot 1:

75, 1991.

73. BARBANO PR, ALDEGHI A, FAGLIA E, ET AL: Results of

revascularization and amputation of the gangrenous

diabetic foot: importance of a multidisciplinary ap-

proach [in Italian]. Minerva Cardioangiol 43: 97, 1995.

74. FAGLIA E, FAVALES F, ALDEGHI A, ET AL: Change in major

amputation rate in a center dedicated to diabetic foot

care during the 1980s: prognostic determinants for

major amputation. J Diabetes Complications 12: 96,

1998.

75. EDMONDS M, FOSTER A: Reduction of major amputations

in the diabetic ischaemic foot: a strategy to ‘‘take

control’’ with conservative care as well as revascular-

ization. VASA 58 (suppl): 6, 2001.

76. FOSTER AV, SNOWDEN S, GRENFELL A, ET AL: Reduction of

gangrene and amputations in diabetic renal transplant

patients: the role of a special foot clinic. Diabet Med 12:

632, 1995.

77. MCARTHUR CS, SHEAHAN MG, POMPOSELLI FB JR, ET AL:

Infrainguinal revascularization after renal transplanta-

tion. J Vasc Surg 37: 1181, 2003.

78. RAMDEV P, RAYAN SS, SHEAHAN M, ET AL: A decade

experience with infrainguinal revascularization in a

dialysis-dependent patient population. J Vasc Surg 36:

969, 2002.

79. UCCIOLI L, FAGLIA E, MONTICONE G, ET AL: Manufactured

shoes in the prevention of diabetic foot ulcers. Diabetes

Care 18: 1376, 1995.

80. CALLE-PASCUAL AL, DURAN A, BENEDI A, ET AL: Reduction in

foot ulcer incidence: relation to compliance with a

prophylactic foot care program. Diabetes Care 24: 405,

2001.

81. MCCABE CJ, STEVENSON RC, DOLAN AM: Evaluation of a

diabetic foot screening and protection programme.

Diabet Med 15: 80, 1998.

82. DONOHUE M, FLETTON J, TOOKE JE: ‘‘The Exeter Integrated

Diabetic Foot Project,’’ in The Foot in Diabetes, 3rd Ed,

ed by AJM Boulton, H Connor, PR Cavanagh, p 87, John

Wiley & Sons Ltd, Chichester, 2000.

83. DONOHOE ME, FLETTON JA, HOOK A, ET AL: Improving foot

care for people with diabetes mellitus: a randomized

controlled trial of an integrated care approach. Diabet

Med 17: 581, 2000.

84. GERSHATER MA, LONDAHL M, NYBERG P, ET AL: Complexity of

factors related to outcome of neuropathic and neuro-

ischaemic/ischaemic diabetic foot ulcers: a cohort

study. Diabetologia 52: 398, 2009.

85. FAGLIA E, DALLA PAOLA L, CLERICI G, ET AL: Peripheral

angioplasty as the first-choice revascularization proce-

dure in diabetic patients with critical limb ischemia:

prospective study of 993 consecutive patients hospital-

ized and followed between 1999 and 2003. Eur J Vasc

Endovasc Surg 29: 620, 2005.

86. EL SAKKA K, FASSIADIS N, GAMBHIR RP, ET AL: An integrated

care pathway to save the critically ischaemic diabetic

foot. Int J Clin Pract 60: 667, 2006.

87. ZAYED H, HALAWA M, MAILLARDET L, ET AL: Improving limb

salvage rate in diabetic patients with critical leg

ischaemia using a multidisciplinary approach. Int J Clin

Pract 63: 855, 2009.

88. TRAUTNER C, HAASTERT B, SPRAUL M, ET AL: Unchanged

incidence of lower-limb amputations in a German City,

1990–1998. Diabetes Care 24: 855, 2001.

89. CANAVAN RJ, UNWIN NC, KELLY WF, ET AL: Diabetes- and

nondiabetes-related lower extremity amputation inci-

dence before and after the introduction of better

organized diabetes foot care: continuous longitudinal

monitoring using a standard method. Diabetes Care 31:

459, 2008.

90. CHEER K, SHEARMAN C, JUDE EB: Managing complications

of the diabetic foot. BMJ 339: b4905, 2009.

91. ANICHINI R, ZECCHINI F, CERRETINI I, ET AL: Improvement of

diabetic foot care after the implementation of the

International Consensus on the Diabetic Foot (ICDF):

results of a 5-year prospective study. Diabetes Res Clin

Pract 75: 153, 2007.

92. ESKELINEN E, ESKELINEN A, ALBACK A, ET AL: Major

amputation incidence decreases both in non-diabetic

and in diabetic patients in Helsinki. Scand J Surg 95:

185, 2006.

93. YOUNG MJ, MCCARDLE JE, RANDALL LE, ET AL: Improved

survival of diabetic foot ulcer patients 1995–2008:

possible impact of aggressive cardiovascular risk

management. Diabetes Care 31: 2143, 2008.

94. LINCOLN NB, RADFORD KA, GAME FL, ET AL: Education for

secondary prevention of foot ulcers in people with

diabetes: a randomised controlled trial. Diabetologia 51:

1954, 2008.

95. JEFFCOATE WJ, PRICE PE, PHILLIPS CJ, ET AL: Randomised

controlled trial of the use of three dressing preparations

in the management of chronic ulceration of the foot in

diabetes. Health Technol Assess 13: 1, 2009.

96. LOBMANN R, MULLER E, KERSKEN J, ET AL: The diabetic foot

in Germany: analysis of quality in specialised diabetic

footcare centres. Diabetic Foot J 10: 68, 2007.

334 September/October 2010 � Vol 100 � No 5 � Journal of the American Podiatric Medical Association