Diabetes Research and Clmicaf Practice, 17 (1992) 1-8 8 1992 Elsevier Science Publishers B.V. All rights reserved 0168-8227/92/$05.00 DIABET
1
00627
Mini-review
The diabetic foot problem - a failed system of health care? Karl E. Sussman a, Gayle Reiberb and Stephen
F. Albert a
“Denver VA Medical Center, University of Colorado Health Sciences Center, Denver CO 80220, USA and bDepartment of Health Services. School of Public Health and Community Medicine, University of Washington, Seattle, WA 98195. USA and Health Services Research and Development, Seattle VA Medical Center, Seattle, WA 98195, USA (Received 18 November 199 1) (Accepted 9 January 1992)
Summary It is evident that there is excess morbidity and mortality as a consequence of foot problems in patients with diabetes mellitus. Most of the data relative to foot lesions is taken from the study of subsets of diabetic patients undergoing lower extremity amputation. Such data probably do not provide accurate information relative to the incidence and/or prevalence of diabetic foot problems. Available evidence does suggest that diabetic foot care may be inadequate and the efficacy of various diagnostic and therapeutic modalities has not been proven. Advances have been made in obtaining a better understanding of the microbiology of lower extremity infected lesions both in hospitalized patients and in those subjects being followed in the outpatient setting. Attention should be directed at developing a systematic classification of foot lesions which can be universally applied. We need to understand and relate to those risk factors contributing to the development and progression of lower extremity lesions in the diabetic patient. In evaluating the efficacy of diverse diagnostic and therapeutic approaches, well-controlled clinical investigations need to be undertaken. Attention should be focussed upon both measures of process and outcome where appropriate. Finally, there needs to be recognition that the problem of the diabetic foot lesion represents a major public health challenge. Key words: Diabetes;
Foot care; Prevention;
Health care delivery;
Notwithstanding the tremendous advances which have been made in the delivery of health care to patients with diabetes, one has the uneasy feeling that there is excess morbidity and perhaps mortality as a consequence of foot problems [ l-51. In Correspondence to: K.E. Sussman, M.D., VA Medical Center, 1055 Clermont Street, Denver, CO 80220, USA. This article is dedicated to our esteemed colleague Roger E. Pecoraro, M.D., for his major scientific contributions to research concerning diabetic foot problems.
Epidemiology
fact, precise data relative to the incidence and/or prevalence of foot problems in the diabetic are remarkably scarce, this standing in contrast to our knowledge of retinopathy or nephropathy in this patient population. In addition, there are relatively few analytic studies which attempt to quantify risk factors which play a role in the development and progression of diabetic lower extremity lesions. We do have some information relative to the
2
frequency of amputations in patients with diabetes. Most and Sinnock have reported that 459/, of all lower extremity amputations are performed on patients with diabetes [6]. This figure may be an underestimate of the number of lower extremity amputations which can be attributed to diabetes. Others have stated that perhaps 70”#; of lower extremity amputations were performed in patients with diabetes [2]. Overall, diabetic patients have a 15 times higher age-adjusted risk of lower extremity amputations than nondiabetics [ 61. While clearly, the event of amputation is of major importance to the diabetic patient, such information does not in and of itself provide data relative to the incidence and prevalence of diabetic foot problems. Most published case series represent unique practice catchment areas, lack appropriate control groups and thus limit the inferences which can be drawn. Available amputation data are largely surgical case series that reflect a select referral population. Diabetic amputations are unequivocable and measurable, but the data acquired should be subject to more critical analysis and review. Reported data should reflect only diabetic, non-traumatic, non-cancer amputations. It would be helpful, if in the reports, information was provided as to the site of amputation, even though at times this is determined by the preference and clinical judgement of the clinician. Finally, in risk assessment, one needs information as to whether the procedure was the first ever amputation to an extremity, a revision, subsequent amputation or a contralateral amputation. The indications for amputation may vary amongst health professionals, so that even as a rough guide, the information relative to amputation rates may not be helpful in estimating the prevalence and incidence of diabetic foot problems. Indeed, the evidence suggests that it is only a small fraction of patients with foot lesions who progress to the point where amputation is required [ 71. The number of patients with foot or lower extremity lesions greatly exceeds those undergoing amputations. It has been estimated that 25 9’, of patients with
diabetes will consult physicians, surgeons, podiatrists or other health professionals for a diabetesrelated foot or leg problem [ 81. In fact, solid data relative to the prevalence of foot problems are difficult to find in the current literature. Even data relative to hospital discharge rates for diabetic foot problems are scarce. Such information again might underestimate the prevalence of diabetic foot problems, but at least would be closer to actual morbidity as a consequence of serious problems involving the foot or the lower extremity in the patient with diabetes. The most frequent cause of hospitalization of diabetic patients is due to the existence of serious foot or lower extremity problems [ 11. One out of five admissions to hospitals in the United Kingdom is for the treatment of foot problems in the patient with diabetes [9]. Boulton estimates that the mean duration of hospital admissions for foot problems in the diabetic patient is 4 weeks [I]. Whatever data exists suggests that as a complication of diabetes, foot problems exact a toll not only in terms of morbidity and mortality but also relative to costs as well. In the United States, the actual cost of diabetic foot problems is unknown [lo]. A cost of illness study assessing U.S. economic costs for non-insulin-dependent diabetes (NIDDM) in 1986 estimated ‘chronic skin ulcers’ totaled $250 million in health care expenditures [ 111. Of 103 admissions for diabetic foot infections, an average length of stay of 22 days was recorded at an estimated cost of $6600 per hospitalization [ 121. In the United Kingdom, more hospital beds are filled with people with diabetic foot complications than are filled from all other diabetic complications combined [ 131. The direct cost of an amputation, including hospitalization, surgery, and anaesthesia, is approximately $20000 to $25000 per case [lo]. To further compound the problem concerning the delivery of optimal diabetic foot care, various therapeutic approaches are recommended in the absence of well controlled clinical trials. We recognize that, on the face of it, some recommendations seem fundamentally sound and that no controlled clinical trials are necessary (e.g.,
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patients with diabetes should always wear shoes when walking about the house). Nevertheless, recommendations for certain, more sophisticated therapies (e.g., therapeutic shoes) may need substantiation. Within this context, it is evident that health professionals may not focus enough attention on preventive strategies concerning foot care in the patient population with diabetes. Especially disturbing are data which demonstrated that the rate of foot examination over the period of a year ranges from 30 to 50 ?, in caring for patients with diabetes [ 14-161. On the day in which diabetic patients were being seen, the frequency of foot examination was as low as 12-19% [ 14,151. The situation may be worse insofar as the quality of the foot examination may vary and may be insufficient to detect serious or potential foot pathology. A recent report suggests that there may be delays in referring patients with serious foot problems which may make therapy more difficult and contribute to greater morbidity, more extensive amputations and excess limb loss. Mills and associates reported on a review of records of 55 patients with localized gangrene or infection 1171. In 16 of the patients (29%), there was a prolonged delay between initial treatment and referral for definitive care. The causes of the delay were underestimation of the severity of the foot infection in ten patients, and lack of recognition of ischemia due to large vessel occlusive disease in six. These delays led to more proximal levels of amputation in six patients, including three belowknee amputations in patients with limbs that were initially thought to be salvageable [ 171. Evidence does suggest that if more attention is directed to foot care as part of an effort in intensive care in the diabetic patient that serious morbidity can be avoided [ 7,18,19]. Especially striking are the data of Edmonds and associates who demonstrated clearly the value of a program of intensive attention to foot care [ 71. In their clinic, a major emphasis was on the use of specially constructed shoes, intensive chiropody and better directed antibiotic treatment. In their series of patients, healing was achieved in 86’~ (*O~/ZX)of
neuropathic ulcers and in 72:)” (lo7/143) of ischemic ulcers. Relapse frequency was 26Y/, in patients wearing special shoes, and 83:; in patients preferring to wear their own shoes. In the 2-year period before the establishment of this special clinic devoted to foot care, the annual frequency of amputations was 1 l-12 per year, with the clinic in operation there were 5-7 amputations yearly. These data, while not representing a definitive controlled study, do indeed suggest that intensive attention to foot care may dramatically alter morbidity statistics and result in positive outcomes in the evolution and progression of foot lesions. Patient knowledge concerning appropriate foot care may be woefully lacking [9]. In a United Kingdom survey, the vast majority of diabetic patients with foot ulcers were purchasing shoes over the counter or by mail order [93. Their feet were not being measured and the shoes were not being checked to see whether there was a satisfactory fit. Given this somewhat negative assessment, it is appropriate to consider what is being done at the present time to improve clinical care of patients with foot problems and what additional measures might be required. It is important to recognize that our approach to foot lesions has improved over the years. For example, more refined microbiological techniques have demonstrated the importance of anaerobic organisms in infected ulcers [ 8,20-251. Special attention has been directed to the presence of Bacteroides as well as Peptostreptococcus and Peptococcus existing in combination with other organisms in infected lesions in diabetic patients [36,27]. Also, the literature has pointed to the need to culture deep tissues (for example, during debridement) to be able to assess the offending organisms and devise appropriate antibiotic regimens [ 828.291. Appropriate surgical debridement may be as important as the selection of a specific antimicrobial agent for the successful management of patients with infections caused by anaerobic microorganisms [ 271. It should be noted that microbiological assess-
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ment may yield different results, depending upon whether the investigation is directed at hospitalized patients undergoing amputation or the more prevalent group of diabetic subjects with less severe infections [30]. Most foot infections are not complicated by deep tissue involvement, osteomyelitis or gangrene [ 301. Lipsky and associates demonstrated in an outpatient diabetic population with foot infections, the most common offending organisms are gram-positive cocci. These organisms were isolated in 89% of cases and were the sole pathogen in 42% of the infections observed [ 301. In contrast, amputation patients have an overwhelming incidence of polymicrobial infections with 5.8 organisms being isolated on curettage culture. In the outpatients with foot infections, aerobic gram-negative organisms may be isolated (36%) and the incidence of anaerobes is really quite low (7%). These latter organisms are most commonly seen in polymicrobial infections [ 301. Another advance in foot care has been the use of arterial reconstructive procedures. Although microcirculation abnormalities exist in patients with diabetes, their role in the pathogenesis of foot lesions has been questioned [31-341. Macrovascular disease has been estimated to be present in approximately 16% of individuals with diabetes and is thought to represent the critical vascular abnormality in the development and progression of lower extremity lesions [8,35-371. Arterial reconstructive procedures are being used to enhance wound healing and may obviate the need for amputation [ 8,17,36,37]. However, the widespread use of arterial reconstructive procedures to augment wound healing is not warranted at this point in time. Clearly, this is an area in which controlled studies need to be undertaken not only to establish the effectiveness of this approach but also to define the indications and the patients most suitable for this procedure in the setting of faulty wound healing. There has been a recent flurry of interest in the use of white blood cell scintigraphy in the diagnosis of osteomyelitis in patients with diabetes [38]. The radioactive label employed is
indium-1 11. The technique appears to be better for the diagnosis of osteomyelitis when present in the tarsometatarsal region as opposed to the toes. In 19 patients who had clinically evident osteomyelitis, white blood cell scintigraphic studies were positive in 100% of cases. In the report by Keenan and associates, white blood cell scintigraphy appeared to be more accurate than conventional X-ray studies or investigations using three-phase bone scintigraphy [ 381. However, false positive results are obtained due to a number of factors, including the presence of aseptic soft tissue and bone inflammation, hyperemia/hypervascularity which may or may not be associated with inflammation, inflammatory arthritis, adjacent cellulitis or when an ulcer is located particularly close to bone [ 381. Other constraints include the presence of neuropathic disease, the presence of trauma, and degenerative arthritis. Even in the study by Keenan, it is not clear whether the technique will detect osteomyelitis when not suspected, or whether the technique can differentiate osteomyelitis from diabetic neuroarthropathy. Finally, the literature is not clear whether white blood cell scintigraphy has made any difference in clinical treatment or therapeutic outcome. Indeed, the feeling is extant that this is an expensive technique which really does not have much of a role in the management of foot problems [39]. Concerning recommendations as to future courses of action, the first step should be to acquire more precise data concerning lower extremity lesions in the patient population with diabetes. It is necessary to compile accurate data concerning the incidence and prevalence of diabetic foot problems. This information needs to be collected from all health care units caring for patients with diabetes. We need to know the total number of diabetic patients being treated as well as the number of patients presenting with foot problems. Since patients may have repeated foot problems, data must be acquired concerning the number of patients with foot problems as well as the number of episodes per patient. Foot problems must be classified according to severity to maximize the usefulness of the data. There are
several wound classification systems described in the literature which have been developed for specific purposes, e.g. assessment of amputation risk, healing potential/amputation level, clinical care or clinical/epidemiology research [ 1,10,40,41]. It is evident that the purpose for which the classification is to be used influences the type of system developed [42]. Hopefully, a standardized classification system can be promulgated which will yield meaningful data relative to specific therapeutic modalities as well as shed light on the epidemiology of chronic wounds in the patient population with diabetes. Such a system should be based upon well-defined objective criteria and should avoid subjective or vague wound descriptions [42]. Pecoraro has discussed the advantages and the potential utility of the various classification systems [ 421. We need to know more about the factors that play a role in the development of foot lesions. The second recommendation would be to develop a more systematic approach to the study, classification and evaluation of the risk factors contributing to the development and progression of lower extremity lesions in the diabetic patient. It would seem that the sophisticated approach employed by Pecoraro and colleagues could be applied logically to discerning and quantitating the role of various factors in the development of and progression of foot lesions in the patient with diabetes [43]. These authors employed a model to study causation based on the concept that there exist two general types of causes, ‘sufficient’ and ‘component’ causes [44,45]. Sufficient causes inevitably produce the effect and in the case of lower extremity amputation referred to, the set of minimal conditions or events that inevitably result in amputations [43]. Minimal meant that none of the conditions or events were superfluous. Component causes were defined& causes of interest that are not sufficient in themselves but are components of one or more distinctive sufficient causes. Removing or blocking of a component cause renders the action of other components as insufficient to produce the effect being studied. Thus, in a defined causal pathway leading to lower
extremity amputation, the existence of neuropathy and trauma might be considered as just two component causes amongst others which form the completed causal chain leading to amputation. The absence of neuropathy or trauma in a designated causal chain would prevent the expression of the other components and therefore the amputation would not ensue. Based on previous literature, the authors studied seven potential causes and four major pathophysiologic mechanisms including neuropathy, ischemia, infection and wound healing failure, two common soft tissue complications, cutaneous ulceration and gangrene, and minor trauma to the extremity [43]. In their study, they found that the sequence of minor trauma, cutaneous ulceration and wound healing failure accounted for 727, of amputations, this causal chain being commonly associated with infection and gangrene [43]. In 46% of amputations, ischemia was a causal factor, infection in 599; of amputations, neuropathy - 6 1%) faulty wound healing - 8 1%) gangrene - 55 %, and initial minor trauma -81:;. The limitation of this particular study may be that only males were studied, although it does seem that males are at greater risk for lower extremity amputation [ 61. Notwithstanding, it would seem that this method of analysis could well be applied and refined in the study and characterization of those factors playing a role in foot problems in the patient with diabetes. Perhaps, one could include in this analysis the newer methods of evaluating factors which might play a role in the development and progression of foot lesions, for example the combined use of ankle and toe pressure measurements to predict wound healing or pedobarographic studies to study weight bearing and special areas of the foot being subjected to abnormal pressures and loads [ 1,39,46-493. The third recommendation would be to initiate well controlled studies of various diagnostic and treatment modalities, using both process and outcome measures to assess therapeutic efficacy. The first two recommendations related to the need to define foot lesions and the factors that
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play a role in pathogenesis. Using these latter constructs to define the nature of foot problems in patients, it should be possible to assess our success in our attempts in diagnosis and treatment. It is critical to differentiate between process and outcome measurements in gauging our therapeutic success. For example, it may be quite useful as a diagnostic process to use scintigraphy to diagnose osteomyelitis as opposed to diabetic neuroarthropathy, but this may not make any difference in terms of outcomes [ 38,391. By the same token, assessing therapeutic efficacy by simply measuring outcomes may yield misleading information. One must be able to establish that a given intervention has resulted in a change in some process which thereby was correlated with a given alteration in outcomes. Thus special shoes should be shown to have altered patterns of weight bearing which in turn is reflected in decreased incidence and/or prevalence of foot lesions. An example of a process measure is the study by Veves and colleagues in which they evaluated the effectiveness of experimental padded hosiery in reducing abnormal foot pressures [ 501. The well controlled study of the use of total contact casting in treatment of diabetic plantar ulcers is a good example of an investigation directed at outcome assessment [ 5 11. Finally, there needs to be recognition that the problem of the diabetic foot lesion represents a major public health challenge. The evidence suggests that this issue is not only one of morbidity and mortality, but also one of costs to society in terms of the expense of health care, and also lost days of productivity as well. Research needs to be undertaken to demonstrate whether diagnostic and treatment strategies are biologically plausible and therapeutically efficacious. Then, if such strategies prove to be cost effective, they should be implemented by health professionals. Strategies proven to be effective in the prevention of foot lesions need financial support. It is incumbent upon health professionals to demonstrate which measures are medically sound and should be universally implemented. Third party insurance carriers and other entities providing financial sup-
port to the health care system must be informed as to the severity of the problem of the diabetic foot and also advised as to what specific measures should be undertaken to help the patient with diabetes. As such, problems in preventing and treating foot lesions still remain a challenge. In considering this topic, we have not attempted to present a comprehensive review of foot lesions and their management. Rather we have focussed on certain problems relative to how the challenge of diabetic foot lesions is presently being pursued. It is evident that data acquisition is critical in order to understand and delineate existing problems relative to lower extremity lesions in diabetic patients. Furthermore, emphasis must be placed on conducting well controlled clinical studies to determine the efficacy of various diagnostic and therapeutic measures. Where appropriate, attention should be devoted to obtaining both process and outcome measures to establish the most effective approaches in the management of foot lesions. The evidence currently available suggests that great strides can be made in decreasing morbidity and mortality due to diabetic foot lesions, but the overall effort needs more rigorous studies, clinical classification, and a reorientation towards evaluating patient and clinical management strategies.
References I Boulton, A.J.M. (1988) The diabetic foot. Med. Clin. North Am. 72, 1513-1530. 2 Levin, M.E. and O’Neal, F.W. (1988). The Diabetic Foot. C.V. Mosby, St. Louis, Missouri. 3 Brenner, M.A. (1987) Management of the Diabetic Foot. Williams & Wilkins, Baltimore, Maryland. 4 Kozak, G.P. (1984) Diabetic foot disease: a major problem. In: G.P. Kozak, C.S. Hoar, J.L. Rowbotham, F.C. Wheelock, G.W. Gibbons and D. Campbell (Eds.), Management of Diabetic Foot Problems. W.B. Saunders, Philadelphia, Pennsylvania, pp. 1-8. 5 Levin, M.E. (1987) The diabetic foot. In: K.E. Sussman, B. Draznin and W.E. James (Eds.), Clinical Guide to Diabetes Mellitus. Alan R. Liss, Inc., New York, pp. 159-173. 6 Most, R.S. and Sinnock. P. (1983) The epidemiology of
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lower extremity amputations in diabetic individuals. Diabetes Care 6. 87-91. Edmonds, M.E., Blundell, M.P., Morris, M.E., Thomas, E.M., Cotton, L.T. and Watkins, P.J. (1986) Improved survival of the diabetic foot: the role of a specialized foot clinic. Q. J. Med. 60, 763-771. Gibbons, G.W. (1987) The diabetic foot: amputation and drainage of infection. J. Vast. Surg. 5, 791-793. Masson, E.A., Angle, S. and Roseman, P. (1988) Foot ulcers. Do diabetic patients know how to protect themselves?. Pratt. Diabetes 78, 371-378. Reiber, G.E. (1992) Diabetic foot care: guidelines and financial implications. Diabetes Care (Suppl. 1) 15, 29-31. Huse, D.M., Oster, G., Killen, A.R., Lacey, M.J. and Colditz, G.A. (1989) The economic cost of non-insulin dependent diabetes mellitus. JAMA 262, 2708-2713. Wheat, L.J., Allen, S.D. and Henry, M. (1986) Diabetic foot infections, bacteriologic analysis. Arch. Intern. Med. 146, 1935-1940. Dyck, P.J., Thomas, P.K. Lambert, E.H. et al. (Eds.), Diabetic Neuropathy. W.B. Saunders, Philadelphia. Cohen, S.J. (1983) Potential barriers to diabetes care. Diabetes Care 6, 499-500. Bailey, T.S.. Yu. H.M. and Rayfield, E. (1985) Patterns of foot examination in a diabetic clinic. Am. J. Med. 78, 311-314. Payne. T.H.. Gabella, B.A., Michael. S.L.. Young, W.F., Pickard. J.. Hofeldt. F.D., Fan, F.. Stromberg, J.S. and Hamman. R.F. (1989) Preventive care in diabetes mellitus: current practice in urban health care system. Diabetes Care 12, 745-747. Mills. J.L., Beckett, W.C. and Taylor, S.M. (1991) The diabetic foot: consequences of delayed treatment and referral. South. Med. J. 84, 970-974. Runyan, J.W. (1975) The Memphis chronic disease program. JAMA 231, 364-267. Davidson. J.K., Alogna. M., Goldsmith, M. and Borden, J. ( 198 1) Assessment of program effectiveness at Grady Memorial Hospital. In: G. Steiner and P.A. Lawrence (Eds.), Educating Diabetic Patients. Springer Publishing Co., New, York, pp. 329-348. Jones. E.W.. Edwards, R., Firch, R. and Jeffcoate, W.J. (1985) A microbiologic study of diabetic foot lesions. Diabetic Med. 2, 213-215. Louie, T.J., Bartlett. J.G., Tally, F.P. and Gorbach, S.L. (1976) Aerobic and anaerobic bacteria in diabetic foot ulcers. Ann. Intern. Med. 85, 461-463. Sapico. F.L., Witte. J.L. and Canawati, H.N. (1984) The infected foot of the diabetic patient: quantitative microbiology and analysis of clinical features. Rev. Infect. Dis. 6 (Suppl. 1). 171-176. Goldberg, D. and Neu. H.C. (1987) Infectious diseases of the diabetic foot. In: M.A. Brenner (Ed.), Management of the Diabetic Foot, Williams and Wilkins. Baltimore, hlnryland. pp. 9X-109.
24 Sapico, F.L., Bessman, A.N. and Canawati, H.N. (1982) Bacteremia in diabetic patients with infected lower extremities. Diabetes Care 5. 101-104. 25 Sapico, F.L., Canawati, H.N., Witte, J.L.. Montgomerie. J., Wagner, F.W. Jr. and Bessman. A.N. (1980) Quantitative aerobic and anaerobic bacteriology of infected diabetic feet. J. Clin. Microbial. 12. 413-420. 26 Krepel, C.J.. Gohr, C.M.. Edmiston, C.E. Jr. and Farmer, S.G. (1991) Anaerobic pathogenesis: collagenase production by Peptostreptococcus magnus and its relationship to site of infection. J. Infect. Dis. 163, 1148-l 150. 27 Wilson, W.R. (1991) Treatment of infections caused by anaerobes. J. Chemother. 3, 7-l 1. 28 Sharp, C.S., Bessman, A.L. and Wagner, F.W. (1979) Microbiology of superficial and deep tissues in infected diabetic gangrene. Surg., Gynecol. Obstet. 149,217-219. 29 Silva, J.R. Jr. and Sussman, K.E. (1987) Infection in diabetes. In: K.E. Sussman, B. Draznin and W.E. James (Eds.), Clinical Guide to Diabetes Mellitus. Alan R. Liss, Inc., New York, pp. 183-191. 30 Lipsky, B.A., Pecoraro, R.E., Larson, S.A., Hanley, M.E. and Ahroni, J.H. (1990) Outpatient management of uncomplicated lower extremity infections in diabetic patients. Arch. Intern. Med. 150, 790-797. 31 Walsh, C.H., Soler, M.G. and Fitzgerald, M.G. (1975) Association of foot lesions with retinopathy in patients with newly diagnosed diabetes. Lancet i, 878-880. 32 Young, R.J. (1987) Identification of the subject ‘at risk’ of foot ulceration. In: H. Connor, A.J.M. Boulton and J.D. Ward (Eds.). The Foot in Diabetes. John Wiley & Sons, Chichester, pp. l-10. 33 Tooke, J.E. (1987) Blood flow abnormalities in the diabetic foot: diagnostic aid or research tool?. In: H. Connor, A.J.M. Boulton and J.D. Ward (Eds.), The Foot in Diabetes. John Wiley & Sons, Chichester, pp. 23-3 1 34 Logerfo, F.W. and Coffman, J.D. (1984) Vascular and microvascular disease of the foot in diabetes. N. Engl. J. Med. 311, 1615-1619. 35 Janku, H.U., Standl, E. and Mehnert, H. (1980) Peripheral vascular disease in diabetes mellitus and its relationship to cardiovascular risk factors: screening with Doppler’s ultrasound technique. Diabetes Care 3, 207-212. 36 Bartlett, F.F., Gibbons, G.W. and Wheelock, F.C. Jr. (1986) Aortic reconstruction for occlusive disease: comparable results in diabetics. Arch. Surg. 121, 1150-l 153. 37 Wheelock, F.C. Jr. and Gibbons, G.W. (1984) Arterial reconstruction-femoral-popliteal-tibial. In: G.P. Kozak, D. Campbell and C.S. Hoar (Eds.), Management of Diabetic Foot Problems. W.B. Saunders, Philadelphia. Pennsylvania, pp. 173-187. 38 Keenan, A.M., Tindel, N.L. and Alavi, A. (1989) Diagnosis ofpedal osteomyelitis in diabetic patients using current scintigraphic techniques. Arch. Intern. Med. 149, 2262-2266.
8 39 Fernando,D.J.S.,Connor,H. andBoulton,A.J.M.(1991) The diabetic foot 1990. Diabetic Med. 8, 82-85. 40 Wagner, F.W. (1983) Algorithms ofdiabetic foot care. In: M;E. Levin and F.W. O’Neal (Eds.), The Diabetic Foot. C.V. Mosby Co., St.Louis, Missouri, pp. 291-300. 41 Knighton, D.R., Ciresi, K.F., Fiegel, V.D., Austin, L.L. and Butler, E.L. (1986) Classification and treatment of chronic non-healing wounds. Successful treatment with autologous platelet-derived wound healing factors (PDWHF). Ann. Surg. 204, 322-330. 42 Pecoraro, R.E. (1991) Diabetic skin ulcer classification for clinical investigations. Clin. Mater., 8, 257-262. 43 Pecoraro, R.E., Reiber, G.E. and Burgess, E.M. (1990) Pathways to diabetic limb amputation - basis for prevention. Diabetes Care 13, 513-521. 44 Rothman, K.J. (1976) Causes. Am. J. Epidemiol. 104, 587-592 (Abstract). 45 Rothman, K.J. (1986) Modern Epidemiology. Little, Brown, Boston, Massachusetts. 46 Fernando, D.J.S., Masson, E.A., Veves, A. and Boulton, A.J.M. (1991) Limited joint mobility: relationship to abnormal foot pressures and diabetic foot ulceration. Diabetes Care 14, 8-l 1.
47 Duckworth, T., Boulton, A.J.M., Betts, R.P., Franks, C.I. and Ward, J.D. (1985) Plantar foot pressure measurements and the prevention of ulceration in the diabetic foot. J. Bone Jt Surg. 67B, 79-85. 48 Boulton, A.J.M. (1987) The importance of abnormal foot pressures and gait in the causation of foot ulcers. In: H. Connor, A.J.M. Boulton and J.D. Ward (Eds.), The Foot in Diabetes. John Wiley & Sons, Chichester, pp. 11-21. 49 Apelqvist, J., Castenfors, J., Larsson, J., Stenstrom, A. and Agardh, CD. (1989) Prognostic value of systolic ankle and toe blood pressure levels in outcome of diabetic foot ulcer. Diabetes Care 12, 373-378. 50 Veves, A., Masson, E.A., Fernando, D.J.S. and Boulton, A.J.M. (1989) Use of experimental padded hosiery to reduce abnormal foot pressures in diabetic neuropathy. Diabetes Care 12, 653-655. 51 Mueller, M.J., Diamond, J.E., Sinacore, D.R., Delitto, A., Blair III, V.P., Drury, D.A. and Rose, S.J. (1989) Total contact casting in treatment of diabetic plantar ulcers: controlled clinical trial. Diabetes Care 12. 384-388.
Roger E. Pecoraro, M.D. 1943-1991 From time to time a gifted clinical investigator appears and makes substantive contributions to our knowledge of medicine. Such a person was Roger E. Pecoraro, M.D., Associate Professor of Internal Medicine, University of Washington, Seattle, WA, who died December 17, 1991. The research interests of Dr. Roger Pecoraro combined an understanding of biochemistry and pathophysiology with keen clinical observations. Working with patients stimulated many diabetes care and control questions. After carefully observing clinical phenomena, he studied available data, and formulated theories, which often challenged conventional wisdom. He published papers on the measurement of glycated hemoglobin, outpatient management of chronic diseases, treatment of outpatient foot infections, and determinants of tissue repair in the diabetic foot. Joining the University of Washington faculty in 1975, he helped start the Seattle VA General Internal Medicine Program. He delighted in managing patients with complicated diabetes. At the same time that he was pursuing clinical research, he dedicated himself to rendering excellent care to his patients. He represented the best in terms of being a caring and compassionate physician. When several important clinical topics lacked clarity, he proposed measures to further characterize the mechanisms involved. His research papers on the pathogenesis and evolution of diabetic foot lesions stand as seminal publications in this most difficult area. His observations and thinking will serve as a beacon guiding investigators and clinicians for years to come. Descriptions of diabetic lesions resulted in development of the Seattle Wound Classification System, which complemented prior classification systems by carefully describing lesions observed in outpatient populations. Likewise an algorithm was developed and validated to allow noninvasive characterization of diabetes type. He was particularly interested in the role of nutritional parameters and growth factors in wound healing. Roger (and his colleagues) provided an insightful description of causal pathways leading to diabetic limb amputation, and he suggested how patients and health care professionals could alter a number of risk factors and decrease the major human and dollar costs accompanying diabetic limb loss. We acknowledge the many contributions of Dr. Roger E. Pecoraro. His clinical observations and investigations helped awaken research interest and advance understanding of the diabetic foot problem. As health care providers working in the field of diabetes, we shall always remain indebted to Roger Pecoraro, M.D.
1
00627
Mini-review
The diabetic foot problem - a failed system of health care? Karl E. Sussman a, Gayle Reiberb and Stephen
F. Albert a
“Denver VA Medical Center, University of Colorado Health Sciences Center, Denver CO 80220, USA and bDepartment of Health Services. School of Public Health and Community Medicine, University of Washington, Seattle, WA 98195. USA and Health Services Research and Development, Seattle VA Medical Center, Seattle, WA 98195, USA (Received 18 November 199 1) (Accepted 9 January 1992)
Summary It is evident that there is excess morbidity and mortality as a consequence of foot problems in patients with diabetes mellitus. Most of the data relative to foot lesions is taken from the study of subsets of diabetic patients undergoing lower extremity amputation. Such data probably do not provide accurate information relative to the incidence and/or prevalence of diabetic foot problems. Available evidence does suggest that diabetic foot care may be inadequate and the efficacy of various diagnostic and therapeutic modalities has not been proven. Advances have been made in obtaining a better understanding of the microbiology of lower extremity infected lesions both in hospitalized patients and in those subjects being followed in the outpatient setting. Attention should be directed at developing a systematic classification of foot lesions which can be universally applied. We need to understand and relate to those risk factors contributing to the development and progression of lower extremity lesions in the diabetic patient. In evaluating the efficacy of diverse diagnostic and therapeutic approaches, well-controlled clinical investigations need to be undertaken. Attention should be focussed upon both measures of process and outcome where appropriate. Finally, there needs to be recognition that the problem of the diabetic foot lesion represents a major public health challenge. Key words: Diabetes;
Foot care; Prevention;
Health care delivery;
Notwithstanding the tremendous advances which have been made in the delivery of health care to patients with diabetes, one has the uneasy feeling that there is excess morbidity and perhaps mortality as a consequence of foot problems [ l-51. In Correspondence to: K.E. Sussman, M.D., VA Medical Center, 1055 Clermont Street, Denver, CO 80220, USA. This article is dedicated to our esteemed colleague Roger E. Pecoraro, M.D., for his major scientific contributions to research concerning diabetic foot problems.
Epidemiology
fact, precise data relative to the incidence and/or prevalence of foot problems in the diabetic are remarkably scarce, this standing in contrast to our knowledge of retinopathy or nephropathy in this patient population. In addition, there are relatively few analytic studies which attempt to quantify risk factors which play a role in the development and progression of diabetic lower extremity lesions. We do have some information relative to the
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frequency of amputations in patients with diabetes. Most and Sinnock have reported that 459/, of all lower extremity amputations are performed on patients with diabetes [6]. This figure may be an underestimate of the number of lower extremity amputations which can be attributed to diabetes. Others have stated that perhaps 70”#; of lower extremity amputations were performed in patients with diabetes [2]. Overall, diabetic patients have a 15 times higher age-adjusted risk of lower extremity amputations than nondiabetics [ 61. While clearly, the event of amputation is of major importance to the diabetic patient, such information does not in and of itself provide data relative to the incidence and prevalence of diabetic foot problems. Most published case series represent unique practice catchment areas, lack appropriate control groups and thus limit the inferences which can be drawn. Available amputation data are largely surgical case series that reflect a select referral population. Diabetic amputations are unequivocable and measurable, but the data acquired should be subject to more critical analysis and review. Reported data should reflect only diabetic, non-traumatic, non-cancer amputations. It would be helpful, if in the reports, information was provided as to the site of amputation, even though at times this is determined by the preference and clinical judgement of the clinician. Finally, in risk assessment, one needs information as to whether the procedure was the first ever amputation to an extremity, a revision, subsequent amputation or a contralateral amputation. The indications for amputation may vary amongst health professionals, so that even as a rough guide, the information relative to amputation rates may not be helpful in estimating the prevalence and incidence of diabetic foot problems. Indeed, the evidence suggests that it is only a small fraction of patients with foot lesions who progress to the point where amputation is required [ 71. The number of patients with foot or lower extremity lesions greatly exceeds those undergoing amputations. It has been estimated that 25 9’, of patients with
diabetes will consult physicians, surgeons, podiatrists or other health professionals for a diabetesrelated foot or leg problem [ 81. In fact, solid data relative to the prevalence of foot problems are difficult to find in the current literature. Even data relative to hospital discharge rates for diabetic foot problems are scarce. Such information again might underestimate the prevalence of diabetic foot problems, but at least would be closer to actual morbidity as a consequence of serious problems involving the foot or the lower extremity in the patient with diabetes. The most frequent cause of hospitalization of diabetic patients is due to the existence of serious foot or lower extremity problems [ 11. One out of five admissions to hospitals in the United Kingdom is for the treatment of foot problems in the patient with diabetes [9]. Boulton estimates that the mean duration of hospital admissions for foot problems in the diabetic patient is 4 weeks [I]. Whatever data exists suggests that as a complication of diabetes, foot problems exact a toll not only in terms of morbidity and mortality but also relative to costs as well. In the United States, the actual cost of diabetic foot problems is unknown [lo]. A cost of illness study assessing U.S. economic costs for non-insulin-dependent diabetes (NIDDM) in 1986 estimated ‘chronic skin ulcers’ totaled $250 million in health care expenditures [ 111. Of 103 admissions for diabetic foot infections, an average length of stay of 22 days was recorded at an estimated cost of $6600 per hospitalization [ 121. In the United Kingdom, more hospital beds are filled with people with diabetic foot complications than are filled from all other diabetic complications combined [ 131. The direct cost of an amputation, including hospitalization, surgery, and anaesthesia, is approximately $20000 to $25000 per case [lo]. To further compound the problem concerning the delivery of optimal diabetic foot care, various therapeutic approaches are recommended in the absence of well controlled clinical trials. We recognize that, on the face of it, some recommendations seem fundamentally sound and that no controlled clinical trials are necessary (e.g.,
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patients with diabetes should always wear shoes when walking about the house). Nevertheless, recommendations for certain, more sophisticated therapies (e.g., therapeutic shoes) may need substantiation. Within this context, it is evident that health professionals may not focus enough attention on preventive strategies concerning foot care in the patient population with diabetes. Especially disturbing are data which demonstrated that the rate of foot examination over the period of a year ranges from 30 to 50 ?, in caring for patients with diabetes [ 14-161. On the day in which diabetic patients were being seen, the frequency of foot examination was as low as 12-19% [ 14,151. The situation may be worse insofar as the quality of the foot examination may vary and may be insufficient to detect serious or potential foot pathology. A recent report suggests that there may be delays in referring patients with serious foot problems which may make therapy more difficult and contribute to greater morbidity, more extensive amputations and excess limb loss. Mills and associates reported on a review of records of 55 patients with localized gangrene or infection 1171. In 16 of the patients (29%), there was a prolonged delay between initial treatment and referral for definitive care. The causes of the delay were underestimation of the severity of the foot infection in ten patients, and lack of recognition of ischemia due to large vessel occlusive disease in six. These delays led to more proximal levels of amputation in six patients, including three belowknee amputations in patients with limbs that were initially thought to be salvageable [ 171. Evidence does suggest that if more attention is directed to foot care as part of an effort in intensive care in the diabetic patient that serious morbidity can be avoided [ 7,18,19]. Especially striking are the data of Edmonds and associates who demonstrated clearly the value of a program of intensive attention to foot care [ 71. In their clinic, a major emphasis was on the use of specially constructed shoes, intensive chiropody and better directed antibiotic treatment. In their series of patients, healing was achieved in 86’~ (*O~/ZX)of
neuropathic ulcers and in 72:)” (lo7/143) of ischemic ulcers. Relapse frequency was 26Y/, in patients wearing special shoes, and 83:; in patients preferring to wear their own shoes. In the 2-year period before the establishment of this special clinic devoted to foot care, the annual frequency of amputations was 1 l-12 per year, with the clinic in operation there were 5-7 amputations yearly. These data, while not representing a definitive controlled study, do indeed suggest that intensive attention to foot care may dramatically alter morbidity statistics and result in positive outcomes in the evolution and progression of foot lesions. Patient knowledge concerning appropriate foot care may be woefully lacking [9]. In a United Kingdom survey, the vast majority of diabetic patients with foot ulcers were purchasing shoes over the counter or by mail order [93. Their feet were not being measured and the shoes were not being checked to see whether there was a satisfactory fit. Given this somewhat negative assessment, it is appropriate to consider what is being done at the present time to improve clinical care of patients with foot problems and what additional measures might be required. It is important to recognize that our approach to foot lesions has improved over the years. For example, more refined microbiological techniques have demonstrated the importance of anaerobic organisms in infected ulcers [ 8,20-251. Special attention has been directed to the presence of Bacteroides as well as Peptostreptococcus and Peptococcus existing in combination with other organisms in infected lesions in diabetic patients [36,27]. Also, the literature has pointed to the need to culture deep tissues (for example, during debridement) to be able to assess the offending organisms and devise appropriate antibiotic regimens [ 828.291. Appropriate surgical debridement may be as important as the selection of a specific antimicrobial agent for the successful management of patients with infections caused by anaerobic microorganisms [ 271. It should be noted that microbiological assess-
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ment may yield different results, depending upon whether the investigation is directed at hospitalized patients undergoing amputation or the more prevalent group of diabetic subjects with less severe infections [30]. Most foot infections are not complicated by deep tissue involvement, osteomyelitis or gangrene [ 301. Lipsky and associates demonstrated in an outpatient diabetic population with foot infections, the most common offending organisms are gram-positive cocci. These organisms were isolated in 89% of cases and were the sole pathogen in 42% of the infections observed [ 301. In contrast, amputation patients have an overwhelming incidence of polymicrobial infections with 5.8 organisms being isolated on curettage culture. In the outpatients with foot infections, aerobic gram-negative organisms may be isolated (36%) and the incidence of anaerobes is really quite low (7%). These latter organisms are most commonly seen in polymicrobial infections [ 301. Another advance in foot care has been the use of arterial reconstructive procedures. Although microcirculation abnormalities exist in patients with diabetes, their role in the pathogenesis of foot lesions has been questioned [31-341. Macrovascular disease has been estimated to be present in approximately 16% of individuals with diabetes and is thought to represent the critical vascular abnormality in the development and progression of lower extremity lesions [8,35-371. Arterial reconstructive procedures are being used to enhance wound healing and may obviate the need for amputation [ 8,17,36,37]. However, the widespread use of arterial reconstructive procedures to augment wound healing is not warranted at this point in time. Clearly, this is an area in which controlled studies need to be undertaken not only to establish the effectiveness of this approach but also to define the indications and the patients most suitable for this procedure in the setting of faulty wound healing. There has been a recent flurry of interest in the use of white blood cell scintigraphy in the diagnosis of osteomyelitis in patients with diabetes [38]. The radioactive label employed is
indium-1 11. The technique appears to be better for the diagnosis of osteomyelitis when present in the tarsometatarsal region as opposed to the toes. In 19 patients who had clinically evident osteomyelitis, white blood cell scintigraphic studies were positive in 100% of cases. In the report by Keenan and associates, white blood cell scintigraphy appeared to be more accurate than conventional X-ray studies or investigations using three-phase bone scintigraphy [ 381. However, false positive results are obtained due to a number of factors, including the presence of aseptic soft tissue and bone inflammation, hyperemia/hypervascularity which may or may not be associated with inflammation, inflammatory arthritis, adjacent cellulitis or when an ulcer is located particularly close to bone [ 381. Other constraints include the presence of neuropathic disease, the presence of trauma, and degenerative arthritis. Even in the study by Keenan, it is not clear whether the technique will detect osteomyelitis when not suspected, or whether the technique can differentiate osteomyelitis from diabetic neuroarthropathy. Finally, the literature is not clear whether white blood cell scintigraphy has made any difference in clinical treatment or therapeutic outcome. Indeed, the feeling is extant that this is an expensive technique which really does not have much of a role in the management of foot problems [39]. Concerning recommendations as to future courses of action, the first step should be to acquire more precise data concerning lower extremity lesions in the patient population with diabetes. It is necessary to compile accurate data concerning the incidence and prevalence of diabetic foot problems. This information needs to be collected from all health care units caring for patients with diabetes. We need to know the total number of diabetic patients being treated as well as the number of patients presenting with foot problems. Since patients may have repeated foot problems, data must be acquired concerning the number of patients with foot problems as well as the number of episodes per patient. Foot problems must be classified according to severity to maximize the usefulness of the data. There are
several wound classification systems described in the literature which have been developed for specific purposes, e.g. assessment of amputation risk, healing potential/amputation level, clinical care or clinical/epidemiology research [ 1,10,40,41]. It is evident that the purpose for which the classification is to be used influences the type of system developed [42]. Hopefully, a standardized classification system can be promulgated which will yield meaningful data relative to specific therapeutic modalities as well as shed light on the epidemiology of chronic wounds in the patient population with diabetes. Such a system should be based upon well-defined objective criteria and should avoid subjective or vague wound descriptions [42]. Pecoraro has discussed the advantages and the potential utility of the various classification systems [ 421. We need to know more about the factors that play a role in the development of foot lesions. The second recommendation would be to develop a more systematic approach to the study, classification and evaluation of the risk factors contributing to the development and progression of lower extremity lesions in the diabetic patient. It would seem that the sophisticated approach employed by Pecoraro and colleagues could be applied logically to discerning and quantitating the role of various factors in the development of and progression of foot lesions in the patient with diabetes [43]. These authors employed a model to study causation based on the concept that there exist two general types of causes, ‘sufficient’ and ‘component’ causes [44,45]. Sufficient causes inevitably produce the effect and in the case of lower extremity amputation referred to, the set of minimal conditions or events that inevitably result in amputations [43]. Minimal meant that none of the conditions or events were superfluous. Component causes were defined& causes of interest that are not sufficient in themselves but are components of one or more distinctive sufficient causes. Removing or blocking of a component cause renders the action of other components as insufficient to produce the effect being studied. Thus, in a defined causal pathway leading to lower
extremity amputation, the existence of neuropathy and trauma might be considered as just two component causes amongst others which form the completed causal chain leading to amputation. The absence of neuropathy or trauma in a designated causal chain would prevent the expression of the other components and therefore the amputation would not ensue. Based on previous literature, the authors studied seven potential causes and four major pathophysiologic mechanisms including neuropathy, ischemia, infection and wound healing failure, two common soft tissue complications, cutaneous ulceration and gangrene, and minor trauma to the extremity [43]. In their study, they found that the sequence of minor trauma, cutaneous ulceration and wound healing failure accounted for 727, of amputations, this causal chain being commonly associated with infection and gangrene [43]. In 46% of amputations, ischemia was a causal factor, infection in 599; of amputations, neuropathy - 6 1%) faulty wound healing - 8 1%) gangrene - 55 %, and initial minor trauma -81:;. The limitation of this particular study may be that only males were studied, although it does seem that males are at greater risk for lower extremity amputation [ 61. Notwithstanding, it would seem that this method of analysis could well be applied and refined in the study and characterization of those factors playing a role in foot problems in the patient with diabetes. Perhaps, one could include in this analysis the newer methods of evaluating factors which might play a role in the development and progression of foot lesions, for example the combined use of ankle and toe pressure measurements to predict wound healing or pedobarographic studies to study weight bearing and special areas of the foot being subjected to abnormal pressures and loads [ 1,39,46-493. The third recommendation would be to initiate well controlled studies of various diagnostic and treatment modalities, using both process and outcome measures to assess therapeutic efficacy. The first two recommendations related to the need to define foot lesions and the factors that
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play a role in pathogenesis. Using these latter constructs to define the nature of foot problems in patients, it should be possible to assess our success in our attempts in diagnosis and treatment. It is critical to differentiate between process and outcome measurements in gauging our therapeutic success. For example, it may be quite useful as a diagnostic process to use scintigraphy to diagnose osteomyelitis as opposed to diabetic neuroarthropathy, but this may not make any difference in terms of outcomes [ 38,391. By the same token, assessing therapeutic efficacy by simply measuring outcomes may yield misleading information. One must be able to establish that a given intervention has resulted in a change in some process which thereby was correlated with a given alteration in outcomes. Thus special shoes should be shown to have altered patterns of weight bearing which in turn is reflected in decreased incidence and/or prevalence of foot lesions. An example of a process measure is the study by Veves and colleagues in which they evaluated the effectiveness of experimental padded hosiery in reducing abnormal foot pressures [ 501. The well controlled study of the use of total contact casting in treatment of diabetic plantar ulcers is a good example of an investigation directed at outcome assessment [ 5 11. Finally, there needs to be recognition that the problem of the diabetic foot lesion represents a major public health challenge. The evidence suggests that this issue is not only one of morbidity and mortality, but also one of costs to society in terms of the expense of health care, and also lost days of productivity as well. Research needs to be undertaken to demonstrate whether diagnostic and treatment strategies are biologically plausible and therapeutically efficacious. Then, if such strategies prove to be cost effective, they should be implemented by health professionals. Strategies proven to be effective in the prevention of foot lesions need financial support. It is incumbent upon health professionals to demonstrate which measures are medically sound and should be universally implemented. Third party insurance carriers and other entities providing financial sup-
port to the health care system must be informed as to the severity of the problem of the diabetic foot and also advised as to what specific measures should be undertaken to help the patient with diabetes. As such, problems in preventing and treating foot lesions still remain a challenge. In considering this topic, we have not attempted to present a comprehensive review of foot lesions and their management. Rather we have focussed on certain problems relative to how the challenge of diabetic foot lesions is presently being pursued. It is evident that data acquisition is critical in order to understand and delineate existing problems relative to lower extremity lesions in diabetic patients. Furthermore, emphasis must be placed on conducting well controlled clinical studies to determine the efficacy of various diagnostic and therapeutic measures. Where appropriate, attention should be devoted to obtaining both process and outcome measures to establish the most effective approaches in the management of foot lesions. The evidence currently available suggests that great strides can be made in decreasing morbidity and mortality due to diabetic foot lesions, but the overall effort needs more rigorous studies, clinical classification, and a reorientation towards evaluating patient and clinical management strategies.
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24 Sapico, F.L., Bessman, A.N. and Canawati, H.N. (1982) Bacteremia in diabetic patients with infected lower extremities. Diabetes Care 5. 101-104. 25 Sapico, F.L., Canawati, H.N., Witte, J.L.. Montgomerie. J., Wagner, F.W. Jr. and Bessman. A.N. (1980) Quantitative aerobic and anaerobic bacteriology of infected diabetic feet. J. Clin. Microbial. 12. 413-420. 26 Krepel, C.J.. Gohr, C.M.. Edmiston, C.E. Jr. and Farmer, S.G. (1991) Anaerobic pathogenesis: collagenase production by Peptostreptococcus magnus and its relationship to site of infection. J. Infect. Dis. 163, 1148-l 150. 27 Wilson, W.R. (1991) Treatment of infections caused by anaerobes. J. Chemother. 3, 7-l 1. 28 Sharp, C.S., Bessman, A.L. and Wagner, F.W. (1979) Microbiology of superficial and deep tissues in infected diabetic gangrene. Surg., Gynecol. Obstet. 149,217-219. 29 Silva, J.R. Jr. and Sussman, K.E. (1987) Infection in diabetes. In: K.E. Sussman, B. Draznin and W.E. James (Eds.), Clinical Guide to Diabetes Mellitus. Alan R. Liss, Inc., New York, pp. 183-191. 30 Lipsky, B.A., Pecoraro, R.E., Larson, S.A., Hanley, M.E. and Ahroni, J.H. (1990) Outpatient management of uncomplicated lower extremity infections in diabetic patients. Arch. Intern. Med. 150, 790-797. 31 Walsh, C.H., Soler, M.G. and Fitzgerald, M.G. (1975) Association of foot lesions with retinopathy in patients with newly diagnosed diabetes. Lancet i, 878-880. 32 Young, R.J. (1987) Identification of the subject ‘at risk’ of foot ulceration. In: H. Connor, A.J.M. Boulton and J.D. Ward (Eds.). The Foot in Diabetes. John Wiley & Sons, Chichester, pp. l-10. 33 Tooke, J.E. (1987) Blood flow abnormalities in the diabetic foot: diagnostic aid or research tool?. In: H. Connor, A.J.M. Boulton and J.D. Ward (Eds.), The Foot in Diabetes. John Wiley & Sons, Chichester, pp. 23-3 1 34 Logerfo, F.W. and Coffman, J.D. (1984) Vascular and microvascular disease of the foot in diabetes. N. Engl. J. Med. 311, 1615-1619. 35 Janku, H.U., Standl, E. and Mehnert, H. (1980) Peripheral vascular disease in diabetes mellitus and its relationship to cardiovascular risk factors: screening with Doppler’s ultrasound technique. Diabetes Care 3, 207-212. 36 Bartlett, F.F., Gibbons, G.W. and Wheelock, F.C. Jr. (1986) Aortic reconstruction for occlusive disease: comparable results in diabetics. Arch. Surg. 121, 1150-l 153. 37 Wheelock, F.C. Jr. and Gibbons, G.W. (1984) Arterial reconstruction-femoral-popliteal-tibial. In: G.P. Kozak, D. Campbell and C.S. Hoar (Eds.), Management of Diabetic Foot Problems. W.B. Saunders, Philadelphia. Pennsylvania, pp. 173-187. 38 Keenan, A.M., Tindel, N.L. and Alavi, A. (1989) Diagnosis ofpedal osteomyelitis in diabetic patients using current scintigraphic techniques. Arch. Intern. Med. 149, 2262-2266.
8 39 Fernando,D.J.S.,Connor,H. andBoulton,A.J.M.(1991) The diabetic foot 1990. Diabetic Med. 8, 82-85. 40 Wagner, F.W. (1983) Algorithms ofdiabetic foot care. In: M;E. Levin and F.W. O’Neal (Eds.), The Diabetic Foot. C.V. Mosby Co., St.Louis, Missouri, pp. 291-300. 41 Knighton, D.R., Ciresi, K.F., Fiegel, V.D., Austin, L.L. and Butler, E.L. (1986) Classification and treatment of chronic non-healing wounds. Successful treatment with autologous platelet-derived wound healing factors (PDWHF). Ann. Surg. 204, 322-330. 42 Pecoraro, R.E. (1991) Diabetic skin ulcer classification for clinical investigations. Clin. Mater., 8, 257-262. 43 Pecoraro, R.E., Reiber, G.E. and Burgess, E.M. (1990) Pathways to diabetic limb amputation - basis for prevention. Diabetes Care 13, 513-521. 44 Rothman, K.J. (1976) Causes. Am. J. Epidemiol. 104, 587-592 (Abstract). 45 Rothman, K.J. (1986) Modern Epidemiology. Little, Brown, Boston, Massachusetts. 46 Fernando, D.J.S., Masson, E.A., Veves, A. and Boulton, A.J.M. (1991) Limited joint mobility: relationship to abnormal foot pressures and diabetic foot ulceration. Diabetes Care 14, 8-l 1.
47 Duckworth, T., Boulton, A.J.M., Betts, R.P., Franks, C.I. and Ward, J.D. (1985) Plantar foot pressure measurements and the prevention of ulceration in the diabetic foot. J. Bone Jt Surg. 67B, 79-85. 48 Boulton, A.J.M. (1987) The importance of abnormal foot pressures and gait in the causation of foot ulcers. In: H. Connor, A.J.M. Boulton and J.D. Ward (Eds.), The Foot in Diabetes. John Wiley & Sons, Chichester, pp. 11-21. 49 Apelqvist, J., Castenfors, J., Larsson, J., Stenstrom, A. and Agardh, CD. (1989) Prognostic value of systolic ankle and toe blood pressure levels in outcome of diabetic foot ulcer. Diabetes Care 12, 373-378. 50 Veves, A., Masson, E.A., Fernando, D.J.S. and Boulton, A.J.M. (1989) Use of experimental padded hosiery to reduce abnormal foot pressures in diabetic neuropathy. Diabetes Care 12, 653-655. 51 Mueller, M.J., Diamond, J.E., Sinacore, D.R., Delitto, A., Blair III, V.P., Drury, D.A. and Rose, S.J. (1989) Total contact casting in treatment of diabetic plantar ulcers: controlled clinical trial. Diabetes Care 12. 384-388.
Roger E. Pecoraro, M.D. 1943-1991 From time to time a gifted clinical investigator appears and makes substantive contributions to our knowledge of medicine. Such a person was Roger E. Pecoraro, M.D., Associate Professor of Internal Medicine, University of Washington, Seattle, WA, who died December 17, 1991. The research interests of Dr. Roger Pecoraro combined an understanding of biochemistry and pathophysiology with keen clinical observations. Working with patients stimulated many diabetes care and control questions. After carefully observing clinical phenomena, he studied available data, and formulated theories, which often challenged conventional wisdom. He published papers on the measurement of glycated hemoglobin, outpatient management of chronic diseases, treatment of outpatient foot infections, and determinants of tissue repair in the diabetic foot. Joining the University of Washington faculty in 1975, he helped start the Seattle VA General Internal Medicine Program. He delighted in managing patients with complicated diabetes. At the same time that he was pursuing clinical research, he dedicated himself to rendering excellent care to his patients. He represented the best in terms of being a caring and compassionate physician. When several important clinical topics lacked clarity, he proposed measures to further characterize the mechanisms involved. His research papers on the pathogenesis and evolution of diabetic foot lesions stand as seminal publications in this most difficult area. His observations and thinking will serve as a beacon guiding investigators and clinicians for years to come. Descriptions of diabetic lesions resulted in development of the Seattle Wound Classification System, which complemented prior classification systems by carefully describing lesions observed in outpatient populations. Likewise an algorithm was developed and validated to allow noninvasive characterization of diabetes type. He was particularly interested in the role of nutritional parameters and growth factors in wound healing. Roger (and his colleagues) provided an insightful description of causal pathways leading to diabetic limb amputation, and he suggested how patients and health care professionals could alter a number of risk factors and decrease the major human and dollar costs accompanying diabetic limb loss. We acknowledge the many contributions of Dr. Roger E. Pecoraro. His clinical observations and investigations helped awaken research interest and advance understanding of the diabetic foot problem. As health care providers working in the field of diabetes, we shall always remain indebted to Roger Pecoraro, M.D.
