- Email: [email protected]
The costs of diabetic foot: The economic case for the limb salvage team
The costs of diabetic foot: The economic case for the limb salvage team Vickie R. Driver, MS DPM, FACFAS,a Matteo Fabbi, MD,a Lawrence A. Lavery, DPM, MPH,b and Gary Gibbons, MD,a Boston, Mass; and Georgetown, Tex Background: In 2007, the treatment of diabetes and its complications in the United States generated at least $116 billion in direct costs; at least 33% of these costs were linked to the treatment of foot ulcers. Although the team approach to diabetic foot problems is effective in preventing lower extremity amputations, the costs associated with implementing a diabetic foot care team are not well understood. An analysis of these costs provides the basis for this report. Results: Diabetic foot problems impose a major economic burden, and costs increase disproportionately to the severity of the condition. Compared with diabetic patients without foot ulcers, the cost of care for patients with a foot ulcer is 5.4 times higher in the year after the first ulcer episode and 2.8 times higher in the second year. Costs for the treatment of the highest-grade ulcers are 8 times higher than for treating low-grade ulcers. Patients with diabetic foot ulcers require more frequent emergency department visits, are more commonly admitted to hospital, and require longer length of stays. Implementation of the team approach to manage diabetic foot ulcers within a given region or health care system has been reported to reduce long-term amputation rates from 82% to 62%. Limb salvage efforts may include aggressive therapy, such as revascularization procedures and advanced wound healing modalities. Although these procedures are costly, the team approach gradually leads to improved screening and prevention programs and earlier interventions, and thus seems to reduce long-term costs. Conclusions: To date, aggressive limb preservation management for patients with diabetic foot ulcers has not usually been paired with adequate reimbursement. It is essential to direct efforts in patient-caregiver education to allow early recognition and management of all diabetic foot problems and to build integrated pathways of care that facilitate timely access to limb salvage procedures. Increasing evidence suggests that the costs for implementing diabetic foot teams can be offset over the long-term by improved access to care and reductions in foot complications and in amputation rates. ( J Vasc Surg 2010;52:17S-22S.)
Limb preservation team services have been shown to reduce major limb amputation, but the associated costs are not well understood or reported. Perhaps this is true because the burden of preventing amputations is often realized at a critical health care event, such as limb-threatening infection or acute critical limb ischemia. In many cases, these diabetic patients are at very high risk for limb loss, newly consulted for their acute event, and, therefore, in their highest health-related cost status. An adequate and comprehensive cost-effectiveness analysis must consider health states with limb-preserving impact figures and their relative cost, as it relates to severity of disease and prevention of amputations. Lower extremity amputations contribute disproportionately to diabetes-related costs.1 From the Department of Surgery, Boston University School of Medicine and Boston Medical Center;a and the Department of Surgery, Scott and White Hospital.b Competition of interest: none. This article is being co-published in the Journal of Vascular Surgery® and the Journal of the American Podiatric Medical Association. Correspondence: Lawrence A. Lavery, Scott and White Hospital, Department of Surgery, 703 Highland Spring Ln, Georgetown, TX 78628 (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest. 0741-5214/$36.00 Copyright © 2010 by the Society for Vascular Surgery and the American Podiatric Medical Association. doi:10.1016/j.jvs.2010.06.003
MAGNITUDE OF THE PROBLEM According to the Centers for Disease Control and Prevention, 7.8% of the United States population had diabetes in 2007, which equals almost 24 million persons.2 In 2007, diabetes and its complications cost the United States $174 billion; $116 billion were in direct costs and $58.3 billion in indirect costs such as loss of productivity, disability, and premature mortality.3 Peripheral vascular complications and neurologic complications, which are closely linked to foot ulceration, accounted for 31% and 24% of the expenses, respectively, and were among the major contributors to inpatient length of stay. Foot problems in persons with diabetes have been recognized as a major health issue since the times of Joslin and before the advent of insulin. The diabetic foot with gangrene was one of the leading causes of death from diabetes, second only to diabetic coma.4 The rate of hospital discharges for diabetic patients with leg/foot ulcers for 1000 diabetic patients rose from 5.4 in 1980 to 6.9 in 2003.2 Ulcer prevalence among persons aged ⬍44 years was 6.5/1000 diabetics and it rose progressively to 10.3/ 1000 diabetics in individuals aged ⬎75 years. Hospitalizations for lower extremity amputations rose from 33,000 in 1980 to 71,000 in 2005; however, average length of stay fell from 35.3 to 10.7 days during the same period. More than 60% of nontraumatic lower limb amputations occur in diabetic individuals, and at least 80% of amputations are preceded by an ulcer. The causative path17S
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way leading from a foot ulcer to amputation is well known. The progressive additive effects of neuropathy, minor trauma, ulceration, faulty healing, ischemia, and infection leading to amputation were first characterized in 1990.5 Early recognition of foot problems and effective intervention along the causative pathways may not only improve outcomes by reducing major amputations and increasing quality of life, but also reduce costs related to diabetic foot complications. Studies on diabetic foot-related health care costs are sometimes difficult to compare due to dissimilar health care systems, reimbursement methods, and access to care. THE COSTS OF DIABETIC FOOT The cost of care for diabetic patients with a lower extremity ulcer is a major economic burden compared with the management of a patient with diabetes but no ulceration. Economic factors will play an ever-increasing role because third-party payers cannot reimburse all therapies used to treat chronic ulcerations. A retrospective analysis of insurance claims from a large population of private employer-sponsored insurance enrollees during the period 1991 to 1992,6 analyzed 3013 patients aged 18 to 64 years who had 3524 ulcer episodes. They were divided into three severity-level categories according to Wagner classification: grade 1 or 2, grade 3, and grade 4 or 5. The average cost for an ulcer episode was $4595. This study showed incremental resource utilization in patients with diabetic foot ulcers progressing from Wagner grade 1 to 2 to the highest grades. Wagner grade 1 or 2 ulcer costs averaged $1929, whereas Wagner grade 3 and grade 4 or 5 ulcer costs averaged $3980 and $15,792, respectively. Inpatient expenditures accounted for 80% of the total costs. Poor vascular status was also strongly associated with longer in-hospital stays and higher average total payments. An analysis of Medicare claims data from 1995 to 1996 showed that expenditures for diabetic foot patients were three times higher than for the general population ($15,309 vs $5226), yielding a total cost for Medicare in 1995 of $1.5 billion.7 Lower extremity ulcers accounted for 24% of the overall cost for diabetic population with an ulcer. Inpatient stays accounted for 73% of increased cost.7 A retrospective nested case-control study demonstrated that the relative cost of care for diabetic patients with lower extremity ulcers ranges from 1.5 to 2.4 times higher than that of diabetic patients without an ulcer in the year before diagnosis to 5.4 times higher in the year after the ulcer episode.8 The cost of care for diabetic patients with an ulcer showed a tendency to return to the non-ulcer group only after 2 years from the first diagnosis, but was still 2.8 times higher. Excess cost was $26,490 in ulcer patients during the year of the ulcer episode and $4927 for diabetic patients without an ulcer. The excess cost persisted during the second year after the ulcer episode. The costs for diabetic foot ulcer patients were $17,245 compared with $5110 for patients with diabetes but no ulcer. Patients with diabetes and a lower extremity ulcer had more inpatient days than
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diabetic patients without ulcers (6.03 vs 1.46 days), and this difference was still significant 1 year after the ulcer episode (4.06 vs 2.61). Diabetic patients with a foot ulcer during the first year of the study also had more emergency department visits (0.42 vs 0.18) and more nonemergency outpatient visits (35.08 vs 13.05).8 Apelqvist et al9 prospectively monitored 314 patients with an ulcer episode. They documented that 54% of patients healed in 2 months, 19% healed in 3 to 4 months, and 27% healed in ⱖ5 months. Healing without amputation averaged $6664, whereas healing by amputation averaged $44,790. Hospitalization costs and topical treatment of ulcers accounted for most of the costs. For patients that healed without amputation, 37% and 45% of the total costs were for hospitalizations and ulcer treatments, and for patients that healed with amputations, 65% of total costs were for hospitalizations and 13% for ulcer treatments. The same group estimated that the long-term costs of diabetic foot ulcers remain elevated during the first 3 years after healing of an ulcer.10 A retrospective study of diabetic patients with lower extremity ulcers revealed an average cost per ulcer episode of $13,179. Again, there was an increase in cost according to ulcer depth as evaluated by the Wagner classification system. Costs associated with a Wagner grade 1 ulcer averaged $1892, and Wagner grade 4/5 ulcers averaged $27,721. This study confirmed the high impact of inpatient stay as being 77% of the overall cost. Progression from Wagner ulcers with lower grades to higher grades carried an additional increase in cost of $20,136.11 This study also confirmed a higher cost per ulcer episode in patients with poor vascular status. Patients with a diabetic foot ulcer have an average hospital length of stay that can be 50% higher than that of patients without an ulcer.12 A synopsis of the studies evaluating the costs of diabetic foot is reported in Table I. Higher grade lesions and peripheral arterial disease not only lead to higher amputation rates but are also associated with higher costs of care mainly due to higher hospitalization rates and longer length of stay. Once an ulcer is present, higher costs are projected over a period of 2 to 3 years compared with patients without foot ulcers. Socioeconomic factors and reduced or absent insurance coverage can be very important and may thwart access to limb-preserving procedures. A study of a large cohort of individuals from 1998 to 2002 showed that nonwhite, low-income, Medicare and Medicaid patients were more likely to undergo an amputation for leg ischemia and to have less access to limb salvage procedures (eg, revascularization) compared with higher income individuals with private insurances.13 This may be explained by a delay in diagnosis of critical leg ischemia and limited access to care involving both primary care and vascular surgeries. THE LIMB SALVAGE TEAM It has long been recognized that the complex nature of diabetic foot pathology is best treated with a team approach. The group from New England Deaconess Hospital
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Table I. Synopsis of studies evaluating the direct cost of diabetic foot patients First author
Study type
Study population
Holzer, 1998
Retrospective analysis of private insurance claims
3013 subjects Study period: 1991-1992 Age: 18-64 y 3524 ulcer episodes
Harrington, 2000
Retrospective analysis of Medicare claims
⬎400,000 Medicare beneficiaries with DFUs Study period: 1995-1996
Ramsey, 1999
Retrospective casecontrol study in HMO
Apelqvist, 1994
Prospective study
8905 subjects Study period: 1992-1995 Age ⬎18 y 541 foot ulcers 314 subjects with DFU Subjects followed-up through their ulcer episode
Stockl, 2004
Retrospective claims data analysis
2253 subjects Study period: 2000-2001
Results
Notes
Average ulcer episode cost: $4595 1. Primary healing: $1929 2. Healing by amputation: $44,790 Grade 1 or 2 ulcers cost: $1929 Grade 3 ulcers cost: $3980 Grade 4 or 5 ulcers cost: $15,792 Aggregate disease attributable cost: $1.45 billion Average ulcer-related cost/ year: $3609 Medicare spending among ulcer patients/y: $15,309 All Medicare spending among all Medicare patients/y: $5266 Average cost of ulcer episode over 1 year: $26,490 Total attributable cost of DFU: $27,987a Average ulcer episode cost: 1. Primary healing: $6664 2. Healing by amputation: $44,790 Average ulcer episode cost: $13,179 Grade 1 ulcers: $1892 Grade 2 ulcers: $4345 Grade 3 ulcers: $12,255 Grade 4 or 5 ulcers: $27,721
Severity grading according to Wagner classification as 1 or 2; 3; 4 or 5
Excess cost for ulcer patients: 73.7% inpatient 10.9% outpatient 11.4% home health 4.0% SNF/hospice
Ulcer patients had more inpatient days and more emergency department visits over the study period Cost for ulcer patients: 61% inpatient 39% outpatient Severity grading according to Wagner classification as 1; 2; 3; 4 or 5 77% inpatient cost
DFU, Diabetic foot ulcer; HMO, health maintenance organization; SNF, skilled nurse facility. a Attributable cost of DFU has been calculated as the difference between average expenditures for DFU patients over the first and second years after diagnosis and the expenditures the year before DFU diagnosis.
and Joslin Diabetes Clinic in Boston, Massachusetts, is regarded as a forerunner of this approach. In 1992, LoGerfo et al14 published the results of aggressive use of distal bypass grafting revascularization in diabetic patients with ischemic ulcers. They showed a progressive increase in the bypass/amputation ratio comparing outcomes of patients from 1984 to 1990. A retrospective evaluation was reported of two groups of patients followed-up before and after implementing diabetic foot care with a team approach that focused on aggressive early intervention and extensive use of surgical revascularization. LoGerfo et al15 showed a reduction in major amputations, overall length of stay, and total cost of care. The authors, however, pointed out that Medicare reimbursement was inadequate to cover all the procedures. The widespread use of endovascular revascularization techniques has further broadened the spectrum of revascularization options for diabetic patients with critical leg ischemia. A prospective study of peripheral angioplasty at both proximal and distal levels showed an excellent limb salvage rate, with only 10 of 191 patients (5.2%) undergoing a major amputation.16 Whether an open surgical or an
endovascular procedure should be the first-line treatment for diabetic patients with critical leg ischemia is still a matter of debate and so is which of these two procedures might represent the most cost-effective treatment. Regardless of the procedure type, aggressive and effective revascularization is crucial in limb salvage, particularly in amputation reduction, an important driver of cost. Many studies have now shown that a team approach to diabetic foot conditions is effective in amputation prevention. Zayed et al17 reported results of a retrospective analysis of 312 patients with diabetes and critical leg ischemia and demonstrated a reduction in amputation rate in a multidisciplinary setting. The team was composed of a vascular and podiatric surgeon, diabetologist, tissue viability nurse, interventional radiologist, and a radiology coordinator. A retrospective study from Sweden18 showed a 78% decrease in major amputations after the implementation of a multidisciplinary program for the management of diabetic foot patients. A prospective study of a United States population showed that podiatry-vascular surgery collaboration resulted in 83% limb salvage at 5 years.19
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Likewise, Driver et al20,21 reported the outcomes of a multidisciplinary team to prevent amputations reduction. During a 4-year period, there was an 82% reduction in major amputations. A prospective study from the United Kingdom showed a 62% reduction in major amputations and a 40% decrease in all amputations during an 11-year period after a diabetic foot care service was started.22 Implementation of existing guidelines is likely to lower amputation rates. Results from a prospective study at a specialized diabetic foot clinic in Italy showed that implementing the International Consensus on the Diabetic Foot recommendations resulted in a decrease in major amputations from 10.7 per 100,000 inhabitants at the beginning of the study to 6.24 per 100,000 inhabitants after 5 years. This decrease was paired with a progressive increase in minor amputations.23 The authors also documented a progressive extensive referral to the diabetic foot service during the study period. This aspect is of particular interest because it shows that improving provider education about diabetic foot disease may also improve more appropriate referral patterns. COST EFFECTIVENESS OF INTERVENTIONS Few studies have addressed the economic benefits of interventions for the prevention and treatment of diabetic foot disease. Most studies explore results from predictive models, with the most common being the Markov model. This can be a useful mathematic tool for obtaining a projection of cost and effects of an intervention. This method for modeling disease, such as diabetic foot ulcers, is relevant because it can take into account both the chronicity of the disease and the occurrence of the same events more than once.24 However, data from these studies are difficult to compare due to differences in demographics and health care systems. A model to evaluate the effects of different types of interventions on economic outcomes in a theoretic cohort of 10,000 diabetic patients25 showed that prevention and appropriate management of diabetic foot patients might avoid up to 50% of amputations. The authors estimated that educational intervention, a multidisciplinary team approach, and therapeutic footwear coverage could avoid 72%, 47%, and 53% of amputations, respectively. This translates to $1,100,000, $750,000, and $850,000 in potential savings over 1 year for each intervention. The authors concluded that prevention, a multidisciplinary team approach, and therapeutic footwear could save from $2,900 to $4,442 in per patient costs. These United States data strongly indicate a cost-savings from the initiation of preventive strategies in the management of diabetic foot patients in concert with a multidisciplinary team approach. Apelqvist et al24 analyzed 5 years of cost-utility data from preventive interventions on patients with diabetic foot ulcers. The study focused on implementation of guidelines from the International Working Group on Diabetic Foot (IWGDF) and sought to demonstrate that the costs of implementing a preventive system would be offset by the benefits of amputation prevention.24 This study showed
that an intensive prevention strategy composed of patient education, foot care, and therapeutic footwear is costeffective in a Swedish population, if the risk of foot ulcers and amputations can be reduced by 25%. Another European study used a Markov model to assess the potential economic effects of two interventions in patients with diabetic foot ulcers: intensive glycemic control and optimal foot care as defined by IWGDF guidelines, taken singularly or coupled vs standard of care without guidelines implementation.26 The study showed that the greatest reduction in amputation would have been achieved with the combination of the two interventions. The most favorable cost-effectiveness ratio was strongly linked to ulcer prevention. The increased costs for guideline implementation were associated with less than $25,000 per quality-adjusted life-years gained (1999 currency) provided a reduction of 40% in amputations was obtained. Management of the diabetic foot according to guideline-based care improves survival, reduces diabetic foot complications, is cost-effective, and even cost-saving compared with usual care. Thus, policy makers and clinicians working in the field of diabetic foot management should see the cost of guidelines implementation as an attractive option. The effect of a staged management diabetic foot program has been retrospectively evaluated in a sample of 169 patients from a public hospital system.27 In this study, 454 patients received regular foot care visits; patient education and footwear were compared with 169 patients receiving none of these services. During a 12-month period, the diabetic foot care approach cohort had fewer hospitalizations, amputations, and emergency department visits for foot-related problems; outpatient visits increased. These improvements in outcomes translated into differences in charges between the two groups of $4776 vs $5411 per patient, with a savings of $635 per patient with access to a foot and ankle specialist. Studies evaluating the costeffectiveness of interventions for the management of diabetic foot patients are summarized in Table II. Matricali et al28 conducted a recent systematic review on the health economics of diabetic foot care in the context of a multidisciplinary setting. They found that the team approach seems to be cost-effective, with the greatest benefits expected over the long-term. The authors recommended that policy makers should be particularly focused on reimbursement for preventive and early intervention, as well as for limb salvage procedures. CONCLUSIONS Extensive patient education, early assessment, and aggressive treatment by a multidisciplinary team represent the best approach to manage high-risk patients with diabetes. Clinical and economic outcomes demonstrate reduced amputations, length of stay, and costs. The team must continue to become more effective, especially regarding early cost-effective use of appropriate care, interventions, and appropriate consultations to specialized teams. Early recognition and prevention of diabetic foot disease has been
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Table II. Synopsis of cost-effectiveness studies on interventions for diabetic foot ulcers First author Ollendorf, 1998
Study type
Study population
Model of hypothetical 10,000 subjects cohort to estimate incidence and cost of DFU
Ragnarson Markov model Tennvall, Theoretic cohorts 2001 Ortegon, 2004
Risk-based Markov model Theoretical cohorts
Horswel, 2003
Retrospective cohort
10,000 Swedish persons per model simulation Age: ⬎24 y 5-year period 10,000 US subjects with diabetes per model simulation, followed-up for the entire life 1999 currency 169 subjects 12-month period
Results Potential savings: 1. Educational intervention: $1.1 million 2. Multidisciplinary approach: $750,000 3. Therapeutic footwear: $850,000
Notes Estimated % amputation reduction: 1. Educational intervention: 72% 2. Multidisciplinary approach: 47% 3. Therapeutic footwear: 53%
Potential savings: Lower costs and highest QALYs only for at-risk patients, provided a 25% reduction in amputations is achieved Cost per QALY gained Considered to be attractive 1. Intensive glycemic control: $32,057 from a policy maker 2. Guidelines implementation: $12,169 prospective: $25,000 per to $220,100 depending on ulcer QALY attained reduction 1 ⫹ 2: ⬍$25,000 Savings per patient followed in a specialized foot clinic: $635 in 1 year
DFU, Diabetic foot ulcer; QALY, quality-adjusted life year.
greatly emphasized and proven to be effective in the United States; however, limb preservation services are frequently consulted very late in the disease process, after significant pathology has progressed. It is quite clear that by using an interdisciplinary team, we can improve function and reduce amputation, but what are the costs? Future clinical research might incorporate specific evidenced-based pathways to reduce amputation while choosing the most cost-effective diagnostic and treatment options. The next step is to break down silos of care between the various care settings, to improve the continuum of care while realizing more productive and costeffective methods for saving limbs, and caring for our high-risk population. REFERENCES 1. Davis WA, Norman PE, Bruce DG, Davis TM. Predictors, consequences and costs of diabetes-related lower extremity amputation complicating type 2 diabetes: the Fremantle Diabetes Study. Diabetologia 2006;49:2634-41. 2. Centers For Disease Control and Prevention (CDC) diabetes factsheet. At http://apps.nccd.cdc.gov/DDTSTRS/default.aspx. 3. American Diabetes Association (ADA). Economic costs of diabetes in the U.S. 2007. Diabetes Care 2008;31:596-615. 4. Connor H. Some historical aspects of diabetic foot disease. Diabetes Metab Res Rev 2008;24(Suppl 1):S7-13. 5. Pecoraro RE, Reiber GE, Burgess EM. Pathways to diabetic limb amputation. Basis for prevention. Diabetes Care 1990;13:513-21. 6. Holzer SE, Camerota A, Martens L, Cuerdon T, Crystal-Peters J, Zagari M. Costs and duration of care for lower extremity ulcers in patients with diabetes. Clin Ther 1998;20:169-81. 7. Harrington C, Zagari MJ, Corea J, Klitenic J. A cost analysis of diabetic lower-extremity ulcers. Diabetes Care 2000;23:1333-8. 8. Ramsey SD, Newton K, Blough D, McCulloch DK, Sandhu N, Reiber GE, et al. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 1999;22:382-7. 9. Apelqvist J, Ragnarson-Tennvall G, Persson U, Larsson J. Diabetic foot ulcers in a multidisciplinary setting. An economic analysis of primary healing and healing with amputation. J Intern Med 1994;235:463-71.
10. Apelqvist J, Ragnarson-Tennvall G, Larsson J, Persson U. Long-term costs for foot ulcers in diabetic patients in a multidisciplinary setting. Foot Ankle Int 1995;16:388-94. 11. Stockl K, Vanderplas A, Tafesse E, Chang E. Costs of lower-extremity ulcers among patients with diabetes. Diabetes Care 2004;27:2129-34. 12. Reiber GE, Boyko EJ, Smith DG. Lower extremity foot ulcers and amputations in diabetes. In: Harris M, editor. Diabetes in America. 2nd ed. Bethesda: National Institutes of Health; 1995. p. 409-28. 13. Eslami MH, Zayaruzny M, Fitzgerald GA. The adverse effects of race, insurance status, and low income on the rate of amputation in patients presenting with lower extremity ischemia. J Vasc Surg 2007;45:55-9. 14. LoGerfo FW, Gibbons GW, Pomposelli FB Jr, Campbell DR, Miller A, Freeman DV, et al. Trends in the care of the diabetic foot. Expanded role of arterial reconstruction. Arch Surg 1992;127:617-20. 15. Gibbons GW, Marcaccio EJ Jr, Burgess AM, Pomposelli FB Jr, Freeman DV, Campbell DR, et al. Improved quality of diabetic foot care, 1984 vs 1990. Reduced length of stay and costs, insufficient reimbursement. Arch Surg 1993;128:576-81. 16. Faglia E, Mantero M, Caminiti M, Caravaggi C, De Giglio R, Pritelli C, et al. Extensive use of peripheral angioplasty, particularly infrapopliteal, in the treatment of ischaemic diabetic foot ulcers: clinical results of a multicentric study of 221 consecutive diabetic subjects. J Intern Med 2002;252:225-32. 17. Zayed H, Halawa M, Maillardet L, Sidhu PS, Edmonds M, Rashid H. Improving limb salvage rate in diabetic patients with critical leg ischemia using a multidisciplinary approach. Int J Clin Pract 2009;63: 855-8. 18. Larsson J, Apelqvist J, Agardh CD, Stenström A. Decreasing incidence of major amputation in diabetic patients: a consequence of a multidisciplinary foot care team approach? Diabet Med 1995;12:770-6. 19. Van Gils CC, Wheeler LA, Mellstrom M, Brinton EA, Mason S, Wheeler CG. Amputation prevention by vascular surgery and podiatry collaboration in high-risk diabetic and nondiabetic patients. The Operation Desert Foot experience. Diabetes Care 1999;22:678-83. 20. 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 2005;28:248-53. 21. Driver VR, Goodman RA, Fabbi M, French MA, Andersen CA. The impact of a podiatric lead limb preservation team on disease outcomes and risk prediction in the diabetic lower extremity: a retrospective cohort study. J Am Podiatr Med Assoc 2010;100:235-41. 22. Krishnan S, Nash F, Baker N, Fowler D, Rayman G. Reduction in diabetic amputations over 11 years in a defined U.K. population:
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benefits of multidisciplinary team work and continuous prospective audit. Diabetes Care 2008;31:99-101. 23. Anichini R, Zecchini F, Cerretini I, Meucci G, Fusilli D, Alviggi L, 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 2007;75: 153-8. 24. Ragnarson Tennvall G, Apelqvist J. Prevention of diabetes-related foot ulcers and amputations: a cost-utility analysis based on Markov model simulations. Diabetologia 2001;44:2077-87. 25. Ollendorf DA, Kotsanos JG, Wishner WJ, Friedman M, Cooper T, Bittoni M, et al. Potential economic benefits of lower-extremity
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amputation prevention strategies in diabetes. Diabetes Care 1998;21:1240-5. 26. Ortegon MM, Redekop WK, Niessen LW. Cost-effectiveness of prevention and treatment of the diabetic foot: a Markov analysis. Diabetes Care 2004;27:901-7. 27. Horswell RL, Birke JA, Patout CA Jr. A staged management diabetes foot program versus standard care: a 1-year cost and utilization comparison in a state public hospital system. Arch Phys Med Rehabil 2003;84:1743-6. 28. Matricali GA, Dereymaeker G, Muls E, Flour M, Mathieu C. Economic aspects of diabetic foot care in a multidisciplinary setting: a review. Diabetes Metab Res Rev 2007;23:339-47.
Limb preservation team services have been shown to reduce major limb amputation, but the associated costs are not well understood or reported. Perhaps this is true because the burden of preventing amputations is often realized at a critical health care event, such as limb-threatening infection or acute critical limb ischemia. In many cases, these diabetic patients are at very high risk for limb loss, newly consulted for their acute event, and, therefore, in their highest health-related cost status. An adequate and comprehensive cost-effectiveness analysis must consider health states with limb-preserving impact figures and their relative cost, as it relates to severity of disease and prevention of amputations. Lower extremity amputations contribute disproportionately to diabetes-related costs.1 From the Department of Surgery, Boston University School of Medicine and Boston Medical Center;a and the Department of Surgery, Scott and White Hospital.b Competition of interest: none. This article is being co-published in the Journal of Vascular Surgery® and the Journal of the American Podiatric Medical Association. Correspondence: Lawrence A. Lavery, Scott and White Hospital, Department of Surgery, 703 Highland Spring Ln, Georgetown, TX 78628 (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest. 0741-5214/$36.00 Copyright © 2010 by the Society for Vascular Surgery and the American Podiatric Medical Association. doi:10.1016/j.jvs.2010.06.003
MAGNITUDE OF THE PROBLEM According to the Centers for Disease Control and Prevention, 7.8% of the United States population had diabetes in 2007, which equals almost 24 million persons.2 In 2007, diabetes and its complications cost the United States $174 billion; $116 billion were in direct costs and $58.3 billion in indirect costs such as loss of productivity, disability, and premature mortality.3 Peripheral vascular complications and neurologic complications, which are closely linked to foot ulceration, accounted for 31% and 24% of the expenses, respectively, and were among the major contributors to inpatient length of stay. Foot problems in persons with diabetes have been recognized as a major health issue since the times of Joslin and before the advent of insulin. The diabetic foot with gangrene was one of the leading causes of death from diabetes, second only to diabetic coma.4 The rate of hospital discharges for diabetic patients with leg/foot ulcers for 1000 diabetic patients rose from 5.4 in 1980 to 6.9 in 2003.2 Ulcer prevalence among persons aged ⬍44 years was 6.5/1000 diabetics and it rose progressively to 10.3/ 1000 diabetics in individuals aged ⬎75 years. Hospitalizations for lower extremity amputations rose from 33,000 in 1980 to 71,000 in 2005; however, average length of stay fell from 35.3 to 10.7 days during the same period. More than 60% of nontraumatic lower limb amputations occur in diabetic individuals, and at least 80% of amputations are preceded by an ulcer. The causative path17S
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way leading from a foot ulcer to amputation is well known. The progressive additive effects of neuropathy, minor trauma, ulceration, faulty healing, ischemia, and infection leading to amputation were first characterized in 1990.5 Early recognition of foot problems and effective intervention along the causative pathways may not only improve outcomes by reducing major amputations and increasing quality of life, but also reduce costs related to diabetic foot complications. Studies on diabetic foot-related health care costs are sometimes difficult to compare due to dissimilar health care systems, reimbursement methods, and access to care. THE COSTS OF DIABETIC FOOT The cost of care for diabetic patients with a lower extremity ulcer is a major economic burden compared with the management of a patient with diabetes but no ulceration. Economic factors will play an ever-increasing role because third-party payers cannot reimburse all therapies used to treat chronic ulcerations. A retrospective analysis of insurance claims from a large population of private employer-sponsored insurance enrollees during the period 1991 to 1992,6 analyzed 3013 patients aged 18 to 64 years who had 3524 ulcer episodes. They were divided into three severity-level categories according to Wagner classification: grade 1 or 2, grade 3, and grade 4 or 5. The average cost for an ulcer episode was $4595. This study showed incremental resource utilization in patients with diabetic foot ulcers progressing from Wagner grade 1 to 2 to the highest grades. Wagner grade 1 or 2 ulcer costs averaged $1929, whereas Wagner grade 3 and grade 4 or 5 ulcer costs averaged $3980 and $15,792, respectively. Inpatient expenditures accounted for 80% of the total costs. Poor vascular status was also strongly associated with longer in-hospital stays and higher average total payments. An analysis of Medicare claims data from 1995 to 1996 showed that expenditures for diabetic foot patients were three times higher than for the general population ($15,309 vs $5226), yielding a total cost for Medicare in 1995 of $1.5 billion.7 Lower extremity ulcers accounted for 24% of the overall cost for diabetic population with an ulcer. Inpatient stays accounted for 73% of increased cost.7 A retrospective nested case-control study demonstrated that the relative cost of care for diabetic patients with lower extremity ulcers ranges from 1.5 to 2.4 times higher than that of diabetic patients without an ulcer in the year before diagnosis to 5.4 times higher in the year after the ulcer episode.8 The cost of care for diabetic patients with an ulcer showed a tendency to return to the non-ulcer group only after 2 years from the first diagnosis, but was still 2.8 times higher. Excess cost was $26,490 in ulcer patients during the year of the ulcer episode and $4927 for diabetic patients without an ulcer. The excess cost persisted during the second year after the ulcer episode. The costs for diabetic foot ulcer patients were $17,245 compared with $5110 for patients with diabetes but no ulcer. Patients with diabetes and a lower extremity ulcer had more inpatient days than
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diabetic patients without ulcers (6.03 vs 1.46 days), and this difference was still significant 1 year after the ulcer episode (4.06 vs 2.61). Diabetic patients with a foot ulcer during the first year of the study also had more emergency department visits (0.42 vs 0.18) and more nonemergency outpatient visits (35.08 vs 13.05).8 Apelqvist et al9 prospectively monitored 314 patients with an ulcer episode. They documented that 54% of patients healed in 2 months, 19% healed in 3 to 4 months, and 27% healed in ⱖ5 months. Healing without amputation averaged $6664, whereas healing by amputation averaged $44,790. Hospitalization costs and topical treatment of ulcers accounted for most of the costs. For patients that healed without amputation, 37% and 45% of the total costs were for hospitalizations and ulcer treatments, and for patients that healed with amputations, 65% of total costs were for hospitalizations and 13% for ulcer treatments. The same group estimated that the long-term costs of diabetic foot ulcers remain elevated during the first 3 years after healing of an ulcer.10 A retrospective study of diabetic patients with lower extremity ulcers revealed an average cost per ulcer episode of $13,179. Again, there was an increase in cost according to ulcer depth as evaluated by the Wagner classification system. Costs associated with a Wagner grade 1 ulcer averaged $1892, and Wagner grade 4/5 ulcers averaged $27,721. This study confirmed the high impact of inpatient stay as being 77% of the overall cost. Progression from Wagner ulcers with lower grades to higher grades carried an additional increase in cost of $20,136.11 This study also confirmed a higher cost per ulcer episode in patients with poor vascular status. Patients with a diabetic foot ulcer have an average hospital length of stay that can be 50% higher than that of patients without an ulcer.12 A synopsis of the studies evaluating the costs of diabetic foot is reported in Table I. Higher grade lesions and peripheral arterial disease not only lead to higher amputation rates but are also associated with higher costs of care mainly due to higher hospitalization rates and longer length of stay. Once an ulcer is present, higher costs are projected over a period of 2 to 3 years compared with patients without foot ulcers. Socioeconomic factors and reduced or absent insurance coverage can be very important and may thwart access to limb-preserving procedures. A study of a large cohort of individuals from 1998 to 2002 showed that nonwhite, low-income, Medicare and Medicaid patients were more likely to undergo an amputation for leg ischemia and to have less access to limb salvage procedures (eg, revascularization) compared with higher income individuals with private insurances.13 This may be explained by a delay in diagnosis of critical leg ischemia and limited access to care involving both primary care and vascular surgeries. THE LIMB SALVAGE TEAM It has long been recognized that the complex nature of diabetic foot pathology is best treated with a team approach. The group from New England Deaconess Hospital
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Table I. Synopsis of studies evaluating the direct cost of diabetic foot patients First author
Study type
Study population
Holzer, 1998
Retrospective analysis of private insurance claims
3013 subjects Study period: 1991-1992 Age: 18-64 y 3524 ulcer episodes
Harrington, 2000
Retrospective analysis of Medicare claims
⬎400,000 Medicare beneficiaries with DFUs Study period: 1995-1996
Ramsey, 1999
Retrospective casecontrol study in HMO
Apelqvist, 1994
Prospective study
8905 subjects Study period: 1992-1995 Age ⬎18 y 541 foot ulcers 314 subjects with DFU Subjects followed-up through their ulcer episode
Stockl, 2004
Retrospective claims data analysis
2253 subjects Study period: 2000-2001
Results
Notes
Average ulcer episode cost: $4595 1. Primary healing: $1929 2. Healing by amputation: $44,790 Grade 1 or 2 ulcers cost: $1929 Grade 3 ulcers cost: $3980 Grade 4 or 5 ulcers cost: $15,792 Aggregate disease attributable cost: $1.45 billion Average ulcer-related cost/ year: $3609 Medicare spending among ulcer patients/y: $15,309 All Medicare spending among all Medicare patients/y: $5266 Average cost of ulcer episode over 1 year: $26,490 Total attributable cost of DFU: $27,987a Average ulcer episode cost: 1. Primary healing: $6664 2. Healing by amputation: $44,790 Average ulcer episode cost: $13,179 Grade 1 ulcers: $1892 Grade 2 ulcers: $4345 Grade 3 ulcers: $12,255 Grade 4 or 5 ulcers: $27,721
Severity grading according to Wagner classification as 1 or 2; 3; 4 or 5
Excess cost for ulcer patients: 73.7% inpatient 10.9% outpatient 11.4% home health 4.0% SNF/hospice
Ulcer patients had more inpatient days and more emergency department visits over the study period Cost for ulcer patients: 61% inpatient 39% outpatient Severity grading according to Wagner classification as 1; 2; 3; 4 or 5 77% inpatient cost
DFU, Diabetic foot ulcer; HMO, health maintenance organization; SNF, skilled nurse facility. a Attributable cost of DFU has been calculated as the difference between average expenditures for DFU patients over the first and second years after diagnosis and the expenditures the year before DFU diagnosis.
and Joslin Diabetes Clinic in Boston, Massachusetts, is regarded as a forerunner of this approach. In 1992, LoGerfo et al14 published the results of aggressive use of distal bypass grafting revascularization in diabetic patients with ischemic ulcers. They showed a progressive increase in the bypass/amputation ratio comparing outcomes of patients from 1984 to 1990. A retrospective evaluation was reported of two groups of patients followed-up before and after implementing diabetic foot care with a team approach that focused on aggressive early intervention and extensive use of surgical revascularization. LoGerfo et al15 showed a reduction in major amputations, overall length of stay, and total cost of care. The authors, however, pointed out that Medicare reimbursement was inadequate to cover all the procedures. The widespread use of endovascular revascularization techniques has further broadened the spectrum of revascularization options for diabetic patients with critical leg ischemia. A prospective study of peripheral angioplasty at both proximal and distal levels showed an excellent limb salvage rate, with only 10 of 191 patients (5.2%) undergoing a major amputation.16 Whether an open surgical or an
endovascular procedure should be the first-line treatment for diabetic patients with critical leg ischemia is still a matter of debate and so is which of these two procedures might represent the most cost-effective treatment. Regardless of the procedure type, aggressive and effective revascularization is crucial in limb salvage, particularly in amputation reduction, an important driver of cost. Many studies have now shown that a team approach to diabetic foot conditions is effective in amputation prevention. Zayed et al17 reported results of a retrospective analysis of 312 patients with diabetes and critical leg ischemia and demonstrated a reduction in amputation rate in a multidisciplinary setting. The team was composed of a vascular and podiatric surgeon, diabetologist, tissue viability nurse, interventional radiologist, and a radiology coordinator. A retrospective study from Sweden18 showed a 78% decrease in major amputations after the implementation of a multidisciplinary program for the management of diabetic foot patients. A prospective study of a United States population showed that podiatry-vascular surgery collaboration resulted in 83% limb salvage at 5 years.19
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Likewise, Driver et al20,21 reported the outcomes of a multidisciplinary team to prevent amputations reduction. During a 4-year period, there was an 82% reduction in major amputations. A prospective study from the United Kingdom showed a 62% reduction in major amputations and a 40% decrease in all amputations during an 11-year period after a diabetic foot care service was started.22 Implementation of existing guidelines is likely to lower amputation rates. Results from a prospective study at a specialized diabetic foot clinic in Italy showed that implementing the International Consensus on the Diabetic Foot recommendations resulted in a decrease in major amputations from 10.7 per 100,000 inhabitants at the beginning of the study to 6.24 per 100,000 inhabitants after 5 years. This decrease was paired with a progressive increase in minor amputations.23 The authors also documented a progressive extensive referral to the diabetic foot service during the study period. This aspect is of particular interest because it shows that improving provider education about diabetic foot disease may also improve more appropriate referral patterns. COST EFFECTIVENESS OF INTERVENTIONS Few studies have addressed the economic benefits of interventions for the prevention and treatment of diabetic foot disease. Most studies explore results from predictive models, with the most common being the Markov model. This can be a useful mathematic tool for obtaining a projection of cost and effects of an intervention. This method for modeling disease, such as diabetic foot ulcers, is relevant because it can take into account both the chronicity of the disease and the occurrence of the same events more than once.24 However, data from these studies are difficult to compare due to differences in demographics and health care systems. A model to evaluate the effects of different types of interventions on economic outcomes in a theoretic cohort of 10,000 diabetic patients25 showed that prevention and appropriate management of diabetic foot patients might avoid up to 50% of amputations. The authors estimated that educational intervention, a multidisciplinary team approach, and therapeutic footwear coverage could avoid 72%, 47%, and 53% of amputations, respectively. This translates to $1,100,000, $750,000, and $850,000 in potential savings over 1 year for each intervention. The authors concluded that prevention, a multidisciplinary team approach, and therapeutic footwear could save from $2,900 to $4,442 in per patient costs. These United States data strongly indicate a cost-savings from the initiation of preventive strategies in the management of diabetic foot patients in concert with a multidisciplinary team approach. Apelqvist et al24 analyzed 5 years of cost-utility data from preventive interventions on patients with diabetic foot ulcers. The study focused on implementation of guidelines from the International Working Group on Diabetic Foot (IWGDF) and sought to demonstrate that the costs of implementing a preventive system would be offset by the benefits of amputation prevention.24 This study showed
that an intensive prevention strategy composed of patient education, foot care, and therapeutic footwear is costeffective in a Swedish population, if the risk of foot ulcers and amputations can be reduced by 25%. Another European study used a Markov model to assess the potential economic effects of two interventions in patients with diabetic foot ulcers: intensive glycemic control and optimal foot care as defined by IWGDF guidelines, taken singularly or coupled vs standard of care without guidelines implementation.26 The study showed that the greatest reduction in amputation would have been achieved with the combination of the two interventions. The most favorable cost-effectiveness ratio was strongly linked to ulcer prevention. The increased costs for guideline implementation were associated with less than $25,000 per quality-adjusted life-years gained (1999 currency) provided a reduction of 40% in amputations was obtained. Management of the diabetic foot according to guideline-based care improves survival, reduces diabetic foot complications, is cost-effective, and even cost-saving compared with usual care. Thus, policy makers and clinicians working in the field of diabetic foot management should see the cost of guidelines implementation as an attractive option. The effect of a staged management diabetic foot program has been retrospectively evaluated in a sample of 169 patients from a public hospital system.27 In this study, 454 patients received regular foot care visits; patient education and footwear were compared with 169 patients receiving none of these services. During a 12-month period, the diabetic foot care approach cohort had fewer hospitalizations, amputations, and emergency department visits for foot-related problems; outpatient visits increased. These improvements in outcomes translated into differences in charges between the two groups of $4776 vs $5411 per patient, with a savings of $635 per patient with access to a foot and ankle specialist. Studies evaluating the costeffectiveness of interventions for the management of diabetic foot patients are summarized in Table II. Matricali et al28 conducted a recent systematic review on the health economics of diabetic foot care in the context of a multidisciplinary setting. They found that the team approach seems to be cost-effective, with the greatest benefits expected over the long-term. The authors recommended that policy makers should be particularly focused on reimbursement for preventive and early intervention, as well as for limb salvage procedures. CONCLUSIONS Extensive patient education, early assessment, and aggressive treatment by a multidisciplinary team represent the best approach to manage high-risk patients with diabetes. Clinical and economic outcomes demonstrate reduced amputations, length of stay, and costs. The team must continue to become more effective, especially regarding early cost-effective use of appropriate care, interventions, and appropriate consultations to specialized teams. Early recognition and prevention of diabetic foot disease has been
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Table II. Synopsis of cost-effectiveness studies on interventions for diabetic foot ulcers First author Ollendorf, 1998
Study type
Study population
Model of hypothetical 10,000 subjects cohort to estimate incidence and cost of DFU
Ragnarson Markov model Tennvall, Theoretic cohorts 2001 Ortegon, 2004
Risk-based Markov model Theoretical cohorts
Horswel, 2003
Retrospective cohort
10,000 Swedish persons per model simulation Age: ⬎24 y 5-year period 10,000 US subjects with diabetes per model simulation, followed-up for the entire life 1999 currency 169 subjects 12-month period
Results Potential savings: 1. Educational intervention: $1.1 million 2. Multidisciplinary approach: $750,000 3. Therapeutic footwear: $850,000
Notes Estimated % amputation reduction: 1. Educational intervention: 72% 2. Multidisciplinary approach: 47% 3. Therapeutic footwear: 53%
Potential savings: Lower costs and highest QALYs only for at-risk patients, provided a 25% reduction in amputations is achieved Cost per QALY gained Considered to be attractive 1. Intensive glycemic control: $32,057 from a policy maker 2. Guidelines implementation: $12,169 prospective: $25,000 per to $220,100 depending on ulcer QALY attained reduction 1 ⫹ 2: ⬍$25,000 Savings per patient followed in a specialized foot clinic: $635 in 1 year
DFU, Diabetic foot ulcer; QALY, quality-adjusted life year.
greatly emphasized and proven to be effective in the United States; however, limb preservation services are frequently consulted very late in the disease process, after significant pathology has progressed. It is quite clear that by using an interdisciplinary team, we can improve function and reduce amputation, but what are the costs? Future clinical research might incorporate specific evidenced-based pathways to reduce amputation while choosing the most cost-effective diagnostic and treatment options. The next step is to break down silos of care between the various care settings, to improve the continuum of care while realizing more productive and costeffective methods for saving limbs, and caring for our high-risk population. REFERENCES 1. Davis WA, Norman PE, Bruce DG, Davis TM. Predictors, consequences and costs of diabetes-related lower extremity amputation complicating type 2 diabetes: the Fremantle Diabetes Study. Diabetologia 2006;49:2634-41. 2. Centers For Disease Control and Prevention (CDC) diabetes factsheet. At http://apps.nccd.cdc.gov/DDTSTRS/default.aspx. 3. American Diabetes Association (ADA). Economic costs of diabetes in the U.S. 2007. Diabetes Care 2008;31:596-615. 4. Connor H. Some historical aspects of diabetic foot disease. Diabetes Metab Res Rev 2008;24(Suppl 1):S7-13. 5. Pecoraro RE, Reiber GE, Burgess EM. Pathways to diabetic limb amputation. Basis for prevention. Diabetes Care 1990;13:513-21. 6. Holzer SE, Camerota A, Martens L, Cuerdon T, Crystal-Peters J, Zagari M. Costs and duration of care for lower extremity ulcers in patients with diabetes. Clin Ther 1998;20:169-81. 7. Harrington C, Zagari MJ, Corea J, Klitenic J. A cost analysis of diabetic lower-extremity ulcers. Diabetes Care 2000;23:1333-8. 8. Ramsey SD, Newton K, Blough D, McCulloch DK, Sandhu N, Reiber GE, et al. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 1999;22:382-7. 9. Apelqvist J, Ragnarson-Tennvall G, Persson U, Larsson J. Diabetic foot ulcers in a multidisciplinary setting. An economic analysis of primary healing and healing with amputation. J Intern Med 1994;235:463-71.
10. Apelqvist J, Ragnarson-Tennvall G, Larsson J, Persson U. Long-term costs for foot ulcers in diabetic patients in a multidisciplinary setting. Foot Ankle Int 1995;16:388-94. 11. Stockl K, Vanderplas A, Tafesse E, Chang E. Costs of lower-extremity ulcers among patients with diabetes. Diabetes Care 2004;27:2129-34. 12. Reiber GE, Boyko EJ, Smith DG. Lower extremity foot ulcers and amputations in diabetes. In: Harris M, editor. Diabetes in America. 2nd ed. Bethesda: National Institutes of Health; 1995. p. 409-28. 13. Eslami MH, Zayaruzny M, Fitzgerald GA. The adverse effects of race, insurance status, and low income on the rate of amputation in patients presenting with lower extremity ischemia. J Vasc Surg 2007;45:55-9. 14. LoGerfo FW, Gibbons GW, Pomposelli FB Jr, Campbell DR, Miller A, Freeman DV, et al. Trends in the care of the diabetic foot. Expanded role of arterial reconstruction. Arch Surg 1992;127:617-20. 15. Gibbons GW, Marcaccio EJ Jr, Burgess AM, Pomposelli FB Jr, Freeman DV, Campbell DR, et al. Improved quality of diabetic foot care, 1984 vs 1990. Reduced length of stay and costs, insufficient reimbursement. Arch Surg 1993;128:576-81. 16. Faglia E, Mantero M, Caminiti M, Caravaggi C, De Giglio R, Pritelli C, et al. Extensive use of peripheral angioplasty, particularly infrapopliteal, in the treatment of ischaemic diabetic foot ulcers: clinical results of a multicentric study of 221 consecutive diabetic subjects. J Intern Med 2002;252:225-32. 17. Zayed H, Halawa M, Maillardet L, Sidhu PS, Edmonds M, Rashid H. Improving limb salvage rate in diabetic patients with critical leg ischemia using a multidisciplinary approach. Int J Clin Pract 2009;63: 855-8. 18. Larsson J, Apelqvist J, Agardh CD, Stenström A. Decreasing incidence of major amputation in diabetic patients: a consequence of a multidisciplinary foot care team approach? Diabet Med 1995;12:770-6. 19. Van Gils CC, Wheeler LA, Mellstrom M, Brinton EA, Mason S, Wheeler CG. Amputation prevention by vascular surgery and podiatry collaboration in high-risk diabetic and nondiabetic patients. The Operation Desert Foot experience. Diabetes Care 1999;22:678-83. 20. 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 2005;28:248-53. 21. Driver VR, Goodman RA, Fabbi M, French MA, Andersen CA. The impact of a podiatric lead limb preservation team on disease outcomes and risk prediction in the diabetic lower extremity: a retrospective cohort study. J Am Podiatr Med Assoc 2010;100:235-41. 22. Krishnan S, Nash F, Baker N, Fowler D, Rayman G. Reduction in diabetic amputations over 11 years in a defined U.K. population:
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benefits of multidisciplinary team work and continuous prospective audit. Diabetes Care 2008;31:99-101. 23. Anichini R, Zecchini F, Cerretini I, Meucci G, Fusilli D, Alviggi L, 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 2007;75: 153-8. 24. Ragnarson Tennvall G, Apelqvist J. Prevention of diabetes-related foot ulcers and amputations: a cost-utility analysis based on Markov model simulations. Diabetologia 2001;44:2077-87. 25. Ollendorf DA, Kotsanos JG, Wishner WJ, Friedman M, Cooper T, Bittoni M, et al. Potential economic benefits of lower-extremity
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amputation prevention strategies in diabetes. Diabetes Care 1998;21:1240-5. 26. Ortegon MM, Redekop WK, Niessen LW. Cost-effectiveness of prevention and treatment of the diabetic foot: a Markov analysis. Diabetes Care 2004;27:901-7. 27. Horswell RL, Birke JA, Patout CA Jr. A staged management diabetes foot program versus standard care: a 1-year cost and utilization comparison in a state public hospital system. Arch Phys Med Rehabil 2003;84:1743-6. 28. Matricali GA, Dereymaeker G, Muls E, Flour M, Mathieu C. Economic aspects of diabetic foot care in a multidisciplinary setting: a review. Diabetes Metab Res Rev 2007;23:339-47.