Diabetes Care
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Diabetes Care 29:1288-1293, 2006
DOI: 10.2337/dc05-2425
© 2006 by the American Diabetes Association
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow patientINFORMation
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lavery, L. A.
Right arrow Articles by Lipsky, B. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lavery, L. A.
Right arrow Articles by Lipsky, B. A.
Social Bookmarking
Add to CiteULike   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

Pathophysiology/Complications
Original Article

Risk Factors for Foot Infections in Individuals With Diabetes

Lawrence A. Lavery, DPM, MPH1, David G. Armstrong, DPM2,3, Robert P. Wunderlich, DPM4, M. Jane Mohler, PHD5,6, Christopher S. Wendel, MS5 and Benjamin A. Lipsky, MD7

1 Department of Surgery, Scott and White Hospital, Texas A&M University Health Science Center College of Medicine, Temple, Texas
2 Dr. William M. Scholl College of Podiatric Medicine, Rosalind Franklin University of Medicine and Science, Chicago, Illinois
3 Department of Medicine, Manchester Royal Infirmary, Manchester, U.K.
4 Department of Medicine, Diabetex, San Antonio, Texas
5 Research Service, Southern Arizona Veterans Affairs Medical Center, Tucson, Arizona
6 Epidemiology and Biostatistics Division, College of Public Health, University of Arizona, Tucson, Arizona
7 Department of Medicine, University of Washington and the VA Puget Sound Heath Care System, Seattle, Washington

Address correspondence and reprint requests to Lawrence A. Lavery, Professor, Department of Surgery, Scott and White Hospital, 703 Highland Spring Ln., Georgetown, TX 78628. E-mail: llavery{at}swmail.sw.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
OBJECTIVE—To prospectively determine risk factors for foot infection in a cohort of people with diabetes.

RESEARCH DESIGN AND METHODS—We evaluated then followed 1,666 consecutive diabetic patients enrolled in a managed care–based outpatient clinic in a 2-year longitudinal outcomes study. At enrollment, patients underwent a standardized general medical examination and detailed foot assessment and were educated about proper foot care. They were then rescreened at scheduled intervals and also seen promptly if they developed any foot problem.

RESULTS—During the evaluation period, 151 (9.1%) patients developed 199 foot infections, all but one involving a wound or penetrating injury. Most patients had infections involving only the soft tissue, but 19.9% had bone culture–proven osteomyelitis. For those who developed a foot infection, compared with those who did not, the risk of hospitalization was 55.7 times greater (95% CI 30.3–102.2; P < 0.001) and the risk of amputation was 154.5 times greater (58.5–468.5; P < 0.001). Foot wounds preceded all but one infection. Significant (P < 0.05) independent risk factors for foot infection from a multivariate analysis included wounds that penetrated to bone (odds ratio 6.7), wounds with a duration >30 days (4.7), recurrent wounds (2.4), wounds with a traumatic etiology (2.4), and presence of peripheral vascular disease (1.9).

CONCLUSIONS—Foot infections occur relatively frequently in individuals with diabetes, almost always follow trauma, and dramatically increase the risk of hospitalization and amputation. Efforts to prevent infections should be targeted at people with traumatic foot wounds, especially those that are chronic, deep, recurrent, or associated with peripheral vascular disease.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
Foot wounds are now the most common diabetes-related cause of hospitalization and are a frequent precursor to amputation (1–3). Individuals with diabetes have a 30-fold higher lifetime risk of undergoing a lower-extremity amputation compared with those without diabetes (4,5). An infected foot wound precedes about two-thirds of lower-extremity amputations (6,7), and infection is surpassed only by gangrene as an indication for diabetic lower-extremity amputation (8). Individuals with diabetes have at least a 10-fold greater risk of being hospitalized for soft tissue and bone infections of the foot (9) than individuals without diabetes.

While several retrospective studies address the epidemiology of foot infection in people with diabetes, there are no prospective data addressing this problem. Clinicians, health care organizations, and insurance and funding agencies would benefit from knowing the true incidence, the most common types, the clinical and demographic predisposing risk factors, and the outcomes of these infections. This information could help to predict which patients are at highest risk for diabetic foot infections, thereby helping to plan optimally targeted preventative strategies. We therefore conducted a prospective study of the epidemiology of foot infections, as part of a diabetes disease management program.


   RESEARCH DESIGN AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
RESULTS
 CONCLUSIONS
 References
 
This report includes data from a cohort of the first 1,666 patients enrolled in a program designed to prevent and treat foot complications in diabetic patients (Fig. 1). The methods used in this analysis have been previously published (10). The disease management program was conducted in cooperation with two large primary care physician groups in south Texas. The patients all participated in a commercial HMO insurance plan or a Medicare replacement HMO insurance program. In the 1st year of the program, we identified people with diabetes (ICD-9-CM code of 250) from inpatient and outpatient administrative databases and confirmed the diagnosis by review of medical, laboratory, and pharmacy records. Of those identified, 74% participated in the screening and risk assessment program and were followed in a diabetic foot clinic. This clinic generally served as the patients’ only source for diabetic foot care and for consultations for lower-extremity complications from specialists in vascular surgery or infectious diseases.


Figure 1
View larger version (15K):
[in this window]
[in a new window]
  		Figure 1— Flow chart for patients enrolled in the study.

 
All patients (and any interested family members) were educated on basic diabetes and foot care principles in small group sessions when they were enrolled into the program. Patients were then screened for risk factors known to be associated with lower-extremity complications (11) (e.g., peripheral neuropathy, foot wounds, peripheral vascular disease, Charcot arthropathy, or previous foot surgical procedures). A staff podiatrist and nurse evaluated each patient’s feet using a defined protocol. We diagnosed peripheral sensory neuropathy by either a vibration perception threshold level of >25 volts (VPT Tester; Xilas Medical, San Antonio, TX) or the inability to accurately perceive pressure at one or more site(s) with the 10-g Semmes-Weinstein monofilament (Touch-Test Sensory Evaluator; North Coast Medical, Morgan Hill, CA) (12). We defined peripheral vascular insufficiency as the absence of arterial foot pulses (both dorsalis pedis and posterior tibial arterial pulse) and an ankle-to-arm systolic blood pressure ratio of <0.80 (13). We evaluated for limited joint mobility, hallux rigidus (<50° dorsiflexion of the first metatarsophalangeal joint), or ankle equinus (dorsiflexion of <0°) (14–18), and foot deformities, e.g., hallux valgus, hammer toes, or claw toes. We measured peak foot pressures on the sole of the foot with the EMED force-plate (Novel, Minneapolis, MN), using a two-step method (19–21).

We constructed a database to record the information obtained in the screening evaluation of the enrolled individuals and to track any foot-related clinical outcomes of interest. We used claims data to verify all hospital admissions and amputations. Based on the results of screening examinations, we stratified patients into risk groups using the International Diabetic Foot Classification System (22–24). Low-risk patients (category 0) were annually rescreened for foot problems. High-risk patients (categories 1, 2, or 3) were examined in the foot clinic at least every 12 weeks and, when needed, were fitted for therapeutic shoes and insoles by a certified pedorthist. Subjects in all risk groups were instructed to call for an appointment any time they had a concern about a foot problem.

During the follow-up period, two staff podiatrists (L.A.L., R.P.W.) evaluated and treated any patient who developed a foot complication. We defined a foot wound as a full skin thickness lesion involving any portion of the foot or ankle (25–27). Using a blunt sterile probe, we evaluated the depth of any wound to determine undermining and whether the wound penetrated to tendon, joint capsule, or bone. We also recorded the duration the wound had been present from the time the patient reported it had started until the wound was healed, the wound necessitated an amputation, or the evaluation period ended. We defined Charcot arthropathy as a foot fracture or dislocation occurring with little or no trauma, in the presence of sensory neuropathy but palpable pulses (28,29). We defined a foot infection by clinical criteria consistent with the International Working Group guidelines (23) (i.e., the presence of purulence or two or more other local signs of inflammation). We evaluated patients with an infection for the extent of soft tissue involved and for evidence of bone involvement (30–32). When bone infection was suspected, the patient underwent an appropriate evaluation; we only diagnosed osteomyelitis when there was a positive culture from a bone biopsy (surgical or percutaneous).

Statistical analyses
We compared differences in mean values for various à priori selected factors in patients who developed an infection and those who did not, using the {chi}2 test for categorical predictor variables and t tests for continuous variables. Using infection as the outcome variable, we calculated odds ratios (ORs) and 95% CIs by logistic regression. For categorical variables with more than two levels, such as wound depth or number of missing pulses, we chose one level as baseline and calculated ORs for other levels in comparison to baseline. After the univariate analysis, we used stepwise logistic regression analysis to model the effects of predictors and interactions while simultaneously controlling for potential confounding variables. We included predictors and interaction terms in a stepwise model based on statistical significance ({alpha} = 5%) in the univariate analysis or biological plausibility of an association.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
CONCLUSIONS
 References
 
Over an 8-month period, we enrolled 1,666 diabetic patients in the disease management program and followed this cohort for an average of 27.2 ± 14.2 months (range 3.9–32.0). During the study period, 151 patients (9.1%) developed 199 foot infections. Table 1 shows a comparison of demographic and clinical characteristics present at enrollment for the patients with a wound or penetrating injury who developed a foot infection and those who did not. The average duration of follow-up for subjects with foot wounds was 25.6 ± 11.5 months (median 30.4). Recurrent foot infections at the same or a different site occurred in 23.2% (35 of 151) of study patients; 24 patients had two, 9 had three, and 2 had four infections. Most infections involved only soft tissue, but 30 (19.9%) patients with foot infection had bone culture–proven osteomyelitis.


View this table:
[in this window]
[in a new window]
  		Table 1— Demographic and clinical characteristics at enrollment for patients with foot wounds or penetrating injuries who did and did not develop a foot infection*

 
Sustaining a lower-extremity wound was the most common precipitating event for a foot infection. All but one of the 151 patients who developed a foot infection had a preexisting lower-extremity wound or penetrating injury. The risk of developing an infection was 2,193 times greater in subject who developed a foot wound than in those without a wound (60.7 vs. 0.07% [95% CI 303.6–15,837.6]; P < 0.0001).

During the study period, 69 people were hospitalized for 85 separate lower-extremity–related events. Foot infection was a contributing factor for hospitalization in 71.7% (61 of 85) of these events. Among the patients with a lower-extremity infection, 64.2% (97 of 151) were treated in an outpatient setting, while the rest (35.8%) were admitted for at least one infection-related hospitalization. The risk of hospitalization was 55.7 times greater for people with diabetes who developed a foot infection than for those who did not (95% CI 30.3–102.2; P < 0.001). The risk of amputation was 154.5 times greater in patients with diabetes who had a lower-extremity infection than in those who did not (95% CI 58.5–468.5; P < 0.001).

Using a stepwise logistic regression model we found several factors were significant independent risks (Table 2). We excluded ulceration from the regression model because of its high degree of colinearity with infection. The dominant remaining independent risk factors were wounds that penetrated to bone (OR 6.7; P < 0.001), wound duration of >30 days (4.7; P < 0.004), a history of recurrent wounds during the study period (2.4; P < 0.006), wounds with a traumatic etiology (2.4; P < 0.02), and the presence of peripheral vascular disease (1.9; P < 0.04).


View this table:
[in this window]
[in a new window]
  		Table 2— Variables achieving independent statistical significance as risk factors for foot infection by multivariate analysis

 

   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
References
 
Our search of the literature uncovered no previously published prospective study of this common and important problem. To best define types of and risk factors for foot infections, we conducted a comprehensive prospective study among individuals with diabetes carefully followed in a health management program. This included enrolling consecutive patients in a large cohort study, having specialists examine them thoroughly at baseline, and tracking them carefully during a relatively long follow-up period. The patients received all of their foot care at the site of enrollment. Because the enrolled patients, especially those at high risk for foot wound, made frequent follow-up visits and had ready access to specialty foot care, we likely detected all clinically important infections. We may, however, have missed some mild, self-limited, or patient-treated infections.

The incidence of foot infections in these patients was surprisingly high. Despite being extensively educated, provided with therapeutic shoes and insoles when indicated, followed in a foot clinic, and having ready access to podiatric care, 9.1% of enrolled patients developed a foot infection during just over 2 years of follow-up. As reported in previous retrospective studies (33), infections most commonly involved only the soft tissue, but about one in five extended to the bone.

We identified several risk factors for developing a foot infection in these subjects with diabetes. Sustaining a foot wound was by far the most important antecedent to an infection. In fact, only one infection developed in the absence of a wound or penetrating injury. Since most soft tissue infections occur when pathogens penetrate into the subcutaneous tissue, the association of infection with foot wounds is not surprising. Most (60.9%) foot wounds were clinically infected at presentation, but a substantial minority was not. This is an important distinction, as uninfected foot wounds were not routinely treated with antimicrobial therapy.

By multivariate analysis, we found four statistically significant independent risk factors for foot infection: wounds that penetrated to bone, recurrent wounds, wounds of long duration (30 days), and peripheral vascular disease. It is not surprising that patients with multiple wounds, wounds of long duration, and deeper wounds had a higher risk of infection. Subjects with recurrent wounds during the study period would have had a more prolonged exposure to the primary risk for infection, i.e., a penetrating wound. It is not, therefore, surprising that deeper wounds are associated with slower healing (34,35).

The finding that peripheral vascular disease was associated with an approximately twofold increased risk of foot infection in the multivariate model was unexpected. Foot ischemia certainly appears to be associated with an increased severity of an infection (36). Diabetic patients often have a diminished inflammatory response to injury or infection (37–43); this deficit could be further impaired by ischemia. Diminished blood flow could result in a lack of erythema or induration, visual cues of infection. These deficits, especially in a patient with sensory neuropathy who also lacks the ability to sense pain or warmth, might delay awareness of an infection. In a previous case-control study (43) of patients with an infected puncture wound of the foot, we found that visual cues of inflammation, rather than the pain, were the most frequent presenting complaints in the people with diabetes. The interval from the puncture injury to surgery was also significantly longer in the diabetic individuals, suggesting that their lack of pain perception might delay recognition of a limb-threatening problem (44). The types of traumatic wounds in this study included burns, puncture wounds, blunt trauma, lacerations, and ingrown toenails. The finding that wounds associated with trauma had a high risk of infection may be caused by the fact that these wounds often penetrate to deep structures and inoculate them with bacteria at the time of injury. Traumatic wounds may also be associated with more tissue damage, making it more prone to necrosis and infection.

Risk factors for developing a foot ulcer have been defined in several retrospective and prospective studies (11,14,45–49) We found only one other epidemiological study, however, of foot infections in persons with diabetes. Peters et al. (50) reported a case-control study of 112 patients with diabetes, of whom 68 were hospitalized for a foot infection while the other 44 were hospitalized for other reasons. In this study, neuropathy, peripheral vascular disease, and previous history of amputation were each significantly and independently associated with infection, conferring 3.4-, 5.5-, and 19.9-fold increased risk, respectively. Various social and economic factors were investigated and found not to be risks for infection. These results are similar to those in our study.

The strengths of our study included the fact that it involved a relatively large group of patients, the patients had a thorough and uniform baseline foot examination by experienced podiatrists, and they were then carefully followed for a long period. We also used internationally accepted definitions for foot infections and defined osteomyelitis by bone culture. One limitation of this study is that data on the microbial isolates of the infections were not collected. We rarely take superficial swabs of wounds because they are unreliable culture specimens (51–53). Thus, most of our cultures were of deep tissue and therefore obtained only for the more severe wounds. Another limitation was that we lacked some disease-staging data, such as serial glycated hemoglobin levels, and some information on comorbidities.

The results of this study clearly demonstrate the relatively high incidence of foot infections in people with diabetes, even those who have been subjected to intensive efforts to prevent foot complications. We have also defined the most important risk factors for these infections. Foot infections almost invariably occur in patients who sustain a foot wound, especially if the wound is of long duration and penetrates to underlying bone or if the patient has coexisting peripheral vascular disease or recurrent foot wounds. Finally, we have demonstrated the high amputation risk associated with foot infections in diabetic patients. Fortunately, the risk factors associated with foot wounds and infection are all easily detected by a simple screening foot examination, allowing preventative efforts to be targeted to those at greatest risk (54). Although foot complications occurred despite our interventions, successful preventative efforts could potentially dramatically reduce the high rate of these potentially devastating problems in individuals with diabetes.


   Acknowledgments
 
We thank Edward J. Boyko, MD, for reviewing the manuscript and for providing suggestions for data and statistical analyses.


   Footnotes
 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received for publication December 10, 2005. Accepted for publication February 18, 2006.


   References
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 

  1. Boulton AJ, Vileikyte L: The diabetic foot: the scope of the problem J Fam Pract49(Suppl. 11):S3–S8, 2000
  2. Levin M: Pathophysiology of diabetic foot lesions. In Clinical Diabetes Mellitus: A Problem-Oriented Approach. Davidson JK, Ed. New York, Theime Medical, 1991, p. 504–510
  3. Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J: The global burden of diabetic foot disease. Lancet 366:1719–1724, 2005[Medline]
  4. Lavery LA, Ashry HR, van Houtum W, Pugh JA, Harkless LB, Basu S: Variation in the incidence and proportion of diabetes-related amputations in minorities. Diabetes Care 19:48–52, 1996[Abstract]
  5. Lavery LA, van Houtum WH, Ashry HR, Armstrong DG, Pugh JA: Diabetes-related lower-extremity amputations disproportionately affect blacks and Mexican Americans. South Med J 92:593–599, 1999[Medline]
  6. Pecoraro RE: Chronology and determinants of tissue repair in diabetic lower-extremity ulcers. Diabetes 40:1305–1313, 1991[Abstract]
  7. Pecoraro RE, Reiber GE, Burgess EM: Pathways to diabetic limb amputation: basis for prevention. Diabetes Care 13:513–521, 1990[Abstract]
  8. Fylling CP, Knighton DR: Amputation in the diabetic population: incidence, causes, cost, treatment, and prevention. J Enterostomal Ther 16:247–255, 1989[Medline]
  9. Boyko EJ, Lipsky BA: Infection and diabetes mellitus. In Diabetes in America. 2nd ed. Harris MI, Ed. Washington, DC, National Institutes of Health, 1995, p. 485–496 (publ. no. 95-1468)
  10. Lavery LA, Armstrong DG, Wunderlich RP, Boulton AJM, Tredwell JL: Diabetic foot syndrome: evaluating the prevalence and incidence of foot pathology in Mexican Americans and non-Hispanic whites from a diabetes disease management cohort. Diabetes Care 26:1435–1438, 2003[Abstract/Free Full Text]
  11. Boyko EJ, Ahroni JH, Stensel V, Forsberg RC, Davignon DR, Smith DG: A prospective study of risk factors for diabetic foot ulcer: the Seattle Diabetic Foot Study. Diabetes Care 22:1036–1042, 1999[Abstract/Free Full Text]
  12. Armstrong DG, Lavery LA, Vela SA, Quebedeaux TL, Fleischli JG: Choosing a practical screening instrument to identify patients at risk for diabetic foot ulceration. Arch Intern Med 158:289–292, 1998[Abstract/Free Full Text]
  13. Khan NA, Rahim SA, Anand SS, Simel DL, Panju A: Does the clinical examination predict lower extremity peripheral arterial disease? JAMA 295:536–546, 2006[Abstract/Free Full Text]
  14. Lavery LA, Armstrong DG, Vela SA, Quebedeaux TL, Fleischli JG: Practical criteria for screening patients at high risk for diabetic foot ulceration. Arch Intern Med 158:158–162, 1998
  15. Armstrong DG, Stacpoole-Shea S, Nguyen HC, Harkless LB: Lengthening of the Achilles tendon in diabetic patients who are at high risk for ulceration of the foot. J Bone Joint Surg Am 81:535–538, 1999[Abstract/Free Full Text]
  16. Lavery LA, Armstrong DG, Boulton AJM: Ankle equinus deformity and its relationship to high plantar pressure in a large population with diabetes mellitus. J Am Podiatr Med Assoc 92:479–482, 2002[Abstract/Free Full Text]
  17. Birke J, Cornwall MA, Jackson M: Relationship between hallux limitus and ulceration of the great toe. Sports Phys Ther J Orthop 10:172–176, 1988
  18. Birke JA, Franks D, Foto JG: First ray joint limitation, pressure, and ulceration of the first metatarsal head in diabetes mellitus. Foot Ankle 16:277–284, 1995[Medline]
  19. Quaney B, Meyer K, Cornwall MW, McPoil TG: A comparison of the dynamic pedobarograph and EMED systems for measuring dynamic foot pressures. Foot Ankle Int 16:562–566, 1995[Medline]
  20. Meyers-Rice B, Sugars L, McPoil T, Cornwall MW: Comparison of three methods for obtaining plantar pressures in nonpathologic subjects. J Am Podiatr Med Assoc 84:499–504, 1994[Abstract]
  21. Armstrong DG, Peters EJ, Athanasiou KA, Lavery LA: Is there a critical level of plantar foot pressure to identify patients at risk for neuropathic foot ulceration? J Foot Ankle Surg 37:303–307, 1998[Medline]
  22. Armstrong DG, Lavery LA, Harkless LB: Who is at risk for diabetic foot ulceration? Clin Podiatr Med Surg 15:11–19, 1998[Medline]
  23. International Working Group on the Diabetic Foot: International Consensus on the Diabetic Foot. Apelqvist J, Bakker K, Van Houtum WH, Nabuurs-Franssen MH, Schaper NC, Eds. Maastricht, the Netherlands, International Working Group on the Diabetic Foot, 1999
  24. Peters EJ, Lavery LA: Effectiveness of the diabetic foot risk classification system of the International Working Group on the Diabetic Foot. Diabetes Care 24:1442–1447, 2001[Abstract/Free Full Text]
  25. Lavery LA, Armstrong DG, Harkless LB: Classification of diabetic foot wounds. J Foot Ankle Surg 35:528–531, 1996[Medline]
  26. Armstrong DG, Lavery LA, Harkless LB: Validation of a diabetic wound classification system: the contribution of depth, infection, and vascular disease to the risk of amputation. Diabetes Care 21:855–859, 1998[Abstract]
  27. Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Harkless LB, Boulton AJ: A comparison of two diabetic foot ulcer classification systems: the Wagner and the University of Texas wound classification systems. Diabetes Care 24:84–88, 2001[Abstract/Free Full Text]
  28. Jeffcoate WJ: Theories concerning the pathogenesis of the acute charcot foot suggest future therapy. Curr Diab Rep 5:430–435, 2005[Medline]
  29. Armstrong DG, Todd WF, Lavery LA, Harkless LB: The natural history of acute Charcot’s arthropathy in a diabetic foot specialty clinic. Diabet Med 14:357–363, 1997[Medline]
  30. Lipsky BA: Diabetic foot infections: pathophysiology, diagnosis, and treatment. Int J Dermatol 30:560–562, 1991[Medline]
  31. Lipsky BA: Osteomyelitis of the foot in diabetic patients. Clin Infect Dis 25:1318–1326, 1997[Medline]
  32. Lipsky BA: Evidence-based antibiotic therapy of diabetic foot infections. FEMS Immunol Med Microbiol 26:267–276, 1999[Medline]
  33. Lipsky BA, Pecoraro RE, Wheat LJ: The diabetic foot: soft tissue and bone infection. Infect Dis Clin N Am 4:409–432, 1990[Medline]
  34. Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA: Diabetic neuropathic foot ulcers: predicting which ones will not heal. Am J Med 115:627–631, 2003[Medline]
  35. Birke JA, Novick A, Patout CA, Coleman WC: Healing rates of plantar ulcers in leprosy and diabetes. Lepr Rev 63:365–374, 1992[Medline]
  36. Chang BB, Darling RC: Expeditious management of ischemic invasive foot infections. Cardiovasc Surg 4:792–795, 1996[Medline]
  37. Cruciani M, Lipsky BA, Mengoli C, de Lalla F: Are granulocyte colony-stimulating factors beneficial in treating diabetic foot infections? A meta-analysis. Diabetes Care 28:454–460, 2005[Abstract/Free Full Text]
  38. Peck KR, Son DW, Song JH, Kim S, Oh MD, Choe KW: Enhanced neutrophil functions by recombinant human granulocyte colony-stimulating factor in diabetic patients with foot infections in vitro. J Korean Med Sci 16:39–44, 2001[Medline]
  39. Bessman AN, Sapico FL: Infections in the diabetic patient: the role of immune dysfunction and pathogen virulence factors. J Diabetes Complications 6:258–262, 1992[Medline]
  40. Armstrong AP, Lavery KM, Hollingsworth T: Apocrine hidrocystoma: report of a case. Br J Oral Maxillofac Surg 34:335–337, 1996[Medline]
  41. Armstrong DG, Lavery LA, Saraya M, Ashry H: Leukocytosis is a poor indicator of acute osteomyelitis of the foot in diabetes mellitus. J Foot Ankle Surg 34:280–283, 1996
  42. Armstrong DG, Perales TA, Murff R, Edelson GW, Welchon JG: Value of white blood cell count with differential in the acute diabetic foot infection. J Am Podiatr Med Assn 86:224–227, 1996[Abstract]
  43. Lavery LA, Armstrong DG, Quebedeaux TL, Walker SC: Puncture wounds: the frequency of normal laboratory values in the face of severe foot infections of the foot in diabetic and non-diabetic adults. Am J Med 101:521–525, 1996[Medline]
  44. Armstrong DG, Lavery LA, Quebedeaux TL, Walker SC: Surgical morbidity and the risk of amputation following infected puncture wounds of the foot in diabetic and non-diabetic adults. South Med J 90:384–389, 1997[Medline]
  45. Sriussadaporn S, Mekanandha P, Vannasaeng S, Nitiyanant W, Kolmoltri C, Ploybutr S, Yamwong P, Peerapatdit T, Vichayanrat A: Factors associated with diabetic foot ulceration in Thailand: a case-control study. Diabet Med 14:50–56, 1997[Medline]
  46. Pham HT, Armstrong DG, Harvey C, Harkless LB, Giurini JM, Veves A: Screening techniques to identify the at risk patients for developing diabetic foot ulcers in a prospective multicenter trial. Diabetes Care 23:606–611, 2000[Abstract/Free Full Text]
  47. McNeely MJ, Boyko EJ, Ahroni JE, Stensel VL, Reiber GE, Smith DG, Pecoraro RE: The independent contributions of diabetic neuropathy and vasculopathy in foot ulceration. Diabetes Care 18:216–219, 1995[Abstract]
  48. Abbott CA, Vileikyte L, Williamson S, Carrington AL, Boulton AJ: Multicenter study of the incidence of and predictive risk factors for diabetic neuropathic foot ulceration. Diabetes Care 21:1071–1075, 1998[Abstract]
  49. Abbott CA, Carrington AL, Ashe H, Bath S, Every LC, Griffiths J, Hann AW, Hussein A, Jackson N, Johnson KE, Ryder CH, Torkington R, Van Ross ER, Whalley AM, Widdows P, Williamson S, Boulton AJ: The North-West Diabetes Foot Care Study: incidence of, and risk factors for, new diabetic foot ulceration in a community-based patient cohort. Diabet Med 19:377–384, 2002[Medline]
  50. Peters EJ, Lavery LA, Armstrong DG: Diabetic lower extremity infection Influence of physical, psychological, and social factors. J Diabetes Complications 19:107–112, 2005[Medline]
  51. Perry CR, Pearson RL, Miller GA: Accuracy of cultures of material from swabbing of the superficial aspect of the wound and needle biopsy in the preoperative assessment of osteomyelitis. J Bone Joint Surg Am 73:745–749, 1991[Abstract/Free Full Text]
  52. Armstrong DG, Lipsky BA: Advances in the treatment of diabetic foot infections. Diabetes Technol Ther 6:167–177, 2004[Medline]
  53. Senneville E, Melliez H, Beltrand E, Legout L, Valette M, Cazaubiel M, Cordonnier M, Caillaux M, Yazdanpanah Y, Mouton Y: Culture of percutaneous bone biopsy specimens for diagnosis of diabetic foot osteomyelitis: concordance with ulcer swab cultures. Clin Infect Dis 42:57–62, 2006[Medline]
  54. Singh N, Armstrong DG, Lipsky BA: Preventing foot ulcers in patients with diabetes. JAMA 293:217–228, 2005[Abstract/Free Full Text]

Add to CiteULike CiteULike   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?

Find additional patient-related information at:

Preventing Foot Infections in People With Diabetes


This article has been cited by other articles:


Home page
 West J Nurs ResHome page
W. J. Borges and S. K. Ostwald
Improving Foot Self-Care Behaviors With Pies Sanos
West J Nurs Res, April 1, 2008; 30(3): 325 - 341.
[Abstract] [PDF]

Home page
 Foot & Ankle SpecialistHome page
T. Zgonis, J. J. Stapleton, and T. S. Roukis
A Stepwise Approach to the Surgical Management of Severe Diabetic Foot Infections
Foot & Ankle Specialist, February 1, 2008; 1(1): 46 - 53.
[Abstract] [PDF]

Home page
 Age AgeingHome page
C.-H. Tseng, C.-K. Chong, C.-P. Tseng, and T.-Y. Tai
The association between urinary albumin excretion and ankle-brachial index in elderly Taiwanese patients with type 2 diabetes mellitus
Age Ageing, January 1, 2008; 37(1): 77 - 82.
[Abstract] [Full Text] [PDF]

Home page
 Diabetes CareHome page
L. A. Lavery, E. J.G. Peters, J. R. Williams, D. P. Murdoch, A. Hudson, and D. C. Lavery
Reevaluating the Way We Classify the Diabetic Foot: Restructuring the diabetic foot risk classification system of the International Working Group on the Diabetic Foot
Diabetes Care, January 1, 2008; 31(1): 154 - 156.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Microbiol.Home page
D. M. Citron, E. J. C. Goldstein, C. V. Merriam, B. A. Lipsky, and M. A. Abramson
Bacteriology of Moderate-to-Severe Diabetic Foot Infections and In Vitro Activity of Antimicrobial Agents
J. Clin. Microbiol., September 1, 2007; 45(9): 2819 - 2828.
[Abstract] [Full Text] [PDF]

Home page
 J Antimicrob ChemotherHome page
B. A. Lipsky, P. Giordano, S. Choudhri, and J. Song
Treating diabetic foot infections with sequential intravenous to oral moxifloxacin compared with piperacillin-tazobactam/amoxicillin-clavulanate
J. Antimicrob. Chemother., August 1, 2007; 60(2): 370 - 376.
[Abstract] [Full Text] [PDF]

Home page
 Diabetes CareHome page
A. Sotto, J.-L. Richard, N. Jourdan, C. Combescure, N. Bouziges, J.-P. Lavigne, and on behalf of the Nimes University Hospital Working
Miniaturized Oligonucleotide Arrays: A new tool for discriminating colonization from infection due to Staphylococcus aureus in diabetic foot ulcers
Diabetes Care, August 1, 2007; 30(8): 2051 - 2056.
[Abstract] [Full Text] [PDF]

Home page
 Am J Health Syst PharmHome page
A. D. Tice, R. S. Turpin, C. T. Hoey, B. A. Lipsky, J. Wu, and M. A. Abramson
Comparative costs of ertapenem and piperacillin-tazobactam in the treatment of diabetic foot infections
Am. J. Health Syst. Pharm., May 15, 2007; 64(10): 1080 - 1086.
[Abstract] [Full Text] [PDF]

Home page
 Diabetes CareHome page
L. A. Lavery, D. G. Armstrong, E. J.G. Peters, and B. A. Lipsky
Probe-to-Bone Test for Diagnosing Diabetic Foot Osteomyelitis: Reliable or relic?
Diabetes Care, February 1, 2007; 30(2): 270 - 274.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow patientINFORMation
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lavery, L. A.
Right arrow Articles by Lipsky, B. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lavery, L. A.
Right arrow Articles by Lipsky, B. A.
Social Bookmarking
Add to CiteULike   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Diabetes Diabetes Care Clinical Diabetes Diabetes Spectrum