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Level of Agreement With a Multi-Test Approach to the Diagnosis of Diabetic Foot Osteomyelitis

Published:September 01, 2018DOI:https://doi.org/10.1053/j.jfas.2018.05.010

      Abstract

      Although bone biopsy has historically been considered the “gold standard” or “standard reference” for the diagnosis of diabetic foot osteomyelitis, some contemporary investigations have provided evidence against this as a single diagnostic test and in support of a combination of clinical, laboratory, and radiographic findings. The objective of this investigation was to measure the level of agreement between several commonly used forms of diagnostic testing for diabetic foot osteomyelitis. A retrospective chart review was performed of 50 consecutive patients admitted to a single tertiary healthcare center with the documented performance of 1) a clinical probe-to-bone test on hospital admission; 2) plain film radiographs prior to any surgical intervention; 3) magnetic resonance imaging prior to any surgical intervention; and an intraoperative excisional bone debridement performed, with samples sent for both 4) histologic analysis and 5) microbiologic analysis. A frequency count of agreement among these 5 tests was performed, and the interobserver (or inter-test) agreement was measured using the kappa statistic. We observed low levels of inter-test agreement between the 5 diagnostic tests (range 42.0%–62.0%), and levels of chance-corrected agreement were well below what would be considered appropriate for a “gold standard” or “standard reference.” Levels of the kappa statistic ranged from 0.0 to 0.220, with most inter-test comparisons falling in the “poor agreement” and “slight agreement” interpretation ranges. The highest level of agreement occurred between the plain film radiographs and magnetic resonance imaging (62.0% agreement and kappa statistic of 0.220). Although it is likely that a combination of clinical, radiographic, and laboratory tests provides the best diagnostic approach for diabetic foot osteomyelitis, the data provided herein indicate that the tests themselves might have high intrinsic levels of unreliability and that the specific combination of tests that might be best used remains unclear.

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      References

        • Lipsky BA
        • Berendt AR
        • Deery HG
        • Embil JM
        • Joseph WS
        • Karchmer AW
        • LeFrock JL
        • Lew DP
        • Mader JT
        • Norden C
        • Tan JS
        Infectious Disease Society of America. Diagnosis and treatment of diabetic foot infections.
        Clin Infect Dis. 2004; 39: 885-910
        • Berendt AR
        • Peters EJ
        • Bakker K
        • Embil JM
        • Eneroth M
        • Hinchliffe RJ
        • Jeffcoate WJ
        • Lipsky BA
        • Senneville E
        • Teh J
        • Valk GD
        Diabetic foot osteomyelitis: a progress report on diagnosis and a systematic review of treatment.
        Diabetes Metab Res Rev. 2008; 24: S145-S161
        • Dinh T
        • Snyder G
        • Veves A
        Current techniques to detect foot infection in the diabetic patient.
        Int J Low Extrem Wounds. 2010; 9: 24-30
        • Butalia S
        • Palda VA
        • Sargeant RJ
        • Detsky AS
        • Mourad O
        Does this patient with diabetes have osteomyelitis of the lower extremity?.
        JAMA. 2008; 299: 806-813
        • Hartemann-Heurtier A
        • Senneville E
        Diabetic foot osteomyelitis.
        Diabetes Metab. 2008; 34: 87-95
        • Shank CF
        • Feibel JB
        Osteomyelitis in the diabetic foot: diagnosis and management.
        Foot Ankle Clin. 2006; 11: 775-789
        • Game F
        Management of osteomyelitis of the foot in diabetes mellitus.
        Nat Rev Endocrinol. 2010; 6: 43-47
        • Sage RA
        • Limb salvage and amputation
        Banks AS Downey MS Martin DE Miller SJ McGlamry's Comprensive Textbook of Foot and Ankle Surgery. 3rd ed. Lippincott, Williams & Wilkins, Philadelphia2001: 1617-1633
        • Basile P
        • Rosenblum BI
        Surgical management and stepwise approach to diabetic foot infections.
        in: Zgonis T Surgical Reconstruction of the Diabetic Foot and Ankle. Lippincott, Williams & Wilkins, Philadelphia2009: 90-99
        • Frykberg RG
        • Zgonis T
        The diabetic Charcot foot.
        in: Sidawy AN Diabetic Foot. Lower Extremity Arterial Disease and Limb Salvage. Lippincott, Williams & Wilkins, Philadelphia2006 (177-28)
      1. Banks AS. A Clinical Guide to the Charcot Foot. In: Medical and Surgical Management of the Diabetic Foot. pp.115-143, edited by SJ Kominsky, Mos by, St. Louis. 1994.

        • Berendt AR
        • Lipsky BA
        Challenges in the infected diabetic foot: osteomyelitis and methicillin-resistant Staphylococcus aureus.
        in: Boulton AJM Cavanagh PR Rayman G The Foot in Diabetes. 4th ed. Wiley, West Sussex, England2006: 169-185
        • Grayson ML
        • Gibbons GW
        • Balogh K
        • Levin E
        • Karchmer AW
        Probing to bone in infected pedal ulcers. A clinical sign of underlying osteomyelitis in diabetic patients.
        JAMA. 1995; 273: 721-723
        • Lavery LA
        • Armstrong DG
        • Peters EJ
        • Lipsky BA
        Probe-to-bone test for diagnosing diabetic foot osteomyelitis: reliable or relic?.
        Diabetes Care. 2007; 30: 270-274
        • Aragon-Sanchez J
        • Lipsky BA
        • Lazaro-Martinez JL
        Diagnosing diabetic foot osteomyelitis: is the combination of probe-to-bone test and plain radiography sufficient for high-risk patients?.
        Diabet Med. 2011; 28: 191-194
        • Morales Lozano R
        • Gonzalez Fernandez ML
        • Martinez Hernandez D
        • Beneit Montesinos JV
        • Guisado Jimenez S
        • Gonzales Jurado MA
        Validating the probe-to-bone test and other tests for diagnosing chronic osteomyelits in the diabetic foot.
        Diabetes Care. 2010; 33: 2140-2145
        • Dinh MT
        • Abad CL
        • Safdar N
        Diagnostic accuracy of the physical examination and imaging tests for osteomyelitis underlying diabetic foot ulcers: meta-analysis.
        Clin Infect Dis. 2008; 47: 519-527
        • Nawaz A
        • Torigian DA
        • Siegelman ES
        • Basu S
        • Chryssikos T
        • Alavi A
        Diagnostic performance of FDG-PET, MRI, and plain film radiography (PFR) for the diagnosis of osteomyelitis in the diabetic foot.
        Mol Imaging Biol. 2010; 12: 335-342
        • Ertugrul MB
        • Baktiroglu S
        • Salman S
        • Unal S
        • Aksoy M
        • Berberoglu K
        • Calangu S
        The diagnosis of osteomyelitis of the foot in diabetes: microbiological examination vs. magnetic resonance imaging and labeled leucocyte scanning.
        Diabet Med. 2006; 23: 649-653
        • Kapoor A
        • Page S
        • Lavalley M
        • Gale DR
        • Felson DT
        Magnetic resonance imaging for diagnosing foot osteomyelitis: a meta-analysis.
        Arch Intern Med. 2007; 167: 125-132
        • Joshi R
        • Smith S
        Is magnetic resonance imaging a suitable imaging modality for the diagnosis of osteomyelitis of the foot or ankle?.
        Can Assoc Radiol J. 2009; 60: 119-120
        • Filippi L
        • Uccioli L
        • Giurato L
        • Schillaci O
        Diabetic foot infection: usefulness of SPECT/CT for 99 m Tc-HMPAO-labeled leukocyte imaging.
        Nucl Med. 2009; 50: 1042-1046
        • Rozzanigo U
        • Tagliani A
        • Vittorini E
        • Pacchioni R
        • Brivio LR
        • Caudana R
        Role of magnetic resonance imaging in the evaluation of diabetic foot with suspected osteomyelitis.
        Radiol Med. 2009; 114: 121-132
        • Fleischer AE
        • Didyk AA
        • Woods JB
        • Burns SE
        • Wrobel JS
        • Armstrong DG
        Combined clinical and laboratory testing improves diagnostic accuracy for osteomyelitis in the diabetic foot.
        J Foot Ankle Surg. 2009; 48: 39-46
        • Kaleta JL
        • Fleischli JW
        • Reilly CH
        The diagnosis of osteomyelitis in diabetes using erythrocyte sedimentation rate: a pilot study.
        J Am Podiatr Med Assoc. 2001; 91: 445-450
        • Ertugrul BM
        • Savk O
        • Ozturk B
        • Cobanoglu M
        • Oncu S
        • Sakarya S
        The diagnosis of diabetic foot osteomyelitis: examination findings and laboratory values.
        Med Sci Monit. 2009; 15: CR307-CR312
        • Weiner RD
        • Viselli SJ
        • Accetta P
        Histology versus microbiology for accuracy in identification of osteomyelitis in the diabetic foot.
        J Foot Ankle Surg. 2011; 50: 197-200
        • Lesens O
        • Desbiez F
        • Vidal M
        • Robin F
        • Descamps S
        • Beytout J
        • Laurichesse H
        • Tauveron I
        Culture of per-wound bone specimens: a simplified approach for the medical management of diabetic foot osteomyelitis.
        Clin Microbiol Infect. 2011; 17: 285-291
        • Bernard L
        • Uckay I
        • Vuagnat A
        • Assal M
        • Stern R
        • Rohner P
        • Hoffmeyer P
        Two consecutive deep sinus tract cultures predict the pathogen of osteomyelitis.
        Int J Infect Dis. 2010; 14: e390-e393
        • Zuluaga AF
        • Galvis W
        • Saldarriaga JG
        • Agudelo M
        • Salazar BE
        • Vesga O
        Etiologic diagnosis of chronic osteomyelitis: a prospective study.
        Arch Intern Med. 2006; 166: 95-100
        • 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. 2006; 42: 57-62
        • Ertugrul MB
        • Baktiroglu S
        • Salman S
        • Unal S
        • Aksoy M
        • Berberoglu K
        • Calangu S
        The diagnosis of osteomyelitis of the foot in diabetes: microbiological examination vs. magnetic resonance imaging and labeled leucocyte scanning.
        Diabet Med. 2006; 23: 649-653
        • Meyr AJ
        • Singh S
        • Zhang X
        • Khilko N
        • Mukherjee A
        • Sheridan MH
        • Khurana JS
        Statistical reliability of bone biopsy for the diagnosis of diabetic foot osteomyelitis.
        J Foot Ankle Surg. 2011; 50: 663-667
        • Malay DS
        Osteomyelitis and the tarnished gold standard.
        J Foot Ankle Surg. 2013; 52: 1
        • Ertugrul MB
        • Baktiroglu S
        • Salman S
        • Unal S
        • Aksoey M
        • Berberoglu K
        • Calangu S
        Pathogens isolated from deep soft tissue and bone in patients with diabetic foot infection.
        J Am Podiatr Med Assoc. 2008; 98: 290-295
        • Joseph WS
        Bone and joint infections.
        in: Joseph WS Handbook of Lower Extremity Infections. 2nd ed. Churchill Livingstone, Philadelphia,, 2003: 54-79
        • Golinko MS
        • Joffe R
        • de Vinck D
        • Chandrasekaran E
        • Stojadinovic O
        • Barrientos S
        • Vukelic S
        • Tomic-Canic M
        • Brem H
        Surgical pathology to describe the clinical margin of debridement of chronic wounds using a wound electronic medical record.
        J Am Coll Surg. 2009; 209: 254-260
        • Schiller AL
        • Wang BY
        • Klein MJ
        Bones and joints.
        in: Rubin E Gorstein F Rubin R Schwarting R Strayer D Rubin's Pathology: Clinicopathologic Foundations of Medicine. 4th ed. Lippincott, Willams & Wilkins, Philadelphia2005: 1304-1385
        • McGinn T
        • Guyatt G
        • Cook R
        • Korenstein D
        • Meade MO
        Measuring agreement beyond chance.
        in: Guyatt G Rennie D Meade MO Cook DJ Users’ Guide to the Medical Literature. McGraw Hill Medical, New York2008: 481-489