Challenges in diagnosing infection in the diabetic foot

Diabetic Medicine

Volumn 32, Issue 6, 2015, Pages 748-759

  Glaudemans, A W J M ^a   Uckay I ^b   Lipsky, B A ^b,c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORINE 18; TRACER; BIOLOGICAL MARKER;

BONE SCINTISCANNING; CLINICAL EVALUATION; COMPUTER ASSISTED TOMOGRAPHY; DIABETIC FOOT; ECHOGRAPHY; ERYTHROCYTE SEDIMENTATION RATE; FOOT RADIOGRAPHY; HISTOPATHOLOGY; HUMAN; LEUKOCYTE; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOMYELITIS; PHYSICAL EXAMINATION; PREDICTIVE VALUE; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SKIN FLORA; BLOOD; BONE; COMPLICATION; DIAGNOSTIC IMAGING; INFECTION; INFLAMMATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PROCEDURES;

BIOMARKERS; BONE AND BONES; DIABETIC FOOT; DIAGNOSTIC IMAGING; HUMANS; INFECTION; INFLAMMATION; MICROBIOLOGICAL TECHNIQUES; OSTEOMYELITIS;

EID: 84929504501     PISSN: 07423071     EISSN: 14645491     Source Type: Journal    
DOI: 10.1111/dme.12750     Document Type: Review

References (83)

1. Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ, Armstrong DG et al. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis 2012; 54: e132-173.
2. Lavery LA, Armstrong DG, Wunderlich RP, Mohler MJ, Wendel CS, Lipsky BA. Risk factors for foot infections in individuals with diabetes. Diabetes Care 2006; 29: 1288-1293.
3. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K et al. High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study. Diabetologia 2007; 50: 18-25.
4. Edmonds M, Foster A. The use of antibiotics in the diabetic foot. Am J Surg 2004; 187: 25S-28S.
5. Ertugrul BM, Lipsky BA, Savk O. Osteomyelitis or Charcot neuro-osteoarthropathy? Differentiating these disorders in diabetic patients with a foot problem. Diabet Foot Ankle 2013; 4: doi: 10.3402/dfa.v4i0.21855.
6. Uzun G, Mutluoglu M. Images in clinical medicine. Dependent rubor. N Engl J Med 2011; 364: e56.
7. Chargui M, Uckay I, Suva D, Christofilopoulos P, Lomessy A. Pittet D [Deep soft tissue infections]. Rev Med Suisse 2014; 10: 920-924.
8. Tobalem M, Uckay I. Images in clinical medicine. Evolution of a diabetic foot infection. N Engl J Med 2013; 369: 2252.
9. Cutting KF, White R. Defined and refined: criteria for identifying wound infection revisited. Br J Community Nurs 2004; 9: S6-15.
10. Lipsky BA, Peters EJ, Senneville E, Berendt AR, Embil JM, Lavery LA et al. Expert opinion on the management of infections in the diabetic foot. Diabetes Metab Res Rev 2012; 28(Suppl. 1): 163-178.
11. Newman LG, Waller J, Palestro CJ, Schwartz M, Klein MJ, Hermann G et al. Unsuspected osteomyelitis in diabetic foot ulcers. Diagnosis and monitoring by leukocyte scanning with indium in 111 oxyquinoline. JAMA 1991; 266: 1246-1251.
12. Uckay I, Jugun K, Gamulin A, Wagener J, Hoffmeyer P, Lew D. Chronic osteomyelitis. Curr Infect Dis Rep 2012; 14: 566-575.
13. 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.
14. 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.
15. Mutluoglu M, Uzun G, Sildiroglu O, Turhan V, Mutlu H, Yildiz S. Performance of the probe-to-bone test in a population suspected of having osteomyelitis of the foot in diabetes. J Am Podiatr Med Assoc 2012; 102: 369-373.
16. Garcia ME, Lazaro-Martinez JL, Ragon-Sanchez FJ, Cecilia-Matilla A, Eit-Montesinos JV. Gonzalez Jurado MA. Inter-observer reproducibility of probing to bone in the diagnosis of diabetic foot osteomyelitis. Diabet Med 2011; 28: 1238-1240.
17. 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.
18. Michail M, Jude E, Liaskos C, Karamagiolis S, Makrilakis K, Dimitroulis D et al. The performance of serum inflammatory markers for the diagnosis and follow-up of patients with osteomyelitis. Int J Low Extrem Wounds 2013; 12: 94-99.
19. 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.
20. Eder J, Hlavin G, Haushofer A, Trubert-Exinger D, Trautinger F. Correlation of serum procalcitonin with the severity of skin and skin structure infections - a pilot study. J Dtsch Dermatol Ges 2012; 10: 564-571.
21. Mutluoglu M, Uzun G, Ipcioglu OM, Sildiroglu O, Ozcan O, Turhan V et al. Can procalcitonin predict bone infection in people with diabetes with infected foot ulcers? A pilot study. Diabetes Res Clin Pract 2011; 94: 53-56.
22. Saeed K, Ahmad N, Dryden M. The value of procalcitonin measurement in localized skin and skin structure infection, diabetic foot infections, septic arthritis and osteomyelitis. Expert Rev Mol Diagn 2014; 14: 47-54.
23. Uckay I, Garzoni C, Ferry T, Harbarth S, Stern R, Assal M et al. Postoperative serum pro-calcitonin and C-reactive protein levels in patients with orthopedic infections. Swiss Med Wkly 2010; 140: w13124.
24. Jonaidi JN, Safaee FM, Izadi M. Safaee Firouzabadi MS, Saburi A. Can procalcitonin be an accurate diagnostic marker for the classification of diabetic foot ulcers? Int. J Endocrinol Metab 2014; 12: e13376.
25. Persson L, Johansson C, Ryden C. Antibodies to Staphylococcus aureus bone sialoprotein-binding protein indicate infectious osteomyelitis. Clin Vaccine Immunol 2009; 16: 949-952.
26. Nyazee HA, Finney KM, Sarikonda M, Towler DA, Johnson JE, Babcock HM. Diabetic foot osteomyelitis: bone markers and treatment outcomes. Diabetes Res Clin Pract 2012; 97: 411-417.
27. Aragon-Sanchez J, Cabrera-Galvan JJ. The role of cytokines in diabetic foot osteomyelitis. Diabet Med 2013; 30: 628-629.
28. Petrova NL, Dew TK, Musto RL, Sherwood RA, Bates M, Moniz CF et al. Inflammatory and bone turnover markers in a cross-sectional and prospective study of acute Charcot osteoarthropathy. Diabet Med 2015; 32: 267-273.
29. Senneville E, Morant H, Descamps D, Dekeyser S, Beltrand E, Singer B et al. Needle puncture and transcutaneous bone biopsy cultures are inconsistent in patients with diabetes and suspected osteomyelitis of the foot. Clin Infect Dis 2009; 48: 888-893.
30. Senneville E, Gaworowska D, Topolinski H, Devemy F, Nguyen S, Singer B et al. Outcome of patients with diabetes with negative percutaneous bone biopsy performed for suspicion of osteomyelitis of the foot. Diabet Med 2012; 29: 56-61.
31. Chantelau E, Wolf A, Ozdemir S, Hachmoller A, Ramp U. Bone histomorphology may be unremarkable in diabetes mellitus. Med Klin (Munich) 2007; 102: 429-433.
32. Meyr AJ, Singh S, Zhang X, Khilko N, Mukherjee A, Sheridan MJ et al. Statistical reliability of bone biopsy for the diagnosis of diabetic foot osteomyelitis. J Foot Ankle Surg 2011; 50: 663-667.
33. Cecilia-Matilla A, Lazaro-Martinez JL, Ragon-Sanchez J, Garcia-Morales E, Garcia-Alvarez Y, Eit-Montesinos JV. Histopathologic characteristics of bone infection complicating foot ulcers in diabetic patients. J Am Podiatr Med Assoc 2013; 103: 24-31.
34. Cecilia-Matilla A, Lazaro-Martinez JL, Ragon-Sanchez J. Statistical reliability of bone biopsy for the diagnosis of diabetic foot osteomyelitis. J Foot Ankle Surg 2013; 52: 692.
35. Aragon-Sanchez J. Clinical-pathological characterization of diabetic foot infections: grading the severity of osteomyelitis. Int J Low Extrem Wounds 2012; 11: 107-112.
36. Lipsky BA, Napolitano LM, Moran GJ, Vo L, Nicholson S, Kim M. Inappropriate initial antibiotic treatment for complicated skin and soft tissue infections in hospitalized patients: incidence and associated factors. Diagn Microbiol Infect Dis 2014; 79: 273-279.
37. Lipsky BA, Napolitano LM, Moran GJ, Vo L, Nicholson S, Chen S et al. Economic outcomes of inappropriate initial antibiotic treatment for complicated skin and soft tissue infections: a multicenter prospective observational study. Diagn Microbiol Infect Dis 2014; 79: 266-272.
38. Percival SL, McCarty SM, Lipsky BA. Biofilms and wounds: an overview of the evidence. Adv Wound Care 2014; in press.
39. Nelson EA, Backhouse MR, Bhogal MS, Wright-Hughes A, Lipsky BA, Nixon J et al. Concordance in diabetic foot ulcer infection. BMJ Open 2013; 3(1).
40. Lavigne JP, Sotto A, Dunyach-remy C, Lipsky BA. New molecular techniques to study the skin microbiota of diabetic foot ulcers. Adv Wound Care 2015; 4: 38-49.
41. Gardner SE, Hillis SL, Heilmann K, Segre JA, Grice EA. The neuropathic diabetic foot ulcer microbiome is associated with clinical factors. Diabetes 2013; 62: 923-930.
42. Sotto A, Lina G, Richard JL, Combescure C, Bourg G, Vidal L et al. Virulence potential of Staphylococcus aureus strains isolated from diabetic foot ulcers: a new paradigm. Diabetes Care 2008; 31: 2318-2324.
43. Sotto A, Richard JL, Messad N, Molinari N, Jourdan N, Schuldiner S et al. Distinguishing colonization from infection with Staphylococcus aureus in diabetic foot ulcers with miniaturized oligonucleotide arrays: a French multicenter study. Diabetes Care 2012; 35: 617-623.
44. Berendt AR, Peters EJ, Bakker K, Embil JM, Eneroth M, Hinchliffe RJ et al. Specific guidelines for treatment of diabetic foot osteomyelitis. Diabetes Metab Res Rev 2008; 24(Suppl. 1): S190-S191.
45. Teh J, Berendt T, Lipsky BA. Rational Imaging. Investigating suspected bone infection in the diabetic foot. BMJ 2009; 339: b4690.
46. Donovan A, Schweitzer ME. Current concepts in imaging diabetic pedal osteomyelitis. Radiol Clin North Am 2008; 46: 1105-1124, vii.
47. Morrison WB, Schweitzer ME, Wapner KL, Hecht PJ, Gannon FH, Behm WR. Osteomyelitis in feet of diabetics: clinical accuracy, surgical utility, and cost-effectiveness of MR imaging. Radiology 1995; 196: 557-564.
48. 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.
49. Sanverdi SE, Ergen BF, Oznur A. Current challenges in imaging of the diabetic foot. Diabet Foot Ankle 2012; 3.
50. Tan PL, Teh J. MRI of the diabetic foot: differentiation of infection from neuropathic change. Br J Radiol 2007; 80: 939-948.
51. Klauser AS, Tagliafico A, Allen GM, Boutry N, Campbell R, Court-Payen et al. Clinical indications for musculoskeletal ultrasound: a Delphi-based consensus paper of the European Society of Musculoskeletal Radiology. Eur Radiol 2012; 22: 1140-1148.
52. Loredo R, Rahal A, Garcia G, Metter D. Imaging of the diabetic foot diagnostic dilemmas. Foot Ankle Spec 2010; 3: 249-264.
53. Callegari L, Leonardi A, Bini A, Sabato C, Nicotera P, Spano' E et al. Ultrasound-guided removal of foreign bodies: personal experience. Eur Radiol 2009; 19: 1273-1279.
54. Capriotti G, Chianelli M, Signore A. Nuclear medicine imaging of diabetic foot infection: results of meta-analysis. Nucl Med Commun 2006; 27: 757-764.
55. Glaudemans AW, de Vries EF, Vermeulen LE, Slart RH, Dierckx RA, Signore A. A large retrospective single-centre study to define the best image acquisition protocols and interpretation criteria for white blood cell scintigraphy with (9)(9)mTc-HMPAO-labelled leucocytes in musculoskeletal infections. Eur J Nucl Med Mol Imaging 2013; 40: 1760-1769.
56. Israel O, Sconfienza LM, Lipsky BA. Diagnosing diabetic foot infection: the role of imaging and a proposed flow chart for assessment. Q J Nucl Med Mol Imaging 2014; 58: 33-45.
57. 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.
58. Palestro CJ, Love C. Nuclear medicine and diabetic foot infections. Semin Nucl Med 2009; 39: 52-65.
59. Glaudemans AW, Galli F, Pacilio M, Signore A. Leukocyte and bacteria imaging in prosthetic joint infection. Eur Cell Mater 2013; 25: 61-77.
60. Tondeur MC, Sand A, Ham HH. Interobserver reproducibility in the interpretation of 99mTc-labelled white blood cell scintigraphic images. Nucl Med Commun 2008; 29: 1093-1099.
61. Erba PA, Glaudemans AW, Veltman NC, Sollini M, Pacilio M, Galli F et al. Image acquisition and interpretation criteria for 99mTc-HMPAO-labelled white blood cell scintigraphy: results of a multicentre study. Eur J Nucl Med Mol Imaging 2014; 41: 615-623.
62. Gemmel F, Van den WH, Love C, Welling MM, Gemmel P, Palestro CJ. Prosthetic joint infections: radionuclide state-of-the-art imaging. Eur J Nucl Med Mol Imaging 2012; 39: 892-909.
63. Palestro CJ, Love C, Bhargava KK. Labeled leukocyte imaging: current status and future directions. Q J Nucl Med Mol Imaging 2009; 53: 105-123.
64. Erdman WA, Buethe J, Bhore R, Ghayee HK, Thompson C, Maewal P et al. Indexing severity of diabetic foot infection with 99mTc-WBC SPECT/CT hybrid imaging. Diabetes Care 2012; 35: 1826-1831.
65. Vouillarmet J, Morelec I, Thivolet C. Assessing diabetic foot osteomyelitis remission with white blood cell SPECT/CT imaging. Diabet Med 2014; 31: 1093-1099.
66. Basu S, Chryssikos T, Moghadam-Kia S, Zhuang H, Torigian DA, Alavi A. Positron emission tomography as a diagnostic tool in infection: present role and future possibilities. Semin Nucl Med 2009; 39: 36-51.
67. Palestro CJ. FDG-PET in musculoskeletal infections. Semin Nucl Med 2013; 43: 367-376.
68. Kagna O, Srour S, Melamed E, Militianu D, Keidar Z. FDG PET/CT imaging in the diagnosis of osteomyelitis in the diabetic foot. Eur J Nucl Med Mol Imaging 2012; 39: 1545-1550.
69. 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.
70. Palestro CJ. 18F-FDG and diabetic foot infections: the verdict is. J Nucl Med 2011; 52: 1009-1011.
71. Papanas N, Zissimopoulos A, Maltezos E. (18)F-FDG PET and PET/CT for the diagnosis of diabetic foot osteomyelitis. Hippokratia 2013; 17: 4-6.
72. Treglia G, Sadeghi R, Annunziata S, Zakavi SR, Caldarella C, Muoio B et al. Diagnostic performance of Fluorine-18-Fluorodeoxyglucose positron emission tomography for the diagnosis of osteomyelitis related to diabetic foot: a systematic review and a meta-analysis. Foot 2013; 23: 140-148.
73. Aslangul E, M'bemba J, Caillat-Vigneron N, Coignard S, Larger E, Boitard C et al. Diagnosing diabetic foot osteomyelitis in patients without signs of soft tissue infection by coupling hybrid 67 Ga SPECT/CT with bedside percutaneous bone puncture. Diabetes Care 2013; 36: 2203-2210.
74. Aksoy SY, Asa S, Ozhan M, Ocak M, Sager MS, Erkan ME et al. FDG and FDG-labelled leucocyte PET/CT in the imaging of prosthetic joint infection. Eur J Nucl Med Mol Imaging 2014; 41: 556-564.
75. Glaudemans AW, Quintero AM, Signore A. PET/MRI in infectious and inflammatory diseases: will it be a useful improvement? Eur J Nucl Med Mol Imaging 2012; 39: 745-749.
76. Bhargava KK, Gupta RK, Nichols KJ, Palestro CJ. In vitro human leukocyte labeling with (64)Cu: an intraindividual comparison with (111)In-oxine and (18)F-FDG. Nucl Med Biol 2009; 36: 545-549.
77. Nanni C, Errani C, Boriani L, Fantini L, Ambrosini V, Boschi S et al. 68 Ga-citrate PET/CT for evaluating patients with infections of the bone: preliminary results. J Nucl Med 2010; 51: 1932-1936.
78. Glaudemans AW. Nuclear medicine strategies to image infectious and inflammatory diseases. 2-12-2014. University of Groningen. Ref Type: Thesis/Dissertation Available at http://irs.ub.rug.nl/ppn/371114721. Last accessed 16 March 2015.
79. Bus SA, Hazenberg CE, Klein M, van Baal JG. Assessment of foot disease in the home environment of diabetic patients using a new photographic foot imaging device. J Med Eng Technol 2010; 34: 43-50.
80. Armstrong DG, Holtz-Neiderer K, Wendel C, Mohler MJ, Kimbriel HR, Lavery LA. Skin temperature monitoring reduces the risk for diabetic foot ulceration in high-risk patients. Am J Med 2007; 120: 1042-1046.
81. van Netten JJ, van Baal JG, Liu C, van der HF, Bus SA. Infrared thermal imaging for automated detection of diabetic foot complications. J Diabetes Sci Technol 2013; 7: 1122-1129.
82. Oe M, Yotsu RR, Sanada H, Nagase T, Tamaki T. Thermographic findings in a case of type 2 diabetes with foot ulcer and osteomyelitis. J Wound Care 2012; 21: 276-274.
83. Hazenberg CE, van Netten JJ, van Baal SG, Bus SA. Assessment of signs of foot infection in diabetes patients using photographic foot imaging and infrared thermography. Diabetes Technol Ther 2014; 16: 370-377.