Detection of osteomyelitis in the diabetic foot by imaging techniques: a systematic review and meta-analysis comparing MRI, white blood cell scintigraphy, and FDG-PET.
Open accessAbstract
OBJECTIVE Diagnosing bone infection in the diabetic foot is challenging and often requires several diagnostic procedures, including advanced imaging. We compared the diagnostic performances of MRI, radiolabeled white blood cell (WBC) scintigraphy (either with 99mTc-hexamethylpropyleneamineoxime [HMPAO] or 111In-oxine), and [18F]fluorodeoxyglucose positron emission tomography (18F-FDG–PET)/computed tomography. RESEARCH DESIGN AND METHODS We searched Medline and Embase as of August 2016 for studies of diagnostic tests on patients known or suspected to have diabetes and a foot infection. We performed a systematic review using criteria recommended by the Cochrane Review of a database that included prospective and retrospective diagnostic studies performed on patients with diabetes in whom there was a clinical suspicion of osteomyelitis of the foot. The preferred reference standard was bone biopsy and subsequent pathological (or microbiological) examination. RESULTS Our review found 6,649 articles; 3,894 in Medline and 2,755 in Embase. A total of 27 full articles and 2 posters was selected for inclusion in the analysis. The performance characteristics for the 18F-FDG–PET were: sensitivity, 89%; specificity, 92%; diagnostic odds ratio (DOR), 95; positive likelihood ratio (LR), 11; and negative LR, 0.11. For WBC scan with 111In-oxine, the values were: sensitivity, 92%; specificity, 75%; DOR, 34; positive LR, 3.6; and negative LR, 0.1. For WBC scan with 99mTc-HMPAO, the values were: sensitivity, 91%; specificity, 92%; DOR, 118; positive LR, 12; and negative LR, 0.1. Finally, for MRI, the values were: sensitivity, 93%; specificity, 75%; DOR, 37; positive LR, 3.66, and negative LR, 0.10. CONCLUSIONS The various modalities have similar sensitivity, but 18F-FDG–PET and 99mTc-HMPAO–labeled WBC scintigraphy offer the highest specificity. Larger prospective studies with a direct comparison among the different imaging techniques are required.
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Numerous vascular classifications exist but focus on the degree of ischemia without consideration of tissue loss or infection until the latest stages.
“Similarly, numerous vascular classifications exist but focus on the degree of ischemia without consideration of tissue loss or infection until the latest stages.38”
From Diabetic Foot Ulcers (2023) · cites this paper as [38]
The Eligible Studies section describes a review of imaging tests for diabetic foot osteomyelitis, not vascular classification systems. Searches for vascular classifications, ischemia, tissue loss, and disease stages found no passage in our copy addressing the claim. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThe Wound, Ischemia, Foot Infection (WIfI) classification system was developed and validated as a method to combine wound, ischemia, and foot infection and to accurately assess the risk of limb loss for patients with diabetic foot ulcers.
“TheWound, Ischemia, Foot Infection (WIfI) classification system was developed and validated as a method to combine all 3 variables (wound, ischemia, and foot infection)and to accurately assess the risk of limb loss for patients with diabetic foot ulcers.38,39”
From Diabetic Foot Ulcers (2023) · cites this paper as [38]
The Abstract discusses diabetic foot infection, osteomyelitis, and amputation, while the Methods assess imaging tests for osteomyelitis. Searches for WIfI and for a classification predicting limb loss found no passage about the system’s development, validation, or predictive accuracy; no page numbers are available in our copy. (LLM, conf=0.77)
Experimental — accuracy not yet measuredA higher score on the WIfI scale is associated with lower extremity amputation and morbidity.
“a A higher score on the WIfI scale 38 is associated with lower extremity amputation and morbidity and can be used to determine the need for revascularization.”
From Diabetic Foot Ulcers (2023) · cites this paper as [38]
The Abstract discusses diabetic foot osteomyelitis and lower-extremity amputation, but does not discuss WIfI scores or their association with amputation or morbidity. Searches for WIfI scoring and revascularization found no passage addressing the claim. (LLM, conf=0.76)
Experimental — accuracy not yet measured
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Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042 · see citing works
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Quantifying heterogeneity in a meta‐analysis
Higgins, J. P. T., & Thompson, S. G. (2002) · Statistics in Medicine · doi:10.1002/sim.1186 · Cited by 36,763 · see citing works
QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies
Whiting, P. F., Rutjes, A. W. S., Westwood, M. E., Mallett, S., Deeks, J. J., Reitsma, J. B., Leeflang, M. M. G., Sterne, J. A. C., Bossuyt, P. M. M., & the QUADAS-2 Group* (2011) · Annals of Internal Medicine · doi:10.7326/0003-4819-155-8-201110180-00009 · Cited by 14,199 · see citing works
Global epidemiology of diabetic foot ulceration: a systematic review and meta-analysis
Zhang, P., Lü, J., Jing, Y., Tang, S., Zhu, D., & Bi, Y. (2016) · Annals of Medicine · doi:10.1080/07853890.2016.1231932 · Cited by 1,869 · see citing works
Lipsky, B. A., Berendt, A. R., Cornia, P. B., Pile, J. C., Peters, E. J. G., Armstrong, D. G., Deery, H. G., Embil, J. M., Joseph, W. S., Karchmer, A. W., et al. (2012) · Clinical Infectious Diseases · doi:10.1093/cid/cis346 · Cited by 1,771 · see citing works
Self-citationPrompers, L., Huijberts, M., Apelqvist, J., Jude, E., Piaggesi, A., Bakker, K., Edmonds, M., Holstein, P., Jirkovska, A., Mauricio, D., et al. (2007) · Diabetologia · doi:10.1007/s00125-006-0491-1 · Cited by 1,023 · see citing works
Risk Factors for Foot Infections in Individuals With Diabetes
Lavery, L. A., Armstrong, D. G., Wunderlich, R. P., Mohler, M. J., Wendel, C. S., & Lipsky, B. A. (2006) · Diabetes Care · doi:10.2337/dc05-2425 · Cited by 791 · see citing works
Self-citationIWGDF guidance on the diagnosis and management of foot infections in persons with diabetes
Lipsky, B. A., Aragón‐Sánchez, J., Diggle, M. A., Embil, J. M., Kono, S., Lavery, L. A., Senneville, É., Urbančič‐Rovan, V., van Asten, S. A. V., & on behalf of the International Working Group on the Diabetic Foot (IWGDF) (2015) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2699 · Cited by 566 · see citing works
Self-citationOsteomyelitis of the Foot in Diabetic Patients
Lipsky, B. A. (1997) · Clinical Infectious Diseases · doi:10.1086/516148 · Cited by 363 · see citing works
Self-citationNewman, L. G. (1991) · JAMA · doi:10.1001/jama.266.9.1246 · Cited by 331 · see citing works
Diabetic foot osteomyelitis: a progress report on diagnosis and a systematic review of treatment
Berendt, A. R., Peters, E. J. G., Bakker, K., Embil, J. M., Eneroth, M., Hinchliffe, R. J., Jeffcoate, W. J., Lipsky, B. A., Senneville, É., Teh, J. L., et al. (2008) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.836 · Cited by 318 · see citing works
Self-citationUnsuspected Osteomyelitis in Diabetic Foot Ulcers
Newman, L. G. (1991) · JAMA · doi:10.1001/jama.1991.03470090080036 · Cited by 278 · see citing works
Magnetic Resonance Imaging for Diagnosing Foot Osteomyelitis
Kapoor, A. (2007) · Archives of Internal Medicine · doi:10.1001/archinte.167.2.125 · Cited by 227 · see citing works
Yuh, W., Corson, J., Hm, B., et al. (1989) · American Journal of Roentgenology · doi:10.2214/ajr.152.4.795 · Cited by 190 · see citing works
Nawaz, A., Torigian, D. A., Siegelman, E. S., Basu, S. K., Chryssikos, T. J., & Alavi, A. A. (2009) · Molecular Imaging and Biology · doi:10.1007/s11307-009-0268-2 · Cited by 171 · see citing works
Diabetic foot ulcer severity predicts mortality among veterans with type 2 diabetes.
Brennan, M. B., Hess, T. M., Bartle, B., Cooper, J. M., Kang, J., Huang, E. S., Smith, M., Sohn, M.-W., & Crnich, C. (2017) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2016.11.020 · Cited by 166 · see citing works
The diabetic foot: initial experience with 18F-FDG PET/CT.
Keidar, Z., Militianu, D., Melamed, E. A., et al. (2005) · PubMed · Cited by 149 · see citing works
Rabkin, Z., Israel, O., & Keidar, Z. (2010) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.074294 · Cited by 142 · see citing works
The diabetic foot in 2015: an overview
Markakis, K., Bowling, F. L., & Boulton, A. J. M. (2015) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2740 · Cited by 135 · see citing works
Nuclear Medicine and Diabetic Foot Infections
Palestro, C. J., & Love, C. (2008) · Seminars in Nuclear Medicine · doi:10.1053/j.semnuclmed.2008.08.006 · Cited by 133 · see citing works
Diagnosis of Pedal Osteomyelitis in Diabetic Patients Using Current Scintigraphic Techniques
Keenan, A. M. (1989) · Archives of Internal Medicine · doi:10.1001/archinte.1989.00390100078019 · Cited by 132 · see citing works
Lam, K., van Asten, S. A. V., Nguyen, T., Fontaine, J. L., & Lavery, L. A. (2016) · Clinical Infectious Diseases · doi:10.1093/cid/ciw445 · Cited by 129 · see citing works
The Diabetic Foot: Initial Experience With 18F-FDG PET/CT
Dalinka, M. K. (2006) · Yearbook of Diagnostic Radiology · doi:10.1016/s0098-1672(08)70330-8 · Cited by 123 · see citing works
Glaudemans, A. W. J. M., de Vries, E. F. J., Vermeulen, L. E. M., et al. (2013) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-013-2481-0 · Cited by 114 · see citing works
Self-citationRole of magnetic resonance imaging in the diagnosis of osteomyelitis in diabetic foot infections
Croll, S. D., Nicholas, G. G., Osborne, M. A., et al. (1996) · Journal of Vascular Surgery · doi:10.1016/s0741-5214(96)70102-7 · Cited by 114 · see citing works
Johnson, J. E., Kennedy, E., Shereff, M. J., et al. (1996) · Foot & Ankle International · doi:10.1177/107110079601700103 · Cited by 109 · see citing works
Enderle, M. D., Coerper, S., Schweizer, H. P., et al. (1999) · Diabetes Care · doi:10.2337/diacare.22.2.294 · Cited by 104 · see citing works
Diabetic Foot Infection: Usefulness of SPECT/CT for 99mTc-HMPAO-Labeled Leukocyte Imaging
Filippi, L., Uccioli, L., Giurato, L., et al. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.059493 · Cited by 104 · see citing works
Infection in diabetic osteoarthropathy: use of indium-labeled leukocytes for diagnosis.
Maurer, A. H., Millmond, S. H., Knight, L. C., et al. (1986) · Radiology · doi:10.1148/radiology.161.1.3763871 · Cited by 103 · see citing works
Erba, P. A., Glaudemans, A. W. J. M., Veltman, N. C., et al. (2013) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-013-2631-4 · Cited by 101 · see citing works
Self-citationDiagnosis of osteomyelitis of the foot in diabetic patients: value of 111In-leukocyte scintigraphy.
Larcos, G., Brown, M. L., & Sutton, R. T. (1991) · American Journal of Roentgenology · doi:10.2214/ajr.157.3.1872240 · Cited by 98 · see citing works
Ertuğrul, B., Baktıroğlu, S., Salman, S., et al. (2006) · Diabetic Medicine · doi:10.1111/j.1464-5491.2006.01887.x · Cited by 98 · see citing works
FDG PET/CT imaging in the diagnosis of osteomyelitis in the diabetic foot
Kagna, O., Srour, S., Melamed, E. A., et al. (2012) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-012-2183-z · Cited by 91 · see citing works
Treglia, G., Sadeghi, R., Annunziata, S., et al. (2013) · The Foot · doi:10.1016/j.foot.2013.07.002 · Cited by 91 · see citing works
Can Sequential18F-FDG PET/CT Replace WBC Imaging in the Diabetic Foot?
Familiari, D., Glaudemans, A. W. J. M., Vitale, V., et al. (2011) · Journal of Nuclear Medicine · doi:10.2967/jnumed.110.082222 · Cited by 91 · see citing works
Self-citationNewman, L. G., Waller, J. D., Palestro, C. J., et al. (1992) · Diabetes Care · doi:10.2337/diacare.15.11.1527 · Cited by 80 · see citing works
Ertuğrul, B., Lipsky, B. A., & Şavk, Ö. (2013) · Diabetic Foot & Ankle · doi:10.3402/dfa.v4i0.21855 · Cited by 79 · see citing works
Self-citationLevine, S. E., Neagle, C. E., Esterhai, J. L., et al. (1994) · Foot & Ankle International · doi:10.1177/107110079401500311 · Cited by 73 · see citing works
Devillers, A., Moisan, A., Hennion, F., et al. (1998) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s002590050205 · Cited by 70 · see citing works
Harwood, S. J., Valdivia, S., HUNG, G.-L., et al. (1999) · Clinical Infectious Diseases · doi:10.1086/514791 · Cited by 70 · see citing works
Palestro, C. J., Caprioli, R., Love, C., et al. (2003) · The Journal of Foot & Ankle Surgery · doi:10.1053/jfas.2003.0420001 · Cited by 65 · see citing works
van Asten, S. A. V., Jupiter, D. C., Mithani, M., et al. (2016) · International Wound Journal · doi:10.1111/iwj.12574 · Cited by 55 · see citing works
Charcot Neuropathic Arthropathy of the Foot: A Literature Review and Single-Center Experience
Kučera, T., Shaikh, H. H., & Šponer, P. (2016) · Journal of Diabetes Research · doi:10.1155/2016/3207043 · Cited by 54 · see citing works
Magnetic resonance imaging in the management of diabetic foot infection
Cook, T. A., Rahim, N. I., Simpson, H. C. R., et al. (1996) · British journal of surgery · doi:10.1046/j.1365-2168.1996.02244.x · Cited by 51 · see citing works
Technetium-99-labeled leukocytes in diagnosing diabetic osteomyelitis in the foot
Harvey, J., & Cohen, M. M. (1997) · The Journal of Foot & Ankle Surgery · doi:10.1016/s1067-2516(97)80117-2 · Cited by 50 · see citing works
Delcourt, A., Huglo, D. G., Prangère, T., Benticha, H., Devemy, F., Tsirtsikoulou, D., Lepeut, M., Fontaine, P., & Steinling, M. (2005) · Diabetes & Metabolism · doi:10.1016/s1262-3636(07)70178-7 · Cited by 50 · see citing works
Lazaga, F., van Asten, S. A. V., Nichols, A., et al. (2015) · International Wound Journal · doi:10.1111/iwj.12433 · Cited by 44 · see citing works
Vesco, L., Boulahdour, H., Hamissa, S., et al. (1999) · Metabolism · doi:10.1016/s0026-0495(99)90230-5 · Cited by 44 · see citing works
DIAGNOSIS OF OSTEOMYELITIS IN NEUROPATHIC FOOT ULCERS
Crerand, S., Dolan, M., Laing, P., et al. (1996) · Journal of Bone and Joint Surgery - British Volume · doi:10.1302/0301-620x.78b1.0780051 · Cited by 40 · see citing works
Fontaine, J. L., Bhavan, K., Lam, K., et al. (2016) · PubMed · Cited by 38 · see citing works
Ünal, S. N., Birinci, H., Baktıroğlu, S., et al. (2001) · Clinical Nuclear Medicine · doi:10.1097/00003072-200112000-00005 · Cited by 37 · see citing works
99mTc-Nanocolloid scintigraphy for assessing osteomyelitis in diabetic neuropathic feet
Remedios, D., Valabhji, J., Oelbaum, R., et al. (1998) · Clinical Radiology · doi:10.1016/s0009-9260(98)80058-5 · Cited by 32 · see citing works
Diagnosis of osteomyelitis in neuropathic foot ulcers.
Crerand, S., Dolan, M., Laing, P., et al. (1996) · PubMed · Cited by 30 · see citing works
Yang, H., Zhuang, H., Rubello, D., & Alavi, A. A. (2015) · Nuclear Medicine Communications · doi:10.1097/mnm.0000000000000434 · Cited by 30 · see citing works
Magnetic resonance imaging in the management of diabetic foot infection
Cook, T. A., Rahim, N. I., Simpson, H. C. R., et al. (1996) · British journal of surgery · doi:10.1002/bjs.1800830231 · Cited by 28 · see citing works
Shagos, G., shanmugasundaram, P., Varma, A. K., et al. (2015) · Indian Journal of Nuclear Medicine · doi:10.4103/0972-3919.152946 · Cited by 26 · see citing works
Combined Leukocyte and Bone Imaging Used to Evaluate Diabetic Osteoarthropathy and Osteomyelitis
SPLITTGERBER, G. F., Spiegelhoff, D. R., & Buggy, B. P. (1989) · Clinical Nuclear Medicine · doi:10.1097/00003072-198903000-00002 · Cited by 25 · see citing works
Diagnosing diabetic foot infection: the role of imaging and a proposed flow chart for assessment.
Israel, O., Sconfienza, L. M., & Lipsky, B. A. (2014) · PubMed · Cited by 23 · see citing works
Self-citationThe Diabetic Charcot Foot from 1936 to 2016
Ramanujam, C. L., & Zgonis, T. (2016) · Clinics in Podiatric Medicine and Surgery · doi:10.1016/j.cpm.2016.07.001 · Cited by 23 · see citing works
Przybylski, M., Holloway, S., Vyce, S. D., & Obando, A. (2014) · International Wound Journal · doi:10.1111/iwj.12316 · Cited by 20 · see citing works
Knešaurek, K., Kolker, D., Vatti, S., et al. (2015) · PubMed · Cited by 8 · see citing works
The detection of pedal osteomyelitis in diabetic patients
Kearney, T., Robinson, S., Elkeles, R., et al. (1999) · Practical Diabetes · doi:10.1002/pdi.1960160404 · Cited by 7 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Enderle MD, Coerper S, Schweizer HP, et al. Correlation of imaging techniques to histopathol- ogy in patients with diabetic foot syndrome and clinical suspicion of chronic osteomyelitis. Diabe- tes Care 1999;22:294-299
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Armstrong, D. G., Tan, T.-W., Boulton, A. J. M., & Bus, S. A. (2023) · JAMA · doi:10.1001/jama.2023.10578 · Cited by 1,658 · see citing works
- Authors
- Lauri, C., Tamminga, M., Glaudemans, A. W. J. M., Juárez Orozco, L. E., Erba, P. A., Jutte, P. C., Lipsky, B. A., IJzerman, M. J., Signore, A., & Slart, R. H. J. A.
- Affiliations
- University Medical Center Groningen (NL)
- Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands
- University of Pisa (IT)
- University of Washington (US)
- University of Twente (NL)
- Corresponding author
- Slart, Riemer H.J.A.
- ORCID
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2017-07-11
- Volume
- 40
- Issue
- 8
- Pages
- 1111-1120
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2738855391
- Cited by
- 163
- References
- 65
- Citations by year
- 2026: 12 · 2025: 18 · 2024: 25 · 2023: 15 · 2022: 21 · 2021: 22 · 2020: 18 · 2019: 16 · 2018: 13 · 2017: 2 · 2015: 1
- FWCI
- 1.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- University of Twente Research Information (publishedVersion, other-oa)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, other-oa)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- University of Twente Research Information (submittedVersion, other-oa)
- Funders
- University Medical Center Groningen
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetic Foot Ulcer Assessment and Management
- Health Sciences › Medicine › Surgery › Orthopedic Infections and Treatments
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Foot and Ankle Surgery
- Keywords
- osteomyelitis, diabetic foot, bone infection, magnetic resonance imaging, white blood cell scintigraphy, FDG-PET, 99mTc-HMPAO, 111In-oxine, diagnostic accuracy, sensitivity and specificity, diagnostic imaging comparison, diabetes complications
- MeSH terms
- Bone and Bones, Humans, Leukocytes, Magnetic Resonance Imaging, Osteomyelitis, Radionuclide Imaging, Sensitivity and Specificity, Databases, Factual, Diabetic Foot, Positron-Emission Tomography
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