Imaging Osteomyelitis: An Update

Abstract

Background Hematogenous osteomyelitis has increased over the past quarter century in frequency, virulence, and degree of soft-tissue involvement, bringing about changes in clinical manifestations and management of the disease especially in children that should be reflected in the current imaging approach. Likewise, the global disease burden of diabetes has increased greatly in the same period, compounding the problem of ascertaining osteomyelitis in diabetic foot.

Method This article provides an updated overview of imaging findings in hematogenous and contiguous osteomyelitis based on the literature and our institutional experience, along with salient features of recent recommendations from expert groups on the diagnostic algorithms and reporting terminology.

Results and Conclusion Findings on radiography and especially magnetic resonance imaging (MRI) closely reflect pathophysiology in osteomyelitis, whereby the characteristic involvement of the metaphysis or metaphyseal-equivalents, the formation and subperiosteal extension of intramedullary pus collection, and the development of cloaca, sequestrum, and involucrum are all diagnostic clues. Non-enhancing foci within the medullary bone, the penumbra sign, intra- or extramedullary fat globules, and surrounding soft tissue inflammation or abscesses are among key MRI findings. Diabetic foot is a special condition with characteristic pathophysiologic and imaging features that suggest the likelihood of osteomyelitis and the main differential diagnostic consideration of acute on chronic neuropathic osteoarthropathy with or without osteomyelitis.

Key Points 

• Imaging closely reflects pathophysiology in hematogenous osteomyelitis.

• Acute hematogenous osteomyelitis predominantly involves metaphyses and metaphyseal equivalent sites.

• MRI clues for hematogenous osteomyelitis include central marrow non-enhancement, intra- or extramedullary fat globules, and the “penumbra” sign.

• An increased fluid-sensitive MRI bone signal abutting a soft tissue ulcer, abscess, or sinus tract suggests a high probability of contact osteomyelitis.

Citation Format

• Aydingoz U, Imaging Osteomyelitis: An Update. Fortschr Röntgenstr 2023; 195: 297 – 308

Zusammenfassung

Hintergrund Die hämatogene Osteomyelitis hat im letzten Vierteljahrhundert in Bezug auf Häufigkeit, Virulenz und Grad der Weichteilbeteiligung zugenommen, was insbesondere bei Kindern zu Veränderungen bei den klinischen Manifestationen und der Behandlung der Krankheit geführt hat. Dies sollte sich im aktuellen bildgebenden Ansatz widerspiegeln. Ebenso hat die globale Krankheitslast von Diabetes im gleichen Zeitraum stark zugenommen, was das Problem der Diagnostik der Osteomyelitis beim diabetischen Fuß noch verschärft.

Methode Dieser Artikel gibt, basierend auf der Literatur und unserer institutionellen Erfahrung, einen aktualisierten Überblick über die bildgebenden Befunde bei hämatogener und konsekutiver Osteomyelitis, sowie über die auffälligsten Merkmale nach den aktuellsten Empfehlungen von Expertengruppen zu diagnostischen Algorithmen und Befundterminologie.

Ergebnisse und Schlussfolgerungen Das Röntgenbild und insbesondere die Befunde der Magnetresonanztomografie (MRT) spiegeln die Pathophysiologie der Osteomyelitis sehr gut wider. Diagnostische Hinweise sind in diesem Fall die charakteristische Beteiligung der Metaphyse oder metaphysärer Äquivalente, die Bildung und subperiostale Ausdehnung intramedullärer Eiteransammlungen und die Entwicklung von Kloake, Sequester und Involucrum. Zu den wichtigsten MRT-Befunden gehören Herde mit Nicht-Enhancement innerhalb des Markraums, das Penumbra-Zeichen, intra- oder extramedulläre Fettkügelchen und Entzündung der umgebenden Weichteile oder Abszesse. Der diabetische Fuß ist ein spezielles Krankheitsbild mit charakteristischen pathophysiologischen und bildgebenden Merkmalen, die auf eine Osteomyelitis hindeuten und differentialdiagnostisch in erster Linie an eine akute oder chronische neuropathische Osteoarthropathie mit oder ohne Osteomyelitis denken lassen.

Kernaussagen

• Die Bildgebung spiegelt die Pathophysiologie der hämatogenen Osteomyelitis genau wider.

• Die akute hämatogene Osteomyelitis betrifft überwiegend Metaphysen und metaphysäre Äquivalente.

• MRT-Anhaltspunkte für eine hämatogene Osteomyelitis sind Nicht-Enhancement des zentralen Knochenmarks, intra- oder extramedulläre Fettkügelchen und das Penumbra-Zeichen.

• Ein erhöhtes flüssigkeitssensitives MRT-Knochensignal, das an ein Weichteilgeschwür, einen Abszess oder einen Sinustrakt angrenzt, spricht mit hoher Wahrscheinlichkeit für eine Kontakt-Osteomyelitis.

Key words

bones - infection - MR imaging

Publication History

Received: 15 June 2022

Accepted: 12 September 2022

Article published online:
01 February 2023

• References

• 1 Jaramillo D, Dormans JP, Delgado J. et al. Hematogenous Osteomyelitis in Infants and Children: Imaging of a Changing Disease. Radiology 2017; 283: 629-643
• 2 Crim J, Salmon S, Waranch C. et al. Update on MRI findings of osteomyelitis of long bones in the adult population. Skeletal Radiol 2022;
• 3 McNeil JC, Forbes AR, Vallejo JG. et al. Role of Operative or Interventional Radiology-Guided Cultures for Osteomyelitis. Pediatrics 2016; 137: e20154616
• 4 Wu JS, Gorbachova T, Morrison WB. et al. Imaging-guided bone biopsy for osteomyelitis: are there factors associated with positive or negative cultures?. Am J Roentgenol 2007; 188: 1529-1534
• 5 Said N, Chalian M, Fox MG. et al. Percutaneous image-guided bone biopsy of osteomyelitis in the foot and pelvis has a low impact on guiding antibiotics management: a retrospective analysis of 60 bone biopsies. Skeletal Radiol 2019; 48: 1385-1391
• 6 Hoffer FA, Emans J. Percutaneous drainage of subperiosteal abscess: a potential treatment for osteomyelitis. Pediatr Radiol 1996; 26: 879-881
• 7 Montgomery CO, Porter 3rd A, Sachleben B. et al. Treatment of subperiosteal abscesses in children: is drainage of the intramedullary canal required?. J Pediatr Orthop B 2017; 26: 497-500
• 8 Lin X, Xu Y, Pan X. et al. Global, regional, and national burden and trend of diabetes in 195 countries and territories: an analysis from 1990 to 2025. Sci Rep 2020; 10: 14790
• 9 Gilbertson-Dahdal D, Wright JE, Krupinski E. et al. Transphyseal involvement of pyogenic osteomyelitis is considerably more common than classically taught. Am J Roentgenol 2014; 203: 190-195
• 10 American College of Radiology. ACR Appropriateness Criteria® Suspected Osteomyelitis, Septic Arthritis, or Soft Tissue Infection (Excluding Spine and Diabetic Foot). Accessed June 08, 2022 at: https://acsearch.acr.org/docs/3094201/Narrative
• 11 Shet NS, Iyer RS, Chan SS. Expert Panel on Pediatric Imaging. et al. ACR Appropriateness Criteria Osteomyelitis or Septic Arthritis-Child (Excluding Axial Skeleton). J Am Coll Radiol 2022; 19: S121-S136
• 12 Glaudemans AWJM, Jutte PC, Cataldo MA. et al. Consensus document for the diagnosis of peripheral bone infection in adults: a joint paper by the EANM, EBJIS, and ESR (with ESCMID endorsement). Eur J Nucl Med Mol Imaging 2019; 46: 957-970
• 13 Alaia EF, Chhabra A, Simpfendorfer CS. et al. MRI nomenclature for musculoskeletal infection. Skeletal Radiol 2021; 50: 2319-2347
• 14 Peltola H, Pääkkönen M. Acute osteomyelitis in children. N Engl J Med 2014; 370: 352-360
• 15 Nixon GW. Hematogenous osteomyelitis of metaphyseal-equivalent locations. Am J Roentgenol 1978; 130: 123-129
• 16 Aydıngöz Ü, Yıldız AE, Ergen FB. Zero echo-time (ZTE) imaging in musculoskeletal MRI: technique, optimization, applications, and pitfalls. RadioGraphics 2022; 42: 1398-1414
• 17 Connolly SA, Connolly LP, Drubach LA. et al. MRI for detection of abscess in acute osteomyelitis of the pelvis in children. Am J Roentgenol 2007; 189: 867-872
• 18 Resnick D, Kransdorf MJ. Bone and joint imaging. 3rd ed.. Philadelphia Pa: Elsevier Saunders; 2005: 715
• 19 May DA, Morrison WB, Belair JA. Musculoskeletal imaging. Philadelphia, USA: Elsevier; 2022: 617-618
• 20 Ceroni D, Belaieff W, Cherkaoui A. et al. Primary epiphyseal or apophyseal subacute osteomyelitis in the pediatric population: a report of fourteen cases and a systematic review of the literature. J Bone Joint Surg Am 2014; 96: 1570-1575
• 21 Schmitt SK. Osteomyelitis. Infect Dis Clin North Am 2017; 31: 325-338
• 22 Liu C, Bayer A, Cosgrove SE. et al. Infectious Diseases Society of America. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis 2011; 52: e18-e55
• 23 Karmazyn B. Imaging approach to acute hematogenous osteomyelitis in children: an update. Semin Ultrasound CT MR 2010; 31: 100-106
• 24 Llewellyn A, Jones-Diette J, Kraft J. et al. Imaging tests for the detection of osteomyelitis: a systematic review. Health Technol Assess 2019; 23: 1-128
• 25 Averill LW, Hernandez A, Gonzalez L. et al. Diagnosis of osteomyelitis in children: utility of fat-suppressed contrast-enhanced MRI. Am J Roentgenol 2009; 192: 1232-1238
• 26 Kan JH, Young RS, Yu C. et al. Clinical impact of gadolinium in the MRI diagnosis of musculoskeletal infection in children. Pediatr Radiol 2010; 40: 1197-1205
• 27 Grey AC, Davies AM, Mangham DC. et al. The “penumbra sign” on T1-weighted MR imaging in subacute osteomyelitis: frequency, cause and significance. Clin Radiol 1998; 53: 587-592
• 28 Davies AM, Grimer R. The penumbra sign in subacute osteomyelitis. Eur Radiol 2005; 15: 1268-1270
• 29 Singh J, Rajakulasingam R, Saifuddin A. Langerhans cell histiocytosis of the shoulder girdle, pelvis and extremities: a review of radiographic and MRI features in 85 cases. Skeletal Radiol 2020; 49: 1925-1937
• 30 Davies AM, Hughes DE, Grimer RJ. Intramedullary and extramedullary fat globules on magnetic resonance imaging as a diagnostic sign for osteomyelitis. Eur Radiol 2005; 15: 2194-2199
• 31 Wong A, Grando H, Fliszar E. et al. Intramedullary fat globules related to bone trauma: a new MR imaging finding. Skeletal Radiol 2014; 43: 1713-1719
• 32 Hui CL, Naidoo P. Extramedullary fat fluid level on MRI as a specific sign for osteomyelitis. Australas Radiol 2003; 47: 443-446
• 33 Kumar J, Bandhu S, Kumar A. et al. Extra-osseous fat fluid level: a specific sign for osteomyelitis. Skeletal Radiol 2007; 36 (Suppl. 01) S101-S104
• 34 Blacksin MF, Finzel KC, Benevenia J. Osteomyelitis originating in and around bone infarcts: giant sequestrum phenomena. Am J Roentgenol 2001; 176: 387-391
• 35 Kasalak Ö, Overbosch J, Adams HJ. et al. Diagnostic value of MRI signs in differentiating Ewing sarcoma from osteomyelitis. Acta Radiol 2019; 60: 204-212
• 36 Henninger B, Glodny B, Rudisch A. et al. Ewing sarcoma versus osteomyelitis: differential diagnosis with magnetic resonance imaging. Skeletal Radiol 2013; 42: 1097-1104
• 37 McCarville MB, Chen JY, Coleman JL. et al. Distinguishing osteomyelitis from Ewing sarcoma on radiography and MRI. Am J Roentgenol 2015; 205: 640-650
• 38 Samet J, Weinstein J, Fayad LM. MRI and clinical features of Langerhans cell histiocytosis (LCH) in the pelvis and extremities: can LCH really look like anything?. Skeletal Radiol 2016; 45: 607-613
• 39 Song YS, Lee IS, Yi JH. et al. Radiologic findings of adult pelvis and appendicular skeletal Langerhans cell histiocytosis in nine patients. Skeletal Radiol 2011; 40: 1421-1426
• 40 French J, Epelman M, Jaramillo D. et al. Magnetic resonance imaging evaluation of osteoid osteoma: utility of the dark rim sign. Pediatr Radiol 2020; 50: 1742-1750
• 41 Aydıngöz Ü, Yıldız AE. MRI in the Diagnosis and Treatment Response Assessment of Chronic Nonbacterial Osteomyelitis in Children and Adolescents. Curr Rheumatol Rep 2022; 24: 27-39
• 42 Reiser C, Klotsche J, Hospach A. et al. First-year follow-up of children with chronic nonbacterial osteomyelitis-an analysis of the German National Pediatric Rheumatologic Database from 2009 to 2018. Arthritis Res Ther 2021; 23: 281
• 43 Labbé JL, Peres O, Leclair O. et al. Acute osteomyelitis in children: the pathogenesis revisited?. Orthop Traumatol Surg Res 2010; 96: 268-275
• 44 Girschick H, Finetti M, Orlando F. et al. The multifaceted presentation of chronic recurrent multifocal osteomyelitis: a series of 486 cases from the Eurofever international registry. Rheumatology (Oxford) 2018; 57: 1203-1211
• 45 Sato TS, Watal P, Ferguson PJ. Imaging mimics of chronic recurrent multifocal osteomyelitis: avoiding pitfalls in a diagnosis of exclusion. Pediatr Radiol 2020; 50: 124-136
• 46 Llewellyn A, Kraft J, Holton C. et al. Imaging for detection of osteomyelitis in people with diabetic foot ulcers: A systematic review and meta-analysis. Eur J Radiol 2020; 131: 109215
• 47 Walker EA, Beaman FD, Wessell DE. Expert Panel on Musculoskeletal Imaging. et al. ACR Appropriateness Criteria® Suspected Osteomyelitis of the Foot in Patients With Diabetes Mellitus. J Am Coll Radiol 2019; 16: S440-S450
• 48 Collins MS, Schaar MM, Wenger DE. et al. T1-weighted MRI characteristics of pedal osteomyelitis. Am J Roentgenol 2005; 185: 386-393
• 49 Ahmadi ME, Morrison WB, Carrino JA. et al. Neuropathic arthropathy of the foot with and without superimposed osteomyelitis: MR imaging characteristics. Radiology 2006; 238: 622-631
• 50 Rosskopf AB, Loupatatzis C, Pfirrmann CWA. et al. The Charcot foot: a pictorial review.  Insights Imaging 2019; 10: 77
• 51 Donovan A, Schweitzer ME. Current concepts in imaging diabetic pedal osteomyelitis. Radiol Clin North Am 2008; 46: 1105-1124