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Radiologic Mimics of Osteomyelitis and Septic Arthritis: A Pictorial Essay

Radiologic Mimics of Osteomyelitis and Septic Arthritis: A Pictorial Essay Hindawi Radiology Research and Practice Volume 2021, Article ID 9912257, 18 pages https://doi.org/10.1155/2021/9912257 Review Article Radiologic Mimics of Osteomyelitis and Septic Arthritis: A Pictorial Essay 1,2 1,2,3 1,4 Wanyin Lim , Christen D. Barras, and Steven Zadow Dr Jones and Partners Medical Imaging, Adelaide, South Australia, Australia Department of Radiology, Royal Adelaide Hospital, Adelaide, South Australia, Australia South Australian Health and Medical Research Institute and the University of Adelaide, Adelaide, South Australia, Australia Flinders Medical Centre, Bedford Park, South Australia, Australia Correspondence should be addressed to Wanyin Lim; ynyn146@gmail.com Received 17 March 2021; Revised 12 May 2021; Accepted 18 May 2021; Published 24 May 2021 Academic Editor: Andre´ Luiz Ferreira COSTA Copyright © 2021 Wanyin Lim et al. -is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Various imaging techniques may be employed in the investigation of suspected bone and joint infections. -ese include ul- trasound, radiography, functional imaging such as positron emission tomography (PET) and nuclear scintigraphy, and cross- sectional imaging, including computed tomography (CT) and magnetic resonance imaging (MRI). -e cross-sectional modalities represent the imaging workhorse in routine practice. -e role of imaging also extends to include assessment of the anatomical extent of infection, potentially associated complications, and treatment response. -e imaging appearances of bone and joint infections are heterogeneous and depend on the duration of infection, an individual patient’s immune status, and virulence of culprit organisms. To add to the complexity of radiodiagnosis, one of the pitfalls of imaging musculoskeletal infection is the presence of other conditions that can share overlapping imaging features. -is includes osteoarthritis, vasculopathy, inflam- matory, and even neoplastic processes. Different pathologies may also coexist, for example, diabetic neuropathy and osteomyelitis. -is pictorial review aims to highlight potential mimics of osteomyelitis and septic arthritis that are regularly encountered, with emphasis on specific imaging features that may aid the radiologist and clinician in distinguishing an infective from a noninfective aetiology. ultrasound, computed tomography (CT), and functional 1. Introduction studies including nuclear scintigraphy, white cell scan, and Osteomyelitis is defined as bone inflammation due to in- positron emission tomography (PET). Magnetic resonance fection whilst septic arthritis is defined by infection within a imaging (MRI), being moderately sensitive and specific, is joint [1]. Bone and joint infections have a variable clinical the imaging modality of choice in the evaluation of sus- presentation ranging from acute sepsis to insidious onset of pected osteomyelitis [3, 4]. pain, with or without fever. Laboratory results such as white Understandably, given the heterogeneity of clinical presentations, imaging appearances of infection also vary cell count, C-reactive protein, and erythrocyte sedimenta- tion rate are often, but not always, abnormal. In some cases, considerably, being affected by factors such as the virulence blood cultures are positive. Ultimately, bone biopsy may of the implicated organism, the site of involvement, the ultimately be required to identify the offending organism individual’s immune status, and the duration of symptoms [2]. [1]. To add to the complexity, imaging features for infection Imaging plays a crucial role in the diagnosis of infection, are not necessarily specific for osteomyelitis and can also be assessing disease extent, associated complications, planning shared with multiple other conditions [1]. -ese include biopsy sites, and monitoring treatment response. -e var- degenerative processes, trauma or stress responses, neo- ious imaging tools employed include radiography, plastic processes, vasculopathy, inflammation, neuropathic 2 Radiology Research and Practice (a) (b) (c) (d) Figure 1: Osteomyelitis with an ulcer tract arising from a necrotic, infected pressure sore. Axial CT pelvis with intravenous contrast (a) of a 78-year-old bedbound female worked up for sepsis secondary to an infected pressure ulcer showed the ulcer extending to the coccyx in the left parasagittal region (arrow), with bone erosion (dotted line). -e affected bone is hypointense on the axial T1 (b) and hyperintense on fluid-sensitive, PDFS (proton density with fat saturation, (c)) sequences. Sagittal T1FS postcontrast image (d) shows enhancement of the coccyx (arrow) and sacrococcygeal joint confirming the diagnosis. -e adjacent deep subcutaneous region of nonenhancement is compatible with the area of necrosis (dotted arrow). (a) (b) Figure 2: Discitis-osteomyelitis. (a) Sagittal STIR (short tau inversion recovery) with contiguous marrow oedema signal in the L3 and L4 vertebral bodies with involvement and effusion of the intervening L3/4 disc (arrow). Adjacent diffusely enhancing phlegmon (arrow) on a sagittal T1 postcontrast sequence (b) encroaching on the anterior epidural space, resulting in moderate spinal canal stenosis. Radiology Research and Practice 3 (a) (b) (c) (d) (e) th Figure 3: A 45-year-old man involved in a motor vehicle accident sustained an undisplaced 5 metacarpal shaft fracture ((a), arrow). th th Repeating X-ray 16 days later (b), given the persistent pain, revealed rarefaction of 4 and 5 carpometacarpal (CMC) joints consistent with osteomyelitis and septic arthritis (arrow). X-ray-following washout and introduction of antibiotic-impregnated cement spacer (arrow). nd th Coronal STIR (d) and T1 (e) sequences of the wrist show the extent of the infection involving all carpal bones and base of the 2 to 5 metacarpals. (c) arthropathy, iatrogenic processes, and depositional diseases. T1 hypointense, due to the replacement of normal fatty At times, clinical details may be insufficient to aid image marrow tissue. -e confluent T1-hypointensity usually re- interpretation. sults in loss of distinction between the cortex and medulla, -is pictorial review aims to highlight a few of the referred to as the “ghost sign” (Figure 1). On T2-weighted potential mimics of osteomyelitis and septic arthritis that are sequences, such as T2 with fat saturation (T2FS) and short commonly encountered, with emphasis on specific MRI tau inversion recovery (STIR), affected areas are fluid- features that may aid the radiologist and clinician in dis- hyperintense. Various terms are applied to this finding, tinguishing infection from a noninfective aetiology. Variants including “marrow oedema,” “marrow oedema signal,” and “bone marrow lesion (BML)” [5]. Areas of established in- of infection/osteomyelitis are also briefly covered. fection usually demonstrate enhancement following contrast administration. 1.1. Typical Imaging Appearances of Osteomyelitis and Septic In peripheral body parts, ancillary features to actively Arthritis. To understand the MR imaging appearances of search for include soft tissue inflammation, abscess, and infection mimics, it is first important to know the classic ulceration or sinus tract formation, contiguous with the appearances of infection. Pyogenic osteomyelitis is typically site of bone signal abnormality. Areas of geographical 4 Radiology Research and Practice (a) (b) (c) (d) Figure 4: Tuberculous osteomyelitis. Postcontrast axial (a) and sagittal (b) chest CTof a 34-year-old patient with biopsy-proven TB discitis- osteomyelitis. -ere is lytic destruction of the T7 vertebral body anteriorly ((b) white arrow). -ere is subligamentous soft tissue density extending from T5-T8 (A yellow and B white arrows) with relative sparing of the adjacent T7 end plates (b black arrow). Sagittal T1 (c) and STIR (d) of a different patient with T9/10 osteomyelitis (c arrow) and pronounced subligamentous spread of disease from T8/9-T11 (d arrow). Note the relative sparing of the disc in early disease (c arrow). nonenhancement, which can indicate necrosis, are also are the relative sparing of intervertebral disc spaces early in important to note (Figure 1). In the spine, the involve- the infective process, the subligamentous spread of infection, ment of two contiguous vertebral bodies and their in- and involvement of multiple contiguous levels at once [1] tervening disc is usually indicative of discitis- (Figure 4). osteomyelitis (Figure 2). Chronic osteomyelitis can occur in the context of in- -e earliest findings of marrow oedema signal can be complete treatment or atypical organisms. Disruption of vascular supply results in necrosis or sequestrum formation present within 2 days of symptom onset [1]. In the event of discordant clinical and imaging information, where there is a which then serves as a nidus for continued infection. To wall high clinical index of suspicion for infection despite negative off the infection, granulation tissue and new bone, or in- initial imaging results, repeat imaging is important as im- volucrum, form around the sequestrum. Imaging is char- aging findings may lag behind clinical manifestations by up acterised by a mixed pattern of lysis and sclerosis [1]. Sinus to 2 weeks [6] (Figure 3). tracts can form within the involucrum through which pus or With atypical organisms such as tuberculous osteomy- sequestrum may be expelled (Figure 5). elitis, systemic manifestations may not be as florid. Useful Features that are specific for joint infection include features for mycobacterial infection particularly in the spine lamellated synovial thickening (Figure 6), rapid destruction, Radiology Research and Practice 5 (a) (b) (c) (d) Figure 5: A 30-year-old systemically well man with chronic osteomyelitis who initially presented with an enlarging mass in the posterior thigh. -e planning CT (a) showed femoral shaft sclerosis, periosteal thickening, and cortical expansion which is worse medially. A lucent tract at the inferior border of the abnormal bone extends from the medulla to the cortex, consistent with a sinus tract (arrow). Sagittal T1 (b) demonstrating the extent of the osteomyelitis with sequestrum posteroinferiorly (arrow). Axial PDFS (c) and T1FS postcontrast (d) MRI shows the new bone formation or involucrum attempting to envelop the infection. A cloaca or sinus tract involving the posterolateral thigh discharges into the subcutaneous plane, accounting for the presentation (C arrow). and erosion of the bare areas, where there is less coverage of 1.2. Mimics of Osteomyelitis the bone by hyaline cartilage [7]. Usually, there is a marrow 1.2.1. Degeneration/Mechanical Type. Degenerative spon- oedema signal on both sides of the articular surface, often dyloarthropathy, involving end plate degeneration in the with an accompanying joint effusion and synovial en- spine, particularly of the inflammatory type (Modic type I), hancement, although these features are not as specific [7] characterised by end plate T1-hypointensity and fluid- (Figure 3). 6 Radiology Research and Practice (a) (b) Figure 6: Axial T2 (a) and T1FS postcontrast (b) MRI of the knee in a 6-year-old boy. Lamellated synovial thickening (a) is specific for septic arthritis. (a) (b) (c) (d) Figure 7: End plate degeneration. Sagittal T2 (a), T1 (b), and STIR (c) lumbar spine of a 40-year-old female presenting with right L5 radiculopathy in the background of low back pain. -e fluid-hyperintensity (a, c) and T1 hypointense marrow signal (b) on either side of the L4/5 end plate (arrow), in the context of end plate irregularity and preservation of normal/hypointense disc signal, is consistent with inflammatory or Modic type I degeneration. -e radiculopathy was secondary to impingement of the right L5 nerve root from the herniated disc at this level (not shown). Sagittal CT lumbar spine of a different patient (d) shows a vacuum cleft in the L5/S1 disc space with adjacent end plate sclerosis (Modic III degeneration). -e vacuum cleft is a useful sign of degeneration. hyperintensity, can mimic infection. A useful distinguishing proximal femur and adjacent acetabulum, and hatchet-like feature is end plate irregularity without erosion and presence deformity or flattening of the femoral head (Figure 8). -ese changes can mimic septic arthritis. Useful discriminatory of gas in the adjacent disc space, hypointense on all MRI sequences (Figure 7). -e gas indicates the vacuum phe- features are subchondral geodes and femoral head de- nomenon in the context of degeneration [8, 9] (Figure 7(d)). struction that is disproportionately advanced relative to the -e disc desiccation that accompanies degeneration is acetabular involvement [10]. hypointense instead of hyperintense, as demonstrated in discitis [9]. Rapidly destructive osteoarthritis of the hip is a unique 1.2.2. Trauma. Fractures or stress responses can sometimes condition characterised by rapid cartilage loss [10]. -e MR be mistaken for infection on imaging, particularly when a features include joint effusion, bone marrow oedema in the history of trauma is not provided. Both trauma and infection Radiology Research and Practice 7 (a) (b) (c) (d) Figure 8: Two cases of rapidly progressive hip osteoarthritis. X-ray (a) and coronal STIR (b) of a 78-year-old man presenting with an increasingly painful and stiff left hip, demonstrating left hip joint effusion, joint marrow oedema signal, and flattening of the femoral head. Joint aspirate and subsequent washout were negative for infection. Coronal T1 (c) of a second patient with coronal STIR (d) performed 2 months apart shows the rapidly progressive nature of this condition, with hatchet-like deformity of the femoral head in the latter study (d arrow) due to subchondral insufficiency fracture. (a) (b) Figure 9: Continued. 8 Radiology Research and Practice (c) Figure 9: Stress response. Coronal PD (a), coronal (b), and axial PDFS (c) of a 13-year-old soccer player with persistent forefoot pain. -ere th is diffuse marrow oedema signal centred in the 5 metatarsal shaft with surrounding periosteal and soft tissue oedema. -e linear signal at the medial border of the metatarsal shaft represents an incomplete fracture (a, arrow). (a) (b) (c) Figure 10: Continued. Radiology Research and Practice 9 (d) (e) Figure 10: Metastases. Axial T1 (a) pelvis at the level of the hip joint of a 47-year-old female with metastatic breast cancer involving the right acetabulum. Ill-defined acetabular cortex is consistent with cortical breach of tumour and intraarticular extension (arrow). Tumour exhibits mass-effect that is usually readily apparent on MRI. Tumour is usually hyperintense in fluid-sensitive sequences which can mimic infection. Coronal PDFS (b) at the anterior acetabular margin with fluid-hyperintensity of the tumour breaching the acetabular cortex (arrow). Periosteal extension lateral pelvis (dotted arrow). A separate metastatic deposit also presents in the proximal right femoral shaft which helps clinch the diagnosis (dash). Axial T1 (c) and coronal STIR (d) and axial fat-saturated postcontrast T1 (e) of the right foot of a 38-year-old man with AIDS-related Kaposi sarcoma. -e fungating, partially necrotic/enhancing mass (e) is centred in the forefoot, particularly involving the second metatarsal (arrow). -e signal intensity of the involved bone mimics that of osteomyelitis, although infection should not be infiltrative and mass-forming (dotted arrows). can have surrounding the soft tissue oedema signal. -e nidus at the epicentre of the marrow oedema signal, which is presence of a hypointense fracture line on MRI helps to usually T1 hypointense and T2 hyperintense (Figure 11). -e distinguish a fracture from osteomyelitis (Figure 9). In nidus can often be better appreciated on CT and can have a absence of a clear fracture line, the stress response occurs calcified or lucent matrix. more commonly at the mid-diaphysis, whilst infection typically occurs in areas of the increased vascular supply, 1.2.4. Vasculopathy. Raynaud phenomenon can affect the such as at the epiphysis or metaphysis [1]. -e location of vasculature of the extremities by vasospasm and vasocon- stress fractures is usually characteristic, such as the tibia, striction following exposure to various stressors such as cold distal fibula, and metatarsal shafts. temperature. -is can be associated with an abnormal marrow oedema-like signal limited to the distal phalanges of the hands or feet [13]. Similar changes have also been ob- 1.2.3. Neoplasm. Neoplastic processes, either primary bone served in patients with critical limb ischemia. Although the tumours or skeletal metastases, can also mimic infection. mechanism remains unclear, the signal changes may be due Tumours are usually mass-forming, and whilst this can be to tissue damage from ischaemic injury, oedema following difficult to appreciate on CT or radiographs, this is usually reperfusion, or fibrosis from marrow necrosis. In these cases, evident on a T1 sequence [11] (Figure 10). It is important to noncontiguity of the marrow oedema-like signal involving assess for extraosseous extension of tumour and not confuse multiple bones and absence of surrounding soft tissue ab- it with soft tissue inflammation (Figure 10(c)–10(e)). normality is the key to accurate diagnosis (Figure 12). One specific neoplasm that can be confused with in- fection is osteoid osteoma. -is is a benign osteoblastic neoplasm which is richly innervated and induces a florid 1.2.5. MRI Artefact: Failure of Fat Suppression. -e failure of host response by means of periostitis and marrow oedema fat suppression on MRI, manifesting as increased fluid-signal signal [12]. In addition, up to 10% can be intra-articular towards the extremities of the scan field, or in presence of which can incite marked synovitis and joint effusion (Fig- metalware which can alter the uniformity of the magnetic ure 11). -e clue to the correct diagnosis is the detection of a field, is a potential artefactual pitfall. -is can be distinguished 10 Radiology Research and Practice (a) (b) (c) Figure 11: Cuboid osteoid osteoma in a 17-year-old presenting with a 2-month history of foot pain. Axial PDFS (a) of the foot shows diffuse marrow oedema-signal in the cuboid and lateral cuneiform with adjacent synovitis and soft tissue oedema. -ere is T1 marrow replacement of the cuboid ((b), arrow). A fluid-hyperintense nidus, best seen on the fluid-sensitive sequence, is noted in the medial border of the cuboid, with extension into the articular surface (arrow), accounting for the effusion and reactive synovitis (A yellow dash). -e nidus is confirmed on the CT ((c), arrow), demonstrating central calcification, and distinguishes the diagnosis of osteoid osteoma from infection. (a) (b) Figure 12: Coronal forefoot T1 (a) and STIR (b) sequence of a 45-year-old female with Raynaud phenomenon. -ere is an altered marrow signal (A dotted arrow) with oedema signal (b dotted arrow) in the distal phalanges involving noncontiguous bone. -ere is an impression of early tuft resorption involving the great toe (arrow), with an ill-defined cortex. from pathology, as the adjacent subcutaneous fat will also be 1.2.6. Inflammation. Inflammatory spondyloarthropathy involved or incompletely suppressed (Figure 13). Various comprises a group of chronic inflammatory rheumatologic techniques can be employed to minimise these artefacts, al- conditions with a predilection for the axial skeleton [14, 15]. though this is beyond the scope of the manuscript [5]. -e sacroiliac joints are usually involved during the early Radiology Research and Practice 11 disease-modifying therapies, which can prevent or slow the progression to structural damage. MRI manifestations include marrow oedema on both sides of the sacroiliac joints, usually involving the ante- roinferior or cartilaginous articulation. In the early stages of the disease, joint effusion and marrow oedema signal can be more pronounced at the iliac border as the cartilage is thinner here. As the disease progresses, fatty infiltration in adjacent bone, erosion, and ankylosis can be observed (Figure 14). -is inflammation, unlike infection, is confined to this space, does not cross anatomical borders, and is not associated with surrounding soft tissue oedema [14]. Chronic recurrent multifocal osteomyelitis (CRMO) is an idiopathic inflammatory disorder and shares similar appearances with subacute/chronic osteomyelitis [16]. Me- dial clavicular and multifocal involvement in children or adolescents is classically described. In suspected cases of CRMO, a whole-body MRI should be considered to look for other areas of bone involvement (Figure 15). CRMO is a diagnosis of exclusion after excluding other secondary causes for chronic OM. SAPHO (synovitis, acne, pustulosis, hyperostosis, oste- itis) is a rare condition affecting mostly young to middle- aged adults, representing an older demographic than the CRMO subset [17]. It may sometimes mimic osteomyelitis Figure 13: Artefact. Sagittal PDFS of the ring finger of a healthy due to its bony involvement and osteitis. -is is also usually volunteer demonstrating a failure of fat suppression at the tip of the polyostotic and classically affects the sternoclavicular joints, finger resulting in a false impression of marrow hyperintensity in first rib, sternomanubrial joint, and the anterior aspect of the the distal phalanx. -e adjacent subcutaneous tissue is also in- adequately suppressed (dash). vertebral bodies (Figure 16). 1.2.7. Iatrogenic Processes. Radiation osteonecrosis can occur following radiotherapy (30–50 Gy) due to a combi- nation of damage to osteoblasts, resulting in unopposed osteoclastic activity, and vascular injury [18]. -ere is an initial osteopenia or lysis, followed by a delayed and dis- organised bony repair at least 3 years following radiotherapy, resulting in trabecular disorganisation and patchy marrow density (Figure 17(a)). On MRI, the initial acute changes can be associated with marrow and soft tissue oedema, and these can be difficult to distinguish from osteomyelitis or tumour recurrence (Figures 17(b) and 17(c)). Radiotherapy treat- ment timing, duration, dose, and field are useful parameters in this setting along with previous, baseline imaging for comparison, as radiation osteonecrosis will be confined within the field of radiotherapy even when the borders of the abnormal bone are poorly defined [19]. Associated osteol- Figure 14: Sacroiliitis. Coronal STIR sequence of sacroiliac joints ysis, osseous expansion, or fistula formation is usually more (SIJ) of a 34-year-old male with right acute on chronic and left indicative of infection than osteonecrosis [19]. chronic sacroiliitis. -e region of the acute inflammatory process is Postoperative findings and sterile collections can often denoted by the marrow oedema signal in the cartilaginous com- be difficult to distinguish from infection and image inter- ponent of the right SIJ (arrow). Marrow fat infiltration (dotted pretation can be further complicated by the presence of arrow) adjacent to the left SIJ inferiorly implies prior inflammation. orthopaedic hardware which can lead to susceptibility and Irregular joint surface (dash) is consistent with erosion. field inhomogeneity artefacts (Figure 13). -e presence of metalware reduces the ability to adequately suppress the fat- course of the disease process. Early detection of sacroiliitis signal, simulating marrow and soft tissue oedema. Whilst using a combination of radiologic and clinical findings is various MRI techniques have been employed for artefact important since the condition usually responds well to reduction, nuclear medicine studies and, in particular, the 12 Radiology Research and Practice (a) (b) Figure 15: CRMO. Coronal whole-body MRI of an 8-year-old boy (a) with CRMO initially presenting with right knee pain. Note the multifocal involvement which included both knees, left ankle, and the sacrum (arrow). Axial STIR (b) of a different CRMO patient aged 7, with classic involvement of right medial clavicle with associated hyperostosis (arrow). (a) (b) Figure 16: A 27-year-old female with SAPHO. -ere is hyperostosis and osteitis of the sternomanubrial junction on the sagittal CT (a). Contiguous involvement of multiple vertebral bodies anteriorly with sparing of the intervening disc space as demonstrated on sagittal T1 thoracic spine is typical of this condition (b). Radiology Research and Practice 13 (a) (b) (c) Figure 17: Osteoradionecrosis. Orthopantomogram (OPG, (a)) of a 74-year-old male with a history of T3 oropharyngeal tumour having undergone prior resection and chemoradiotherapy, complicated by osteoradionecrosis. -ere is ill-defined lytic lucency eroding the right mandibular body with background coarsened trabeculation and patchy sclerosis. Axial T1 (b) and T2FS (c) of a different patient with a previous history of radiotherapy for skin SCC, presenting with a nonhealing ulcer due to osteoradionecrosis. -ere are T1 hypointensity and fluid-hyperintensity in the body of the right mandible ((a) arrow). Mild surrounding soft tissue oedema ((b) arrow). white cell scan remains the most valuable imaging modality to assess for infection around a prosthesis [20]. MRI plays a key role in the assessment of delayed- hypersensitivity reactions to arthroplasty-related metal products, known as pseudotumour or adverse reaction to metal debris. -is can lead to aggressive soft tissue de- struction if untreated. Imaging features include effusion with variable thickness of the synovial lining of synovial prolif- eration (Figure 18). It can be associated with perisynovial oedema and local nodal enlargement, mimicking infection. Figure 18: Adverse reaction to metallic debris (ARMD). A 70-year- Increased synovial thickness and T1 and T2-hypointensity old female with left hip resurfacing complicated by pseudotumour favour pseudotumour over infection [21]. formation. Axial T2 pelvis with metal artefact reduction technique demonstrating distension of the left hip pseudocapsule posteriorly (dotted line) and a larger anterior pseudocapsule defect decom- 1.2.8. Neuropathy. Neuropathic arthropathy most com- pressing into the iliopsoas bursa (arrow). -is thickened, T2- monly occurs in patients with altered pain sensation and hypointense rim with synovial proliferation favours pseudotu- proprioception resulting in the accumulation of mour/ARMD over infection. 14 Radiology Research and Practice (a) (b) (c) Figure 19: Lateral and oblique right foot radiographs (a) of a 47-year-old woman with type II diabetes and Charcot arthropathy involving the midfoot. Disorganised hindfoot with joint destruction and disorganisation (arrow). Note the absence of osteopenia that is typically observed in infection. Coronal STIR (b) and T1 (c) of a different patient with Charcot arthropathy with hindfoot destruction, hindfoot valgus, and dislocation. -e contrast was not administered due to chronic renal failure. -e talus is flattened and sclerotic (arrow). Note the fluid collection in the distal tibial shaft (dotted arrow) and the medial tibiotalar articulation. -is patient had both neuropathic arthropathy complicated by chronic osteomyelitis with intraosseous abscess formation. At times, different conditions can preexist, and ultimately, tissue sampling may be required. (a) (b) (c) Figure 20: Continued. Radiology Research and Practice 15 (d) Figure 20: Primary amyloidosis. A 64-year-old woman with known primary amyloidosis of lacrimal glands, initially presenting with neck pain. Sagittal T2 (a), T1 (b), and axial T2FS (c) spine shows an infiltrative process involving the C7 and T1 vertebrae with an extraosseous extension of soft tissue into the epidural and prevertebral spaces (arrow). End plate irregularity is also present. Axial T2FS (c) at the level of C7 demonstrating epidural and prevertebral soft tissue infiltration (arrow). -is case was difficult to distinguish from infection, ultimately requiring a biopsy for the final diagnosis of C7/T1 amyloid deposition. Axial T2 head at the level of the orbits (d) showed bilateral lacrimal gland enlargement secondary to amyloid deposition (arrow). (a) (b) Figure 21: A 49-year-old female with end stage renal failure and tertiary hyperparathyroidism. Sagittal lumbar spine (a) with bone reconstructions shows rugger-jersey spine with sclerosis adjacent to end plates (arrow) whilst axial pelvis (b) demonstrates subperiosteal resorption of the SIJs (arrow). microtrauma [22, 23]. It commonly occurs in the feet of process. Sclerosis on radiographs and stability of findings diabetic patients. In the acute stage, the foot may be over time favour Charcot neuropathy over infection. On the contrary, the contiguity of the marrow change with painful and erythematous, followed by bone dis- organisation, dislocation, secondary degeneration, and any ulcer or collection supports infection (Figures 1, debris formation with preservation of bone density, also 19(b), and 19(c). -e areas affected by osteomyelitis may known as the “Five Ds” (Figure 19). Features that favour be more conspicuous on contrast-enhanced sequences. neuropathy over osteomyelitis are periarticular marrow Various new techniques such as the use of diffusion- oedema-like signal, joint subluxation, and geode forma- weighted imaging (DWI), dynamic postcontrast en- tion, since neuropathy is predominantly an articular hancement, and perfusion may provide further useful 16 Radiology Research and Practice (a) (b) (c) (d) Figure 22: Calcific tendinitis in a 40-year-old female presenting with persistent shoulder pain. Axial PDFS (a) demonstrating marrow oedema signal in the humeral head at the greater tuberosity at teres minor tendon footprint. Sagittal PDFS (b) demonstrating corresponding cortical erosion. -e MRI performed 5 months previously at the comparable plane (c) showed globular hypointense structure within the teres minor tendon footprint (arrow), confirming intraosseous migration of the calcific tendinitis in the most recent images. AP radiograph of the right shoulder (d) performed at the time of initial presentation also demonstrated calcium deposition in rotator cuff tendons. -e calcium deposit is not well appreciated in the more recent study given the acute resorptive phase. information although the utility of these more advanced crystals can, at times, incite an inflammatory response techniques remains to be validated [22]. and result in bone erosion, mimicking infection. In the acute phase, soft tissue swelling and joint effusion can be present. More chronic crystal deposits are usually T1 and 1.2.9. Depositional Disease. Depositional disease such as T2 hypointense, without significant blooming artefact on amyloidosis can radiologically resemble an infection, ulti- susceptibility sequences that may otherwise suggest mately requiring biopsy for diagnosis (Figure 20). In patients pigmented villonodular synovitis (PVNS). Calcific with chronic renal insufficiency, aggressive spondylosis can phosphate can deposit within tendons and can provoke also occur due to amyloid deposition. Features of hyper- an acute inflammatory response in the resorptive phase, parathyroidism such as sclerosis adjacent to end plates during which the calcium can migrate into the adjacent (rugger-jersey spine) and subperiosteal or subligamentous bursa or bone, mimicking osteomyelitis (Figure 22). bone resorption can help clinch the diagnosis [24] Calcium at this phase may be oedematous and difficult to (Figure 21). depict on MRI. A radiograph can be useful for the as- Microcrystals can deposit in periarticular or intra- sessment of soft tissue calcification which may not be articular soft tissue. -is includes monosodium urate in apparent on MRI [25]. Dual-energy CTcan also be used in gouty arthropathy and calcium hydroxyapatite deposi- distinguishing gout from other calcium deposition tion. Most cases are usually asymptomatic although the (Figure 23). Radiology Research and Practice 17 (a) (b) Figure 23: Gouty tophus in a 39-year-old man presenting with a swollen and erythematous toe which was clinically suspected to be an st infection. X-ray showed 1 MTPJ erosion at the medial border associated with dense soft tissue swelling (arrow). Dual-energy CT with material decomposition helped differentiate urate crystals (mapped as green, arrowed) from calcium (blue, not present in this case). 2. Conclusion Acknowledgments -e imaging appearance of the bone and joint infections -e authors would like to thank Dr. Ricky Lu Shi Sheng for may be mimicked by many conditions. It is important to his contribution to the earlier version of the manuscript. consider other differentials when a specific clinical scenario is discordant from the imaging findings. Whilst it is always References important to consider the clinical picture and laboratory findings when interpreting radiologic findings, pertinent [1] Y. J. Lee, S. Sadigh, K. Mankad, N. Kapse, and G. Rajeswaran, information may not always be available. An appreciation of “-e imaging of osteomyelitis,” Quantitative Imaging in the overlap of these differential diagnoses with infection and Medicine and Surgery, vol. 6, no. 2, pp. 184–198, 2016. [2] J. Pupaibool, S. Vasoo, P. J. Erwin, M. H. Murad, and key differentiating factors equips the radiologist with the E. F. Berbari, “-e utility of image-guided percutaneous ability to make a significant contribution to diagnosis and needle aspiration biopsy for the diagnosis of spontaneous appropriate, timely management. vertebral osteomyelitis: a systematic review and meta-anal- ysis,” 6e Spine Journal, vol. 15, no. 1, pp. 122–131, 2015. [3] F. D. Beaman, P. F. von Herrmann, M. J. Kransdorf et al., Data Availability “ACR appropriateness criteria suspected osteomyelitis, septic No new data were used to support this study. arthritis, or soft tissue infection (excluding spine and diabetic foot),” Journal of the American College of Radiology, vol. 14, no. 5, pp. S326–S337, 2017. Ethical Approval [4] C. Pineda, A. Vargas, and A. V. Rodr´ıguez, “Imaging of osteomyelitis: current concepts,” Infectious Disease Clinics of Ethical approval and consent waiver were obtained via the North America, vol. 20, no. 4, pp. 789–825, 2006. institutional ethics board (CHCA-HREC Ref No. 20- [5] W. Lim and A. Saifuddin, “Review article: the differential CHREC-E012). diagnosis of bone marrow edema on wrist MRI,” Skeletal Radiology, vol. 48, no. 10, pp. 1525–1539, 2019. [6] C. Pineda, R. Espinosa, and A. Pena, “Radiographic imaging Conflicts of Interest in osteomyelitis: the role of plain radiography, computed tomography, ultrasonography, magnetic resonance imaging, -e authors declare that they have no conflicts of interest. 18 Radiology Research and Practice and scintigraphy,” Seminars in Plastic Surgery, vol. 23, no. 02, [23] E. A. Jones, B. J. Manaster, D. A. May, and D. G. Disler, pp. 080–089, 2009. “Neuropathic osteoarthropathy: diagnostic dilemmas and [7] M. Karchevsky, M. E. Schweitzer, W. B. Morrison, and differential diagnosis,” RadioGraphics, vol. 20, pp. S279–S293, J. A. Parellada, “MRI findings of septic arthritis and associated osteomyelitis in adults,” American Journal of Roentgenology, [24] M. J. Cobby, R. S. Adler, R. Swartz, and W. Martel, “Dialysis- vol. 182, no. 1, pp. 119–122, 2004. related amyloid arthropathy: MR findings in four patients,” [8] D. Resnick, G. Niwayama, J. Guerra Jr., V. Vint, and American Journal of Roentgenology, vol. 157, no. 5, J. Usselman, “Spinal vacuum phenomena: anatomical study pp. 1023–1027, 1991. and review,” Radiology, vol. 139, no. 2, pp. 341–348, 1981. [25] P. Omoumi, P. Zufferey, J. Malghem, and A. So, “Imaging in [9] R. Rahme and R. Moussa, “-e modic vertebral endplate and gout and other crystal-related arthropathies,” Rheumatic marrow changes: pathologic significance and relation to low Disease Clinics of North America, vol. 42, no. 4, pp. 621–644, back pain and segmental instability of the lumbar spine,” 2016. American Journal of Neuroradiology, vol. 29, no. 5, pp. 838– 842, 2008. [10] N. Boutry, C. Paul, X. Leroy, D. Fredoux, H. Migaud, and A. Cotten, “Rapidly destructive osteoarthritis of the hip: MR imaging findings,” American Journal of Roentgenology, vol. 179, no. 3, pp. 657–663, 2002. [11] M. D. Murphey, L. T. Senchak, P. K. Mambalam, C. I. Logie, M. K. Klassen-Fischer, and M. J. Kransdorf, “From the ra- diologic pathology archives: ewing sarcoma family of tumors: radiologic-pathologic correlation,” RadioGraphics, vol. 33, no. 3, pp. 803–831, 2013. [12] J. W. Chai, S. H. Hong, J.-Y. Choi et al., “Radiologic diagnosis of osteoid osteoma: from simple to challenging findings,” RadioGraphics, vol. 30, no. 3, pp. 737–749, 2010. [13] E. Smitaman, B. P. G. Pereira, B. K. Huang, M. M. Zakhary, E. Fliszar, and D. L. Resnick, “Abnormal bone marrow signal intensity in the phalanges of the foot as a manifestation of Raynaud phenomenon: a report of six patients,” American Journal of Roentgenology, vol. 207, no. 6, pp. 1252–1256, 2016. [14] M. Navallas, J. Ares, B. Beltran, ´ M. P. Lisbona, J. Maymo, ´ and A. Solano, “Sacroiliitis associated with axial spondyloarthr- opathy: new concepts and latest trends,” RadioGraphics, vol. 33, no. 4, pp. 933–956, 2013. [15] C. Tsoi, J. F. Griffith, R. K. L. Lee, P. C. H. Wong, and L. S. Tam, “Imaging of sacroiliitis: current status, limitations and pitfalls,” Quantitative Imaging in Medicine and Surgery, vol. 9, no. 2, pp. 318–335, 2019. [16] G. Khanna, T. S. P. Sato, and P. Ferguson, “Imaging of chronic recurrent multifocal osteomyelitis,” Radiographics, vol. 29, no. 4, pp. 1159–1177, 2009. [17] A. Cotten, R. M. Flipo, A. Mentre, E. Delaporte, B. Duquesnoy, and P. Chastanet, “SAPHO syndrome,” Ra- diographics, vol. 15, no. 5, pp. 1147–1154, 1995. [18] R. Hermans, “Imaging of mandibular osteoradionecrosis,” Neuroimaging Clinics of North America, vol. 13, no. 3, pp. 597–604, 2003. [19] P. M. Phal, R. W. T. Myall, L. A. Assael, and J. L. Weissman, “Imaging findings of bisphosphonate-associated osteonec- rosis of the jaws,” American Journal of Neuroradiology, vol. 28, no. 6, pp. 1139–1145, 2007. [20] C. J. Palestro, “Nuclear medicine and the failed joint re- placement: past, present, and future,” World Journal of Ra- diology, vol. 6, no. 7, pp. 446–458, 2014. [21] J. Fritz, B. Lurie, T. T. Miller, and H. G. Potter, “MR imaging of hip arthroplasty implants,” RadioGraphics, vol. 34, no. 4, pp. E106–E132, 2014. [22] T. M. Noguerol, A. L. Alcala, ´ L. S. Beltran, ´ M. G. Cabrera, J. B. Cabrero, and J. C. Vilanova, “Advanced MR imaging techniques for differentiation of neuropathic arthropathy and osteomyelitis in the diabetic foot,” RadioGraphics, vol. 37, no. 4, pp. 1161–1180, 2017. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Radiology Research and Practice Hindawi Publishing Corporation

Radiologic Mimics of Osteomyelitis and Septic Arthritis: A Pictorial Essay

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Hindawi Radiology Research and Practice Volume 2021, Article ID 9912257, 18 pages https://doi.org/10.1155/2021/9912257 Review Article Radiologic Mimics of Osteomyelitis and Septic Arthritis: A Pictorial Essay 1,2 1,2,3 1,4 Wanyin Lim , Christen D. Barras, and Steven Zadow Dr Jones and Partners Medical Imaging, Adelaide, South Australia, Australia Department of Radiology, Royal Adelaide Hospital, Adelaide, South Australia, Australia South Australian Health and Medical Research Institute and the University of Adelaide, Adelaide, South Australia, Australia Flinders Medical Centre, Bedford Park, South Australia, Australia Correspondence should be addressed to Wanyin Lim; ynyn146@gmail.com Received 17 March 2021; Revised 12 May 2021; Accepted 18 May 2021; Published 24 May 2021 Academic Editor: Andre´ Luiz Ferreira COSTA Copyright © 2021 Wanyin Lim et al. -is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Various imaging techniques may be employed in the investigation of suspected bone and joint infections. -ese include ul- trasound, radiography, functional imaging such as positron emission tomography (PET) and nuclear scintigraphy, and cross- sectional imaging, including computed tomography (CT) and magnetic resonance imaging (MRI). -e cross-sectional modalities represent the imaging workhorse in routine practice. -e role of imaging also extends to include assessment of the anatomical extent of infection, potentially associated complications, and treatment response. -e imaging appearances of bone and joint infections are heterogeneous and depend on the duration of infection, an individual patient’s immune status, and virulence of culprit organisms. To add to the complexity of radiodiagnosis, one of the pitfalls of imaging musculoskeletal infection is the presence of other conditions that can share overlapping imaging features. -is includes osteoarthritis, vasculopathy, inflam- matory, and even neoplastic processes. Different pathologies may also coexist, for example, diabetic neuropathy and osteomyelitis. -is pictorial review aims to highlight potential mimics of osteomyelitis and septic arthritis that are regularly encountered, with emphasis on specific imaging features that may aid the radiologist and clinician in distinguishing an infective from a noninfective aetiology. ultrasound, computed tomography (CT), and functional 1. Introduction studies including nuclear scintigraphy, white cell scan, and Osteomyelitis is defined as bone inflammation due to in- positron emission tomography (PET). Magnetic resonance fection whilst septic arthritis is defined by infection within a imaging (MRI), being moderately sensitive and specific, is joint [1]. Bone and joint infections have a variable clinical the imaging modality of choice in the evaluation of sus- presentation ranging from acute sepsis to insidious onset of pected osteomyelitis [3, 4]. pain, with or without fever. Laboratory results such as white Understandably, given the heterogeneity of clinical presentations, imaging appearances of infection also vary cell count, C-reactive protein, and erythrocyte sedimenta- tion rate are often, but not always, abnormal. In some cases, considerably, being affected by factors such as the virulence blood cultures are positive. Ultimately, bone biopsy may of the implicated organism, the site of involvement, the ultimately be required to identify the offending organism individual’s immune status, and the duration of symptoms [2]. [1]. To add to the complexity, imaging features for infection Imaging plays a crucial role in the diagnosis of infection, are not necessarily specific for osteomyelitis and can also be assessing disease extent, associated complications, planning shared with multiple other conditions [1]. -ese include biopsy sites, and monitoring treatment response. -e var- degenerative processes, trauma or stress responses, neo- ious imaging tools employed include radiography, plastic processes, vasculopathy, inflammation, neuropathic 2 Radiology Research and Practice (a) (b) (c) (d) Figure 1: Osteomyelitis with an ulcer tract arising from a necrotic, infected pressure sore. Axial CT pelvis with intravenous contrast (a) of a 78-year-old bedbound female worked up for sepsis secondary to an infected pressure ulcer showed the ulcer extending to the coccyx in the left parasagittal region (arrow), with bone erosion (dotted line). -e affected bone is hypointense on the axial T1 (b) and hyperintense on fluid-sensitive, PDFS (proton density with fat saturation, (c)) sequences. Sagittal T1FS postcontrast image (d) shows enhancement of the coccyx (arrow) and sacrococcygeal joint confirming the diagnosis. -e adjacent deep subcutaneous region of nonenhancement is compatible with the area of necrosis (dotted arrow). (a) (b) Figure 2: Discitis-osteomyelitis. (a) Sagittal STIR (short tau inversion recovery) with contiguous marrow oedema signal in the L3 and L4 vertebral bodies with involvement and effusion of the intervening L3/4 disc (arrow). Adjacent diffusely enhancing phlegmon (arrow) on a sagittal T1 postcontrast sequence (b) encroaching on the anterior epidural space, resulting in moderate spinal canal stenosis. Radiology Research and Practice 3 (a) (b) (c) (d) (e) th Figure 3: A 45-year-old man involved in a motor vehicle accident sustained an undisplaced 5 metacarpal shaft fracture ((a), arrow). th th Repeating X-ray 16 days later (b), given the persistent pain, revealed rarefaction of 4 and 5 carpometacarpal (CMC) joints consistent with osteomyelitis and septic arthritis (arrow). X-ray-following washout and introduction of antibiotic-impregnated cement spacer (arrow). nd th Coronal STIR (d) and T1 (e) sequences of the wrist show the extent of the infection involving all carpal bones and base of the 2 to 5 metacarpals. (c) arthropathy, iatrogenic processes, and depositional diseases. T1 hypointense, due to the replacement of normal fatty At times, clinical details may be insufficient to aid image marrow tissue. -e confluent T1-hypointensity usually re- interpretation. sults in loss of distinction between the cortex and medulla, -is pictorial review aims to highlight a few of the referred to as the “ghost sign” (Figure 1). On T2-weighted potential mimics of osteomyelitis and septic arthritis that are sequences, such as T2 with fat saturation (T2FS) and short commonly encountered, with emphasis on specific MRI tau inversion recovery (STIR), affected areas are fluid- features that may aid the radiologist and clinician in dis- hyperintense. Various terms are applied to this finding, tinguishing infection from a noninfective aetiology. Variants including “marrow oedema,” “marrow oedema signal,” and “bone marrow lesion (BML)” [5]. Areas of established in- of infection/osteomyelitis are also briefly covered. fection usually demonstrate enhancement following contrast administration. 1.1. Typical Imaging Appearances of Osteomyelitis and Septic In peripheral body parts, ancillary features to actively Arthritis. To understand the MR imaging appearances of search for include soft tissue inflammation, abscess, and infection mimics, it is first important to know the classic ulceration or sinus tract formation, contiguous with the appearances of infection. Pyogenic osteomyelitis is typically site of bone signal abnormality. Areas of geographical 4 Radiology Research and Practice (a) (b) (c) (d) Figure 4: Tuberculous osteomyelitis. Postcontrast axial (a) and sagittal (b) chest CTof a 34-year-old patient with biopsy-proven TB discitis- osteomyelitis. -ere is lytic destruction of the T7 vertebral body anteriorly ((b) white arrow). -ere is subligamentous soft tissue density extending from T5-T8 (A yellow and B white arrows) with relative sparing of the adjacent T7 end plates (b black arrow). Sagittal T1 (c) and STIR (d) of a different patient with T9/10 osteomyelitis (c arrow) and pronounced subligamentous spread of disease from T8/9-T11 (d arrow). Note the relative sparing of the disc in early disease (c arrow). nonenhancement, which can indicate necrosis, are also are the relative sparing of intervertebral disc spaces early in important to note (Figure 1). In the spine, the involve- the infective process, the subligamentous spread of infection, ment of two contiguous vertebral bodies and their in- and involvement of multiple contiguous levels at once [1] tervening disc is usually indicative of discitis- (Figure 4). osteomyelitis (Figure 2). Chronic osteomyelitis can occur in the context of in- -e earliest findings of marrow oedema signal can be complete treatment or atypical organisms. Disruption of vascular supply results in necrosis or sequestrum formation present within 2 days of symptom onset [1]. In the event of discordant clinical and imaging information, where there is a which then serves as a nidus for continued infection. To wall high clinical index of suspicion for infection despite negative off the infection, granulation tissue and new bone, or in- initial imaging results, repeat imaging is important as im- volucrum, form around the sequestrum. Imaging is char- aging findings may lag behind clinical manifestations by up acterised by a mixed pattern of lysis and sclerosis [1]. Sinus to 2 weeks [6] (Figure 3). tracts can form within the involucrum through which pus or With atypical organisms such as tuberculous osteomy- sequestrum may be expelled (Figure 5). elitis, systemic manifestations may not be as florid. Useful Features that are specific for joint infection include features for mycobacterial infection particularly in the spine lamellated synovial thickening (Figure 6), rapid destruction, Radiology Research and Practice 5 (a) (b) (c) (d) Figure 5: A 30-year-old systemically well man with chronic osteomyelitis who initially presented with an enlarging mass in the posterior thigh. -e planning CT (a) showed femoral shaft sclerosis, periosteal thickening, and cortical expansion which is worse medially. A lucent tract at the inferior border of the abnormal bone extends from the medulla to the cortex, consistent with a sinus tract (arrow). Sagittal T1 (b) demonstrating the extent of the osteomyelitis with sequestrum posteroinferiorly (arrow). Axial PDFS (c) and T1FS postcontrast (d) MRI shows the new bone formation or involucrum attempting to envelop the infection. A cloaca or sinus tract involving the posterolateral thigh discharges into the subcutaneous plane, accounting for the presentation (C arrow). and erosion of the bare areas, where there is less coverage of 1.2. Mimics of Osteomyelitis the bone by hyaline cartilage [7]. Usually, there is a marrow 1.2.1. Degeneration/Mechanical Type. Degenerative spon- oedema signal on both sides of the articular surface, often dyloarthropathy, involving end plate degeneration in the with an accompanying joint effusion and synovial en- spine, particularly of the inflammatory type (Modic type I), hancement, although these features are not as specific [7] characterised by end plate T1-hypointensity and fluid- (Figure 3). 6 Radiology Research and Practice (a) (b) Figure 6: Axial T2 (a) and T1FS postcontrast (b) MRI of the knee in a 6-year-old boy. Lamellated synovial thickening (a) is specific for septic arthritis. (a) (b) (c) (d) Figure 7: End plate degeneration. Sagittal T2 (a), T1 (b), and STIR (c) lumbar spine of a 40-year-old female presenting with right L5 radiculopathy in the background of low back pain. -e fluid-hyperintensity (a, c) and T1 hypointense marrow signal (b) on either side of the L4/5 end plate (arrow), in the context of end plate irregularity and preservation of normal/hypointense disc signal, is consistent with inflammatory or Modic type I degeneration. -e radiculopathy was secondary to impingement of the right L5 nerve root from the herniated disc at this level (not shown). Sagittal CT lumbar spine of a different patient (d) shows a vacuum cleft in the L5/S1 disc space with adjacent end plate sclerosis (Modic III degeneration). -e vacuum cleft is a useful sign of degeneration. hyperintensity, can mimic infection. A useful distinguishing proximal femur and adjacent acetabulum, and hatchet-like feature is end plate irregularity without erosion and presence deformity or flattening of the femoral head (Figure 8). -ese changes can mimic septic arthritis. Useful discriminatory of gas in the adjacent disc space, hypointense on all MRI sequences (Figure 7). -e gas indicates the vacuum phe- features are subchondral geodes and femoral head de- nomenon in the context of degeneration [8, 9] (Figure 7(d)). struction that is disproportionately advanced relative to the -e disc desiccation that accompanies degeneration is acetabular involvement [10]. hypointense instead of hyperintense, as demonstrated in discitis [9]. Rapidly destructive osteoarthritis of the hip is a unique 1.2.2. Trauma. Fractures or stress responses can sometimes condition characterised by rapid cartilage loss [10]. -e MR be mistaken for infection on imaging, particularly when a features include joint effusion, bone marrow oedema in the history of trauma is not provided. Both trauma and infection Radiology Research and Practice 7 (a) (b) (c) (d) Figure 8: Two cases of rapidly progressive hip osteoarthritis. X-ray (a) and coronal STIR (b) of a 78-year-old man presenting with an increasingly painful and stiff left hip, demonstrating left hip joint effusion, joint marrow oedema signal, and flattening of the femoral head. Joint aspirate and subsequent washout were negative for infection. Coronal T1 (c) of a second patient with coronal STIR (d) performed 2 months apart shows the rapidly progressive nature of this condition, with hatchet-like deformity of the femoral head in the latter study (d arrow) due to subchondral insufficiency fracture. (a) (b) Figure 9: Continued. 8 Radiology Research and Practice (c) Figure 9: Stress response. Coronal PD (a), coronal (b), and axial PDFS (c) of a 13-year-old soccer player with persistent forefoot pain. -ere th is diffuse marrow oedema signal centred in the 5 metatarsal shaft with surrounding periosteal and soft tissue oedema. -e linear signal at the medial border of the metatarsal shaft represents an incomplete fracture (a, arrow). (a) (b) (c) Figure 10: Continued. Radiology Research and Practice 9 (d) (e) Figure 10: Metastases. Axial T1 (a) pelvis at the level of the hip joint of a 47-year-old female with metastatic breast cancer involving the right acetabulum. Ill-defined acetabular cortex is consistent with cortical breach of tumour and intraarticular extension (arrow). Tumour exhibits mass-effect that is usually readily apparent on MRI. Tumour is usually hyperintense in fluid-sensitive sequences which can mimic infection. Coronal PDFS (b) at the anterior acetabular margin with fluid-hyperintensity of the tumour breaching the acetabular cortex (arrow). Periosteal extension lateral pelvis (dotted arrow). A separate metastatic deposit also presents in the proximal right femoral shaft which helps clinch the diagnosis (dash). Axial T1 (c) and coronal STIR (d) and axial fat-saturated postcontrast T1 (e) of the right foot of a 38-year-old man with AIDS-related Kaposi sarcoma. -e fungating, partially necrotic/enhancing mass (e) is centred in the forefoot, particularly involving the second metatarsal (arrow). -e signal intensity of the involved bone mimics that of osteomyelitis, although infection should not be infiltrative and mass-forming (dotted arrows). can have surrounding the soft tissue oedema signal. -e nidus at the epicentre of the marrow oedema signal, which is presence of a hypointense fracture line on MRI helps to usually T1 hypointense and T2 hyperintense (Figure 11). -e distinguish a fracture from osteomyelitis (Figure 9). In nidus can often be better appreciated on CT and can have a absence of a clear fracture line, the stress response occurs calcified or lucent matrix. more commonly at the mid-diaphysis, whilst infection typically occurs in areas of the increased vascular supply, 1.2.4. Vasculopathy. Raynaud phenomenon can affect the such as at the epiphysis or metaphysis [1]. -e location of vasculature of the extremities by vasospasm and vasocon- stress fractures is usually characteristic, such as the tibia, striction following exposure to various stressors such as cold distal fibula, and metatarsal shafts. temperature. -is can be associated with an abnormal marrow oedema-like signal limited to the distal phalanges of the hands or feet [13]. Similar changes have also been ob- 1.2.3. Neoplasm. Neoplastic processes, either primary bone served in patients with critical limb ischemia. Although the tumours or skeletal metastases, can also mimic infection. mechanism remains unclear, the signal changes may be due Tumours are usually mass-forming, and whilst this can be to tissue damage from ischaemic injury, oedema following difficult to appreciate on CT or radiographs, this is usually reperfusion, or fibrosis from marrow necrosis. In these cases, evident on a T1 sequence [11] (Figure 10). It is important to noncontiguity of the marrow oedema-like signal involving assess for extraosseous extension of tumour and not confuse multiple bones and absence of surrounding soft tissue ab- it with soft tissue inflammation (Figure 10(c)–10(e)). normality is the key to accurate diagnosis (Figure 12). One specific neoplasm that can be confused with in- fection is osteoid osteoma. -is is a benign osteoblastic neoplasm which is richly innervated and induces a florid 1.2.5. MRI Artefact: Failure of Fat Suppression. -e failure of host response by means of periostitis and marrow oedema fat suppression on MRI, manifesting as increased fluid-signal signal [12]. In addition, up to 10% can be intra-articular towards the extremities of the scan field, or in presence of which can incite marked synovitis and joint effusion (Fig- metalware which can alter the uniformity of the magnetic ure 11). -e clue to the correct diagnosis is the detection of a field, is a potential artefactual pitfall. -is can be distinguished 10 Radiology Research and Practice (a) (b) (c) Figure 11: Cuboid osteoid osteoma in a 17-year-old presenting with a 2-month history of foot pain. Axial PDFS (a) of the foot shows diffuse marrow oedema-signal in the cuboid and lateral cuneiform with adjacent synovitis and soft tissue oedema. -ere is T1 marrow replacement of the cuboid ((b), arrow). A fluid-hyperintense nidus, best seen on the fluid-sensitive sequence, is noted in the medial border of the cuboid, with extension into the articular surface (arrow), accounting for the effusion and reactive synovitis (A yellow dash). -e nidus is confirmed on the CT ((c), arrow), demonstrating central calcification, and distinguishes the diagnosis of osteoid osteoma from infection. (a) (b) Figure 12: Coronal forefoot T1 (a) and STIR (b) sequence of a 45-year-old female with Raynaud phenomenon. -ere is an altered marrow signal (A dotted arrow) with oedema signal (b dotted arrow) in the distal phalanges involving noncontiguous bone. -ere is an impression of early tuft resorption involving the great toe (arrow), with an ill-defined cortex. from pathology, as the adjacent subcutaneous fat will also be 1.2.6. Inflammation. Inflammatory spondyloarthropathy involved or incompletely suppressed (Figure 13). Various comprises a group of chronic inflammatory rheumatologic techniques can be employed to minimise these artefacts, al- conditions with a predilection for the axial skeleton [14, 15]. though this is beyond the scope of the manuscript [5]. -e sacroiliac joints are usually involved during the early Radiology Research and Practice 11 disease-modifying therapies, which can prevent or slow the progression to structural damage. MRI manifestations include marrow oedema on both sides of the sacroiliac joints, usually involving the ante- roinferior or cartilaginous articulation. In the early stages of the disease, joint effusion and marrow oedema signal can be more pronounced at the iliac border as the cartilage is thinner here. As the disease progresses, fatty infiltration in adjacent bone, erosion, and ankylosis can be observed (Figure 14). -is inflammation, unlike infection, is confined to this space, does not cross anatomical borders, and is not associated with surrounding soft tissue oedema [14]. Chronic recurrent multifocal osteomyelitis (CRMO) is an idiopathic inflammatory disorder and shares similar appearances with subacute/chronic osteomyelitis [16]. Me- dial clavicular and multifocal involvement in children or adolescents is classically described. In suspected cases of CRMO, a whole-body MRI should be considered to look for other areas of bone involvement (Figure 15). CRMO is a diagnosis of exclusion after excluding other secondary causes for chronic OM. SAPHO (synovitis, acne, pustulosis, hyperostosis, oste- itis) is a rare condition affecting mostly young to middle- aged adults, representing an older demographic than the CRMO subset [17]. It may sometimes mimic osteomyelitis Figure 13: Artefact. Sagittal PDFS of the ring finger of a healthy due to its bony involvement and osteitis. -is is also usually volunteer demonstrating a failure of fat suppression at the tip of the polyostotic and classically affects the sternoclavicular joints, finger resulting in a false impression of marrow hyperintensity in first rib, sternomanubrial joint, and the anterior aspect of the the distal phalanx. -e adjacent subcutaneous tissue is also in- adequately suppressed (dash). vertebral bodies (Figure 16). 1.2.7. Iatrogenic Processes. Radiation osteonecrosis can occur following radiotherapy (30–50 Gy) due to a combi- nation of damage to osteoblasts, resulting in unopposed osteoclastic activity, and vascular injury [18]. -ere is an initial osteopenia or lysis, followed by a delayed and dis- organised bony repair at least 3 years following radiotherapy, resulting in trabecular disorganisation and patchy marrow density (Figure 17(a)). On MRI, the initial acute changes can be associated with marrow and soft tissue oedema, and these can be difficult to distinguish from osteomyelitis or tumour recurrence (Figures 17(b) and 17(c)). Radiotherapy treat- ment timing, duration, dose, and field are useful parameters in this setting along with previous, baseline imaging for comparison, as radiation osteonecrosis will be confined within the field of radiotherapy even when the borders of the abnormal bone are poorly defined [19]. Associated osteol- Figure 14: Sacroiliitis. Coronal STIR sequence of sacroiliac joints ysis, osseous expansion, or fistula formation is usually more (SIJ) of a 34-year-old male with right acute on chronic and left indicative of infection than osteonecrosis [19]. chronic sacroiliitis. -e region of the acute inflammatory process is Postoperative findings and sterile collections can often denoted by the marrow oedema signal in the cartilaginous com- be difficult to distinguish from infection and image inter- ponent of the right SIJ (arrow). Marrow fat infiltration (dotted pretation can be further complicated by the presence of arrow) adjacent to the left SIJ inferiorly implies prior inflammation. orthopaedic hardware which can lead to susceptibility and Irregular joint surface (dash) is consistent with erosion. field inhomogeneity artefacts (Figure 13). -e presence of metalware reduces the ability to adequately suppress the fat- course of the disease process. Early detection of sacroiliitis signal, simulating marrow and soft tissue oedema. Whilst using a combination of radiologic and clinical findings is various MRI techniques have been employed for artefact important since the condition usually responds well to reduction, nuclear medicine studies and, in particular, the 12 Radiology Research and Practice (a) (b) Figure 15: CRMO. Coronal whole-body MRI of an 8-year-old boy (a) with CRMO initially presenting with right knee pain. Note the multifocal involvement which included both knees, left ankle, and the sacrum (arrow). Axial STIR (b) of a different CRMO patient aged 7, with classic involvement of right medial clavicle with associated hyperostosis (arrow). (a) (b) Figure 16: A 27-year-old female with SAPHO. -ere is hyperostosis and osteitis of the sternomanubrial junction on the sagittal CT (a). Contiguous involvement of multiple vertebral bodies anteriorly with sparing of the intervening disc space as demonstrated on sagittal T1 thoracic spine is typical of this condition (b). Radiology Research and Practice 13 (a) (b) (c) Figure 17: Osteoradionecrosis. Orthopantomogram (OPG, (a)) of a 74-year-old male with a history of T3 oropharyngeal tumour having undergone prior resection and chemoradiotherapy, complicated by osteoradionecrosis. -ere is ill-defined lytic lucency eroding the right mandibular body with background coarsened trabeculation and patchy sclerosis. Axial T1 (b) and T2FS (c) of a different patient with a previous history of radiotherapy for skin SCC, presenting with a nonhealing ulcer due to osteoradionecrosis. -ere are T1 hypointensity and fluid-hyperintensity in the body of the right mandible ((a) arrow). Mild surrounding soft tissue oedema ((b) arrow). white cell scan remains the most valuable imaging modality to assess for infection around a prosthesis [20]. MRI plays a key role in the assessment of delayed- hypersensitivity reactions to arthroplasty-related metal products, known as pseudotumour or adverse reaction to metal debris. -is can lead to aggressive soft tissue de- struction if untreated. Imaging features include effusion with variable thickness of the synovial lining of synovial prolif- eration (Figure 18). It can be associated with perisynovial oedema and local nodal enlargement, mimicking infection. Figure 18: Adverse reaction to metallic debris (ARMD). A 70-year- Increased synovial thickness and T1 and T2-hypointensity old female with left hip resurfacing complicated by pseudotumour favour pseudotumour over infection [21]. formation. Axial T2 pelvis with metal artefact reduction technique demonstrating distension of the left hip pseudocapsule posteriorly (dotted line) and a larger anterior pseudocapsule defect decom- 1.2.8. Neuropathy. Neuropathic arthropathy most com- pressing into the iliopsoas bursa (arrow). -is thickened, T2- monly occurs in patients with altered pain sensation and hypointense rim with synovial proliferation favours pseudotu- proprioception resulting in the accumulation of mour/ARMD over infection. 14 Radiology Research and Practice (a) (b) (c) Figure 19: Lateral and oblique right foot radiographs (a) of a 47-year-old woman with type II diabetes and Charcot arthropathy involving the midfoot. Disorganised hindfoot with joint destruction and disorganisation (arrow). Note the absence of osteopenia that is typically observed in infection. Coronal STIR (b) and T1 (c) of a different patient with Charcot arthropathy with hindfoot destruction, hindfoot valgus, and dislocation. -e contrast was not administered due to chronic renal failure. -e talus is flattened and sclerotic (arrow). Note the fluid collection in the distal tibial shaft (dotted arrow) and the medial tibiotalar articulation. -is patient had both neuropathic arthropathy complicated by chronic osteomyelitis with intraosseous abscess formation. At times, different conditions can preexist, and ultimately, tissue sampling may be required. (a) (b) (c) Figure 20: Continued. Radiology Research and Practice 15 (d) Figure 20: Primary amyloidosis. A 64-year-old woman with known primary amyloidosis of lacrimal glands, initially presenting with neck pain. Sagittal T2 (a), T1 (b), and axial T2FS (c) spine shows an infiltrative process involving the C7 and T1 vertebrae with an extraosseous extension of soft tissue into the epidural and prevertebral spaces (arrow). End plate irregularity is also present. Axial T2FS (c) at the level of C7 demonstrating epidural and prevertebral soft tissue infiltration (arrow). -is case was difficult to distinguish from infection, ultimately requiring a biopsy for the final diagnosis of C7/T1 amyloid deposition. Axial T2 head at the level of the orbits (d) showed bilateral lacrimal gland enlargement secondary to amyloid deposition (arrow). (a) (b) Figure 21: A 49-year-old female with end stage renal failure and tertiary hyperparathyroidism. Sagittal lumbar spine (a) with bone reconstructions shows rugger-jersey spine with sclerosis adjacent to end plates (arrow) whilst axial pelvis (b) demonstrates subperiosteal resorption of the SIJs (arrow). microtrauma [22, 23]. It commonly occurs in the feet of process. Sclerosis on radiographs and stability of findings diabetic patients. In the acute stage, the foot may be over time favour Charcot neuropathy over infection. On the contrary, the contiguity of the marrow change with painful and erythematous, followed by bone dis- organisation, dislocation, secondary degeneration, and any ulcer or collection supports infection (Figures 1, debris formation with preservation of bone density, also 19(b), and 19(c). -e areas affected by osteomyelitis may known as the “Five Ds” (Figure 19). Features that favour be more conspicuous on contrast-enhanced sequences. neuropathy over osteomyelitis are periarticular marrow Various new techniques such as the use of diffusion- oedema-like signal, joint subluxation, and geode forma- weighted imaging (DWI), dynamic postcontrast en- tion, since neuropathy is predominantly an articular hancement, and perfusion may provide further useful 16 Radiology Research and Practice (a) (b) (c) (d) Figure 22: Calcific tendinitis in a 40-year-old female presenting with persistent shoulder pain. Axial PDFS (a) demonstrating marrow oedema signal in the humeral head at the greater tuberosity at teres minor tendon footprint. Sagittal PDFS (b) demonstrating corresponding cortical erosion. -e MRI performed 5 months previously at the comparable plane (c) showed globular hypointense structure within the teres minor tendon footprint (arrow), confirming intraosseous migration of the calcific tendinitis in the most recent images. AP radiograph of the right shoulder (d) performed at the time of initial presentation also demonstrated calcium deposition in rotator cuff tendons. -e calcium deposit is not well appreciated in the more recent study given the acute resorptive phase. information although the utility of these more advanced crystals can, at times, incite an inflammatory response techniques remains to be validated [22]. and result in bone erosion, mimicking infection. In the acute phase, soft tissue swelling and joint effusion can be present. More chronic crystal deposits are usually T1 and 1.2.9. Depositional Disease. Depositional disease such as T2 hypointense, without significant blooming artefact on amyloidosis can radiologically resemble an infection, ulti- susceptibility sequences that may otherwise suggest mately requiring biopsy for diagnosis (Figure 20). In patients pigmented villonodular synovitis (PVNS). Calcific with chronic renal insufficiency, aggressive spondylosis can phosphate can deposit within tendons and can provoke also occur due to amyloid deposition. Features of hyper- an acute inflammatory response in the resorptive phase, parathyroidism such as sclerosis adjacent to end plates during which the calcium can migrate into the adjacent (rugger-jersey spine) and subperiosteal or subligamentous bursa or bone, mimicking osteomyelitis (Figure 22). bone resorption can help clinch the diagnosis [24] Calcium at this phase may be oedematous and difficult to (Figure 21). depict on MRI. A radiograph can be useful for the as- Microcrystals can deposit in periarticular or intra- sessment of soft tissue calcification which may not be articular soft tissue. -is includes monosodium urate in apparent on MRI [25]. Dual-energy CTcan also be used in gouty arthropathy and calcium hydroxyapatite deposi- distinguishing gout from other calcium deposition tion. Most cases are usually asymptomatic although the (Figure 23). Radiology Research and Practice 17 (a) (b) Figure 23: Gouty tophus in a 39-year-old man presenting with a swollen and erythematous toe which was clinically suspected to be an st infection. X-ray showed 1 MTPJ erosion at the medial border associated with dense soft tissue swelling (arrow). Dual-energy CT with material decomposition helped differentiate urate crystals (mapped as green, arrowed) from calcium (blue, not present in this case). 2. Conclusion Acknowledgments -e imaging appearance of the bone and joint infections -e authors would like to thank Dr. Ricky Lu Shi Sheng for may be mimicked by many conditions. It is important to his contribution to the earlier version of the manuscript. consider other differentials when a specific clinical scenario is discordant from the imaging findings. Whilst it is always References important to consider the clinical picture and laboratory findings when interpreting radiologic findings, pertinent [1] Y. J. Lee, S. Sadigh, K. Mankad, N. Kapse, and G. Rajeswaran, information may not always be available. An appreciation of “-e imaging of osteomyelitis,” Quantitative Imaging in the overlap of these differential diagnoses with infection and Medicine and Surgery, vol. 6, no. 2, pp. 184–198, 2016. [2] J. Pupaibool, S. Vasoo, P. J. Erwin, M. H. Murad, and key differentiating factors equips the radiologist with the E. F. Berbari, “-e utility of image-guided percutaneous ability to make a significant contribution to diagnosis and needle aspiration biopsy for the diagnosis of spontaneous appropriate, timely management. vertebral osteomyelitis: a systematic review and meta-anal- ysis,” 6e Spine Journal, vol. 15, no. 1, pp. 122–131, 2015. [3] F. D. Beaman, P. F. von Herrmann, M. J. Kransdorf et al., Data Availability “ACR appropriateness criteria suspected osteomyelitis, septic No new data were used to support this study. arthritis, or soft tissue infection (excluding spine and diabetic foot),” Journal of the American College of Radiology, vol. 14, no. 5, pp. S326–S337, 2017. Ethical Approval [4] C. Pineda, A. Vargas, and A. V. Rodr´ıguez, “Imaging of osteomyelitis: current concepts,” Infectious Disease Clinics of Ethical approval and consent waiver were obtained via the North America, vol. 20, no. 4, pp. 789–825, 2006. institutional ethics board (CHCA-HREC Ref No. 20- [5] W. Lim and A. Saifuddin, “Review article: the differential CHREC-E012). diagnosis of bone marrow edema on wrist MRI,” Skeletal Radiology, vol. 48, no. 10, pp. 1525–1539, 2019. [6] C. Pineda, R. Espinosa, and A. Pena, “Radiographic imaging Conflicts of Interest in osteomyelitis: the role of plain radiography, computed tomography, ultrasonography, magnetic resonance imaging, -e authors declare that they have no conflicts of interest. 18 Radiology Research and Practice and scintigraphy,” Seminars in Plastic Surgery, vol. 23, no. 02, [23] E. A. Jones, B. J. Manaster, D. A. May, and D. G. Disler, pp. 080–089, 2009. “Neuropathic osteoarthropathy: diagnostic dilemmas and [7] M. Karchevsky, M. E. Schweitzer, W. B. Morrison, and differential diagnosis,” RadioGraphics, vol. 20, pp. S279–S293, J. A. Parellada, “MRI findings of septic arthritis and associated osteomyelitis in adults,” American Journal of Roentgenology, [24] M. J. Cobby, R. S. Adler, R. Swartz, and W. Martel, “Dialysis- vol. 182, no. 1, pp. 119–122, 2004. related amyloid arthropathy: MR findings in four patients,” [8] D. Resnick, G. Niwayama, J. Guerra Jr., V. Vint, and American Journal of Roentgenology, vol. 157, no. 5, J. Usselman, “Spinal vacuum phenomena: anatomical study pp. 1023–1027, 1991. and review,” Radiology, vol. 139, no. 2, pp. 341–348, 1981. [25] P. Omoumi, P. Zufferey, J. Malghem, and A. So, “Imaging in [9] R. Rahme and R. Moussa, “-e modic vertebral endplate and gout and other crystal-related arthropathies,” Rheumatic marrow changes: pathologic significance and relation to low Disease Clinics of North America, vol. 42, no. 4, pp. 621–644, back pain and segmental instability of the lumbar spine,” 2016. American Journal of Neuroradiology, vol. 29, no. 5, pp. 838– 842, 2008. [10] N. Boutry, C. Paul, X. Leroy, D. Fredoux, H. Migaud, and A. Cotten, “Rapidly destructive osteoarthritis of the hip: MR imaging findings,” American Journal of Roentgenology, vol. 179, no. 3, pp. 657–663, 2002. [11] M. D. Murphey, L. T. Senchak, P. K. Mambalam, C. I. Logie, M. K. Klassen-Fischer, and M. J. Kransdorf, “From the ra- diologic pathology archives: ewing sarcoma family of tumors: radiologic-pathologic correlation,” RadioGraphics, vol. 33, no. 3, pp. 803–831, 2013. [12] J. W. Chai, S. H. Hong, J.-Y. Choi et al., “Radiologic diagnosis of osteoid osteoma: from simple to challenging findings,” RadioGraphics, vol. 30, no. 3, pp. 737–749, 2010. [13] E. Smitaman, B. P. G. Pereira, B. K. Huang, M. M. Zakhary, E. Fliszar, and D. L. Resnick, “Abnormal bone marrow signal intensity in the phalanges of the foot as a manifestation of Raynaud phenomenon: a report of six patients,” American Journal of Roentgenology, vol. 207, no. 6, pp. 1252–1256, 2016. [14] M. Navallas, J. Ares, B. Beltran, ´ M. P. Lisbona, J. Maymo, ´ and A. Solano, “Sacroiliitis associated with axial spondyloarthr- opathy: new concepts and latest trends,” RadioGraphics, vol. 33, no. 4, pp. 933–956, 2013. [15] C. Tsoi, J. F. Griffith, R. K. L. Lee, P. C. H. Wong, and L. S. Tam, “Imaging of sacroiliitis: current status, limitations and pitfalls,” Quantitative Imaging in Medicine and Surgery, vol. 9, no. 2, pp. 318–335, 2019. [16] G. Khanna, T. S. P. Sato, and P. Ferguson, “Imaging of chronic recurrent multifocal osteomyelitis,” Radiographics, vol. 29, no. 4, pp. 1159–1177, 2009. [17] A. Cotten, R. M. Flipo, A. Mentre, E. Delaporte, B. Duquesnoy, and P. Chastanet, “SAPHO syndrome,” Ra- diographics, vol. 15, no. 5, pp. 1147–1154, 1995. [18] R. Hermans, “Imaging of mandibular osteoradionecrosis,” Neuroimaging Clinics of North America, vol. 13, no. 3, pp. 597–604, 2003. [19] P. M. Phal, R. W. T. Myall, L. A. Assael, and J. L. Weissman, “Imaging findings of bisphosphonate-associated osteonec- rosis of the jaws,” American Journal of Neuroradiology, vol. 28, no. 6, pp. 1139–1145, 2007. [20] C. J. Palestro, “Nuclear medicine and the failed joint re- placement: past, present, and future,” World Journal of Ra- diology, vol. 6, no. 7, pp. 446–458, 2014. [21] J. Fritz, B. Lurie, T. T. Miller, and H. G. Potter, “MR imaging of hip arthroplasty implants,” RadioGraphics, vol. 34, no. 4, pp. E106–E132, 2014. [22] T. M. Noguerol, A. L. Alcala, ´ L. S. Beltran, ´ M. G. Cabrera, J. B. Cabrero, and J. C. Vilanova, “Advanced MR imaging techniques for differentiation of neuropathic arthropathy and osteomyelitis in the diabetic foot,” RadioGraphics, vol. 37, no. 4, pp. 1161–1180, 2017.

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Published: May 24, 2021

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