Magnetic resonance imaging of musculoskeletal infections

Cellulitis

Cellulitis is an infection of the deep dermis and superficial subcutaneous tissues, and is typically of bacterial aetiology [1, 21-25]. The superficial fascial planes are commonly affected. Associated skin and soft tissue ulcerations may be present. The most common organisms are Staphylococcus aureus and Streptococcus pyogenes [26]. Cellulitis most often occurs from direct inoculation.

Cellulitis is most often a clinical diagnosis, because soft tissue oedema may result from trauma, lymphoedema, venous stasis, and cardiac insufficiency. MRI may be obtained to evaluate for associated abscesses or deep soft-tissue extension, involvement of the adjacent joint, or osteomyelitis [26-28]. MRI will show thickening of the skin and subcutaneous fat, with hypointense signal on T1W images and hyperintense signal on fluid-sensitive images, and variable enhancement following intravenous contrast administration (Figures 1, 2, 4B-D, 7, 8A, 8C, 9, 20] [1, 24-26, 28-31]. Cellulitis may show restricted diffusion on DWI sequences (Figures 2D-E) [32]. Ulcerations may be seen on MRI as defects on the skin surface, with variable degrees of communication with the deeper soft tissue and bone, and are usually hyperintense on fluid-sensitive images, with peripheral enhancement following intravenous contrast (Figures 17B-D) [31, 33, 34].

Cellulitis is treated with antibiotics and debridement as needed. Wound care is needed for ulcerations.

Abscess/phlegmon

An abscess is a focal fluid collection containing inflammatory cells, bacteria, and necrotic tissue debris surrounded by hypervascular, inflamed connective tissue [1, 25]. A phlegmon is defined as enhancing infected granulation tissue, frequently surrounding an abscess. An abscess may be located in either the superficial or the deep soft tissues and may occur secondarily to direct inoculation, a pre-existing foreign body, contiguous spread from an adjacent infection, or from hematogenous spread [1-3, 35-37].

On MRI, an abscess will have increased signal on fluid sensitive sequences, decreased signal on T1W images, and will show peripheral enhancement following intravenous contrast administration (Figures 1, 2, 3, 11, 13B, 14, 16D, 18D]. Gas within an abscess will be seen as low signal on all sequences with a susceptibility artifact that is exaggerated on gradient echo sequences. Abscesses are often surrounded by hyperaemic phlegmonous tissue, which will be increased in signal on fluid-sensitive sequences and show enhancement on the post-contrast sequences (Figures 2C, 16D). The “penumbra sign”, or the presence of a thin rim of hyperintense signal along the periphery of the abscess, on T1W images has been described to help differentiate soft tissue abscesses from necrotic tumours (Figure 2B) [38].

On DWI, purulent material with an abscess will restrict the free diffusion of water molecules, resulting in high diffusion signal on fractional anisotropy/trace images and low apparent diffusion coefficient (ADC) map signal intensity, which is particularly useful in patients who cannot receive gadolinium-based contrast agents due to impaired renal function or contrast allergy (Figures 2D-E, 11C-D] [25, 39-42]. Use of DCE MRI to differentiate viable tissue, which enhances, from necrotic tissue, which does not enhance, has been described [41].

Treatment for abscess is dependent on size and location, and includes percutaneous drainage, surgical debridement, and intravenous and oral antibiotics.

Myositis/pyomyositis

Myositis is a non-specific term for muscular inflammation, the aetiology of which may be an infectious process. Pyomyositis is a bacterial infection of skeletal muscle, which leads to muscle oedema and often phlegmon formation followed by abscess formation [1, 26, 43, 44]. Previously seen mainly in tropical climates, pyomyositis is increasing in frequency in temperate climates [44-46]. Trauma is the leading cause (25-40%) of pyomyositis in temperate climates, although haematological seeding from adjacent infection is also possible [44, 46, 47]. Pre-existing muscular injury (muscle trauma such as haematoma, underlying myositis, strenuous physical activity) can predispose to pyomyositis [26, 44, 46-49].

On MRI, pyomyositis will demonstrate muscular oedema and enlargement, with increased signal on fluid sensitive sequences and variable enhancement on the post-contrast sequences (Figures 2 and 3). Phlegmon and abscesses may be present. Adjacent bones and joints should be scrutinized for osteomyelitis and septic arthritis, respectively. DWI of the abscess cavity will show restricted diffusion centrally; however, there is often increased diffusion in the surrounding muscle due to inflammation and expanded extracellular space (Figures 2D-E) [32]. Treatment for pyomyositis is dependent on size and location, and includes percutaneous drainage, surgical debridement, and intravenous antibiotics [44].

Diabetic myonecrosis is a non-infectious process that may mimic pyomyositis [1, 24, 26, 36]. Patients often have a long-standing history of uncontrolled diabetes and may develop muscular infarcts that often involve entire muscles and may be bilateral [1, 24, 50, 51]. Diabetic myonecrosis is more common in the lower extremities, particularly involving the quadriceps and the anterior thigh muscles [23, 24, 26] MRI will show subcutaneous, perifascial and muscular oedema as well as perifascial fluid of high signal on fluid sensitive sequences, and rim-enhancing areas of intramuscular non-enhancement in the regions of infarcts on the post-contrast sequences (Figure 5) [23, 24, 26, 29, 51, 52]. Diabetic myonecrosis can be distinguished from abscess by the clinical presentation, and patients with diabetic myonecrosis should not have an elevated white blood cell count nor elevated inflammatory markers; however, diabetic myonecrosis can be complicated with superinfection. Diabetic myonecrosis without associated infection is treated with medical management.

Superficial, deep, and necrotizing fasciitis

In infectious fasciitis, both the superficial and the deep fascia may be infected, and the cause of infection is usually direct inoculation from trauma. Necrotizing fasciitis is a severe, rapidly progressive, potentially fatal subtype of infectious fasciitis that typically occurs in immunocompromised patients (Figure 21) [22, 23, 26, 28, 29, 53-57]. Most infections are polymicrobial, often with Clostridium species and gram-positive cocci [2, 26, 28, 29, 54, 58]. The lower extremities are involved in 50% of cases [25, 56]. Necrotizing fasciitis may be secondary to direct inoculation or may arise secondarily to direct spread from a perforated viscus or urogenital organ [59]. The resulting tissue ischaemia and liquefactive necrosis may spread rapidly, up to an inch per hour [59]. The overall morbidity and mortality rate is 30-80% [24, 29, 54, 56].

Figure 21

Necrotizing fasciitis of the lower leg in a 40-year-old male patient. Lower leg photograph shows marked discoloration of the skin with an area of necrosis (arrows). Courtesy of Jordan Smith, Tuscon, Arizona

In infectious fasciitis, on MRI the affected fascia will be thickened, with increased signal on fluid sensitive sequences and variable enhancement following intravenous contrast administration (Figures 3A-C, 4B-D] [1, 36, 60, 61].

Patients suspected of having necrotizing fasciitis should undergo immediate surgical evaluation rather than imaging (Figure 21). Radiographs and computed tomography (CT) examinations are less time-intensive than MRI and will readily demonstrate soft-tissue gas (Figure 4A). On MRI, there is dermal and soft tissue thickening, with reticulated increased signal intensity on fluid-sensitive sequences and variable signal intensity on T1W images along the deep fascial planes, which are often thickened and show heterogeneous enhancement following intravenous contrast administration; gas is variably present, and the absence of gas does not exclude the diagnosis (Figures 4B-D) [1, 24, 25, 29, 53, 54, 56, 59]. The lack of contrast enhancement may be due to hypoperfusion and tissue necrosis, which may underestimate the disease extent. Subcutaneous oedema may be present but is less common than in cellulitis [29]. In the early stages, the muscles are spared [53, 55]. Kim et al. showed that patients with necrotizing fasciitis have ≥ 3 mm of thick fascial oedema on T2W FS images, extensive involvement of the deep fascia (often with low signal intensity on T2W FS images and areas of non-enhancement), and involvement of 3 or more compartments in 1 extremity when compared to patients with non-necrotizing fasciitis [22, 23, 26, 28, 57, 58, 62].

The differential diagnosis includes other forms of non-infectious fasciitis including paraneoplastic, eosinophilic, and nodular fasciitis [29], and venous obstruction. Distinguishing infectious from non-infectious fasciitis is based mainly on distribution and clinical presentation [29].

Superficial fasciitis often occurs with cellulitis and is treated with antibiotics. Deep fasciitis also may be treated with antibiotics, and surgical intervention is reserved for unresponsive cases [1]. Necrotizing fasciitis is a surgical emergency and is treated with prompt debridement, fasciotomy, and antibiotics [1, 2, 24, 36, 53, 54, 59]. Skin grafting and hyperbaric oxygen therapy are occasionally needed [2, 59].

Acute compartment syndrome results from a prolonged increase in intramuscular pressure with decreased arterial pressure, often affecting the anterior and lateral compartments of the leg, and it usually occurs secondary to prolonged ischaemia, fractures, and crush injuries [24, 29]. When intramuscular pressures increase above 15- 20 mmHg, capillary perfusion and lymphatic flow are impaired, resulting in ischaemic muscular injury [24]. Interstitial oedema from capillary leakage also results in decreased muscle perfusion [24]. An interstitial tissue pressure of 30 mmHg is the typical threshold at which the diagnosis of compartment syndrome should be considered [1, 29].

On MRI, there is low muscular signal on T1-weighted images and a diffuse increase in muscular signal intensity on fluid-sensitive images, with variable contrast enhancement [24, 29]. Treatment of acute compartment syndrome is fasciotomy and decompression [24, 29].

Infectious bursitis

Bursitis is most often non-septic, and it is often caused by repetitive trauma, crystal deposition, and inflammatory arthropathies [26, 63, 64]. Infectious bursitis is most commonly due to bacterial organisms, but may be due to fungal, tuberculous, or atypical mycobacterial aetiologies. Septic bursitis may occur due to either direct inoculation or spread from an adjacent infection, such as a pre-existing inflamed bursa; haematogenous spread is much less common [26, 63, 65, 66]. Superficial septic bursitis is more common than deep septic bursitis [66]. The olecranon and prepatellar bursae are most commonly affected, and approximately one third of olecranon and prepatellar bursitis are septic [1, 26, 63-66]. Iatrogenic septic bursitis can be caused by attempted aspiration or injection of a non-infected bursa [66].

On MRI, infectious bursitis should be considered when the bursa is distended with either fluid, which may be simple or complex, and/or enhancing synovitis (Figure 6). Simple fluid is hypointense in signal on T1W images and hyperintense signal on fluid sensitive images, and demon-strates smooth, thin peripheral synovial enhancement following intravenous contrast administration. If the fluid is complex, due to the presence of blood or debris, it will have a more heterogeneous appearance. Active infectious or inflammatory synovitis will show thick enhancement on post-contrast sequences. If foci of internal low signal are present, the presence of gas should be considered. The peribursal soft tissues may be oedematous, and overlying cellulitis is often present [1]. There may be a sympathetic effusion in an adjacent joint [65]. Septic bursitis may show restricted diffusion on DWI [32].

Superficial infectious bursitis is usually treated with antibiotics, often empirically to avoid iatrogenic infection from aspiration [67]. Percutaneous drainage and surgical bursectomy are reserved for extremely distended bursae and refractory cases that do not respond to antibiotic therapy [1, 65, 68].

Infectious tenosynovitis

Infectious tenosynovitis usually occurs from direct inoculation from penetrating trauma or from extension of adjacent infection [1, 26, 68, 69]. This is most frequently due to bacterial infection but may also be secondary to fungal, tuberculous, and atypical mycobacterial aetiologies [1, 26, 69].Retained foreign bodies may complicate tenosynovitis [69]. Tendon necrosis may occur in the absence of appropriate treatment [69]. Infectious tenosynovitis is important to detect because it may allow rapid migration of organisms from one anatomic region to another.

On MRI, infectious tenosynovitis should be considered when the tendon sheath is distended with simple or complex fluid collections, accompanied by variable thickness and irregular synovial enhancement, frequently with adjacent cellulitis (Figures 7E-G). If foci of diffusely low signal are present, the presence of gas should be considered. The adjacent tendon may become thickened and have an indistinct signal [1, 31-34]. DWI may show restricted diffusion in infectious tenosynovitis [32]. Clinical history and laboratory values can help differentiate septic tenosynovitis from inflammatory teno-synovitis.

In the hand, pyogenic tenosynovitis of the flexor tendons is a particularly challenging closed-space infection given the complex anatomy of the ulnar and radial bursae. The radial bursa is in continuity with the flexor pollicis longus tendon sheath, and the ulnar bursa frequently communicates with the little- or ring-finger flexor tendon sheaths. The index- and middle-finger tendon sheaths typically do not communicate with these bursae. The variability in bursal and tendon sheath interconnections in the hand and the space of Parona, located between the fascia of the pronator quadratus muscle and the flexor digitorum profundus tendons in continuity with the carpal tunnel, allows for rapid spread of infection [70].

Early infectious tenosynovitis is often managed with antibiotics and elevation, with surgical decompression often necessary if there is no improvement within 24 hours [1, 68, 71].

Infectious lymphadenitis

Infectious lymphadenitis is inflammation of the lymphatic system, often caused by a bacterial infection, or less likely a parasitic or mycobacterial infection [72]. Gram-positive bacilli such as group A streptococci are the frequent causative organisms [72, 73].

MRI will show enlarged lymph nodes, often with adjacent soft tissue oedema (Figure 3D) [74]. Acute bacterial lymphadenitis is typically treated with antibiotics.

Osteomyelitis: acute, subacute, and chronic

Osteomyelitis is infection of the bone marrow, which may occur due to haematogenous dissemination from a distant site, by direct inoculation from trauma, or via spread from an adjacent soft tissue infection; the most common causative agent is Staphylococcus aureus [20, 30]. Haematogenous osteomyelitis is more common in children [20]. In adults, haematogenous osteomyelitis occurs more commonly within the spine, pelvis, and small bones, and is often secondary to bacteraemia from endocarditis, genitourinary infections, gastrointestinal infections, or intravenous drug use [75, 76]. Direct inoculation is usually secondary to penetrating trauma or open fracture.

Osteomyelitis may be acute, subacute, or chronic (Figures 6, 7, 8, 9, 13, 14, 16, 22). In the acute phase, there is osseous hyperaemia and oedema, with resulting osseous demineralization, destruction of bony trabeculae, and replacement of the normal bone marrow fat with neutrophilic infiltrate [75]. Subperiosteal abscess formation can occur in the setting of osteomyelitis, more commonly in children than in adults (Figures 8 and 22). Subperiosteal abscesses are thought to occur from outward extension of infection from the cortex or as a result of direct inoculation from trauma or surgery [77, 78].

MRI is highly sensitive and specific in the diagnosis of osteomyelitis. A systematic review by Llewellyn et al. showed that in adults, MRI had 95.6% sensitivity and 80.7% specificity for the diagnosis of osteomyelitis [79]. A recent meta-analysis by Llewellyn et al. showed MRI to have 96.4% sensitivity and 83.8% specificity for the detection of osteomyelitis in people with diabetic foot ulcers [80]. On MRI, acute osteomyelitis is characterized by bone marrow and periosteal oedema, which shows high signal intensity on fluid-sensitive sequences, decreased/intermediate signal with bone marrow effacement on the T1W images, sometimes with interspersed foci of preserved marrow fat, and enhancement on the postcontrast sequences (Figures 6, 7B-G, 8, 9B-D, 13, 14, 16B-D, 18B-D]. Adjacent enhancing soft-tissue oedema is typically present. Intraosseous and subperiosteal abscess and areas of necrosis do not enhance (Figure 8) [14, 75]. On DWI, intraosseous and subperiosteal abscesses may show restricted diffusion [23, 32].

In subacute and chronic osteomyelitis, an intra-osseous abscess can form, with resulting necrosis of a portion of the bone, known as a Brodie abscess (Figures 9, 10, 22) [14, 76]. Brodie abscesses may be intramedullary or cortical. Cortical Brodie abscess is characterized with central necrosis in an area of cortical thickening while an intramedullary Brodie abscess is characterized by a necrotic centre surrounded by peripherally ill-defined sclerosis.

Chronic osteomyelitis, often defined as lasting more than 6 weeks, is manifested by osteonecrosis surrounded by persistent infection (Figures 9 and 22). The fragment of the infected necrotic bone, known as the sequestrum (Figures 9 and 22), develops after approximately 30 days and serves as a reservoir for bacteria. The sequestrum is most specific for chronic osteomyelitis and is separated from the living bone by granulation tissue, surrounded by reactive new bone formation, known as an involucrum (Figures 9 and 22). A periosteal defect/opening in the involucrum is known as a cloaca (Figures 9 and 22). The continuous sinus/fistulous tracts eventually extend to the skin surface [14, 30, 75, 76]. Malignant transformation within the draining sinus tract to squamous cell carcinoma can occur in longstanding chronic osteomyelitis with the reported incidence of less than 0.5% [14].

In subacute osteomyelitis, there may be a thick rim of vascularized granulation tissue along the periphery of the intraosseous abscess, with hyperintense signal on T1W images, known as the “penumbra” sign (Figure 10C) [14, 38, 81]. The penumbra sign has a specificity of 96% for the presence of infection with a sensitivity of 27% [14, 38, 81].

In chronic osteomyelitis, the sequestrum will be of low signal on all sequences, with surrounding high signal granulation tissue on fluid-sensitive sequences, which may eventually become low signal on all sequences due to the formation of avascular, necrotic tissue (Figures 9B-D) [75, 76]. The surrounding involucrum and thickened periosteum have low signal on all sequences (Figures 9B-D). The cloaca will be an intermediate to high signal tract from the sequestrum through the involucrum on fluid-sensitive images (Figure 9B-D). Sinus tracts may be present from the skin surface to the infected bone. The walls of the sinus tract will enhance. Infected bone will enhance; necrotic bone will not enhance. The treatment of chronic osteomyelitis is often surgical, with resection of the sequestrum, debridement of infected bone, and intravenous antibiotics [14].

In the adult spine, osteomyelitis typically occurs in the vertebral body endplate from hematogenous spread and extends into the disc and eventually the contralateral vertebral body endplate; in the paediatric patient, infection tends to originate in the disc, because it is more vascularized [30, 40]. MRI findings are dependent on the causative agent, but initially include loss of the vertebral body hypointense cortex on both T1W and fluid-sensitive images [40]. Additional MRI findings include bone marrow oedema signal on fluid-sensitive images, fatty marrow effacement with low signal on T1W images, and enhancement following contrast administration in the vertebral body endplate, with high signal oedema on fluid-sensitive images and enhancement in the disc (Figures 11, 13, 14)[30, 39, 40]. Epidural and paraspinous phlegmons and abscesses may form (Figures 11A-D) [39, 40]. DWI can help differentiate acute discitis-osteomyelitis from Modic I degenerative changes, which can look similar on MRI (Figures 11E-F, 12, 14C-D] [40, 82]. On sagittal DWI of the spine, a discrete edge of diffusion hyperintensity in the region of bone marrow oedema suggests Modic Ichanges (“claw sign”) (Figure 12) [82]. Diffuse and ill-defined margins of diffusion hyperintensity within bone marrow oedema suggests discitis-osteomyelitis (“reverse claw sign”) [40]. Adjacent psoas muscle infection also suggests discitis-osteomyelitis.

Chronic recurrent multifocal osteomyelitis (CRMO) is an inflammatory non-infectious autoimmune osteomyelitis that occurs more commonly in children (Figure 15) [75, 83]. Patients most often present with osteolytic lesions, periostitis, soft tissue oedema, and eventual osseous sclerosis [75]. Lesions are often bilateral and symmetrical [75]. Clavicular involvement is common; the metaphyses and epiphyses of the femur, tibia, and humerus are also frequently affected (Figure 15) [75, 83].

Septic arthritis

Septic arthritis is an infection of the joint which may occur from direct trauma, pre-existing hardware, operative intervention, and hematogenous spread. It most commonly affects the large joints that have a rich blood supply, such as the hip, shoulder, and knee [23, 25]. Septic arthritis occurs most frequently in individuals under 3 years old and over 55 years old [84]. An infectious aetiology should always be considered in patients with a monoarticular arthritis. Predisposing factors include underlying inflammatory arthropathy, prior trauma, recent surgical intervention, pre-existing hardware, use of immunosuppressive drugs, and underlying medical conditions such as diabetes mellitus and cirrhosis [15]. The gold standard for diagnosing septic arthritis is arthrocentesis with culture.

Bacterial arthritis may lead to rapid joint destruction with loss of function, within 24-48 hours of onset [15, 23, 69]. Delay in diagnosis may result in significant bone and cartilage destruction, osteonecrosis, secondary osteoarthritis, and eventual osseous ankylosis [85]. In children, septic arthritis can lead to premature or asymmetrical closure of the growth plate, with subsequent limb length discrepancy and angular deformities, which may require future surgical interventions [16].

Children with septic arthritis often have associated osteomyelitis and adjacent soft-tissue infections [15, 86-88]. Criteria established by Kocher et al. are useful in differentiating septic arthritis in children with an inflamed hip from other aetiologies such as transient synovitis [15, 88, 89]. They include non-weight bearing, temperature greater than 38.5^oC, white blood cell count greater than 12,000 cells/ mm³, and erythrocyte sedimentation rate greater than 40 mm/hour. The presence of 1 criterion has a 3% probability, 2 criteria have a 40% probability, 3 criteria have a 93% probability, and 4 criteria have a 99% probability of septic hip.

On MRI, a septic joint will usually have joint effusion and thick enhancing synovitis (Figures 6, 7B-G, 18) [25, 90]. MRI findings of osteomyelitis often will be present in the adjacent bones, with high signal intensity bone marrow oedema present on fluid-sensitive images, low signal from effacement of the normal fatty marrow on T1W images, with marrow enhancement following the administration of intravenous gadolinium-based contrast (Figures 6, 7B-G, 18]. Osseous erosions and bone destruction may be present (Figures 6 and 7) [85]. Cartilage loss is also possible, with defects best appreciated on the fluid-sensitive images. There may be inflammatory changes in the adjacent soft tissues, including subcutaneous, fascial, and muscular oedema without or with abscess formation, bursitis, and tenosynovitis (Figures 6, 7, 18) [30]. In a septic joint, the purulent and pus-like intra-articular fluid may show restricted diffusion on DWI [23, 32].

Treatment of septic arthritis includes antibiotics combined with joint irrigation and debridement.