High-resolution ultrasound in the evaluation of musculoskeletal infections

Cellulitis (Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 8) refers to infection of the epidermis, dermis, hypodermis, and occasionally the superficial fascia, often with broken skin and skin ulceration^{(1,2,25–27)}. Usually occurring due to direct inoculation, Staphylococcus aureus and Streptococcus pyogenes are the most common causative organisms^(2,9,28,29). Clinically, patients present with soft tissue swelling, pain, and erythema.

A phlegmon is infected granulation tissue, while an abscess (Fig. 2, Fig. 3) is an infected organized focal fluid collection of debris and inflammatory cells surrounded by hyperemic connective tissue^(1,2,27,29). These may result from direct inoculation, contiguous spread from an adjacent infection, or hematogenous spread^(1,3,30). A retained foreign body (Fig. 1) predisposes to phlegmon/abscess formation. Over time, a phlegmon may organize into a defined abscess collection, which may be amenable to imageguided aspiration or drain placement.

Myositis is nonspecific muscular inflammation, which may be infectious, inflammatory, or traumatic in nature. Pyomyositis (Fig. 3) is a bacterial, mycobacterial or fungal infection of skeletal muscle, usually caused by Staphylococcus aureus, resulting in muscular edema and often phlegmon and abscess formation^{(1,2,26,28,31)}. Patients with underlying muscle injury are at an increased risk of developing pyomyositis^{(20,28,31,32)}. Underlying systemic illnesses, such as human immunodeficiency virus infection, diabetes mellitus, malnutrition, hematologic malignancy, and organ transplantation, also increase the risk of pyomyositis^{(18,28,29,33)}. Although any skeletal muscle may be involved, the quadriceps, gluteal, and iliopsoas musculature are most commonly affected^{(20,27,28,32,33)}.

Infectious fasciitis (Fig. 4) is usually secondary to direct inoculation and can involve both the superficial and deep fascial layers.

Necrotizing deep soft tissue infection/fasciitis (Fig. 4) is a rapidly progressive, often fatal infectious fasciitis, usually polymicrobial, frequently caused by Clostridium species and gram-positive cocci^(2,28,30,34). Mortality rates of necrotizing fasciitis range from 15 to 80%, usually due to sepsis or multisystem organ failure^(30,35). Clinically, patients present with fever, erythematous skin, and pain. Pain is often reported to be out of proportion to the physical examination findings. Crepitus, as well as eventual skin bullae and necrosis, may be present^(28,36). The lower extremities are most commonly affected, representing approximately 50% of cases^(28,37).

Bursitis is most often non-infectious, secondary to repetitive trauma, crystal deposition, and inflammatory arthropathies^(2,28,38,39). Infectious bursitis (Fig. 5) is most commonly due to bacterial organisms, usually from either direct inoculation or spread from an adjacent infection^{(2,28,38,40,41)}. Superficial bursae, such as the olecranon and prepatellar bursae, are more likely to become infected than are deep bursae, as they are more susceptible to direct inoculation from minor trauma^{(1,2,9,28,38–41)}.

Infectious tenosynovitis (Fig. 6) is typically bacterial in etiology, but may also be secondary to atypical mycobacterial, fungal, or tuberculous etiologies. Infectious tenosynovitis usually occurs as a result of either penetrating trauma, often a puncture wound or human, insect, or animal bite, or extension of adjacent infection, and most commonly involves the hands^{(1,2,9,28,29,42)}. Prompt diagnosis is essential to prevent complications such as tendon necrosis and rapid spread of infection^(9,42). This is particularly true in the flexor tendons of the hand and wrist, where pyogenic tenosynovitis can spread rapidly due to variability in bursal and tendon sheath interconnections in the hand and communication of the space of Parona (a potential space along the volar aspect of the forearm and wrist between the flexor digitorum profundus and flexor pollicis longus tendons, and the pronator quadratus muscle) with the carpal tunnel⁽⁴²⁾. Distinguishing infectious from inflammatory tenosynovitis can be difficult, however, typically, internal debris occurs with infectious tenosynovitis.

Septic arthritis (Fig. 7, Fig. 8), or infection of the joint, may occur secondary to direct trauma, hematogenous spread, or may result from indwelling hardware or surgical procedures. Predisposing factors include prosthetic joints as well as underlying medical conditions, such as immunosuppression, diabetes mellitus, cirrhosis, and inflammatory arthropathy^(2,7,25). Septic arthritis occurs most frequently in patients under the age of three and over the age of 55 years⁽⁴³⁾, and most commonly affects the large joints such as the hip, shoulder, and knee, due to their robust vascularity^(25,27). Bacterial arthritis may result in rapid bone and cartilage destruction, with eventual osteonecrosis, secondary osteoarthritis, and osseous ankylosis^(7,9,25).

Septic arthritis should be suspected in patients presenting with an acute monoarticular involvement. Patients typically report a painful joint with associated erythema, swelling, fever, and elevated WBC count and inflammatory markers. Arthrocentesis with culture is needed for definitive diagnosis of septic arthritis.

In the pediatric population, septic arthritis often occurs with osteomyelitis, commonly in joints where the metaphysis is intraarticular, such as the hip and shoulder^{(7,18,44–46)}. The differential diagnosis in children with an acutely painful hip with limp includes trauma, transient synovitis, neoplasm, inflammatory arthritis, osteonecrosis, and septic arthritis⁽⁴⁷⁾. The Kocher criteria are helpful in differentiating septic arthritis from transient synovitis^{(7,19,21,46–48)}. They include non-weight bearing, temperature greater than 38.5 degrees C, WBC count greater than 12,000 cells/mm³, and ESR greater than 40 mm/hour. The presence of one criterion has a 3% probability, two criteria have a 40% probability, three criteria have a 93% probability, and four criteria have a 99% probability of septic hip.

Osteomyelitis (Fig. 9, Fig. 10, Fig. 11, Fig. 12) is infection of the bone marrow, and may be acute, subacute, or chronic in nature. US has limited utility in the diagnosis of osteomyelitis but may be helpful in detecting subperiosteal spread of infection (subperiosteal abscess). Subperiosteal abscess formation (Fig. 9, Fig. 10) is more common in children due to the less adherent periosteum and is thought to be secondary to either extension of infection from the medullary cavity through the cortex or from direct inoculation^(2,19,49,50). In chronic osteomyelitis (Fig. 11, Fig. 12), US may be helpful in identifying cortical defects and sequestrations, as well as sinus tracts extending from the skin surface to the underlying infected bone⁽⁵⁰⁾.

When evaluating for soft tissue infections, high-frequency linear array transducers are typically used (10 MHz and greater), although lower frequency transducers may be needed for the evaluation of deeper soft tissues. In patients with large body habitus, a curvilinear transducer of less than 10 MHz is often needed to evaluate deep structures such as the hip⁽⁵¹⁾. A large amount of US gel, acoustic standoff pad, or water bath may be useful for visualizing superficial structures. Transducer pressure can be utilized to assess the compressibility of fluid. Imaging of the contralateral body part for comparison is often helpful. Color and/or power Doppler interrogation should be utilized to evaluate for increased vascularity when infection is suspected. Care should be taken to avoid excessive transducer pressure, as it can obscure subtle increase in color and power Doppler signal.

Microvascular flow imaging (MVFI) (Fig. 7 B) is a newer technique that uses filters to reduce artifacts from random motion, creating greater sensitivity to low-velocity flow in small vessels⁽⁵²⁾. As a result, MVFI is more sensitive in detecting small vessels compared to the color, power, and spectral Doppler modalities⁽⁵²⁾.

The American College of Radiology (ACR) Appropriateness Criteria endorse radiographs as the initial imaging modality in the setting of “suspected osteomyelitis or septic arthritis or soft tissue infection (excluding spine and diabetic foot)”⁽⁵³⁾. US of the area of interest is considered “usually appropriate” as the next imaging evaluation with normal radiographs or with radiographic findings “suggestive of joint effusion or soft tissue swelling”⁽⁵³⁾. US is considered “usually appropriate” when there is suspected soft tissue infection with a puncture wound and possible retained foreign body and normal radiographs⁽⁵³⁾.

ACR Appropriateness Criteria state that US of the area of interest “may be appropriate” as the next imaging examination for “suspected osteomyelitis or soft tissue infection with implanted extra-articular surgical hardware” with normal radiographs or with radiographic findings “suggestive of osteomyelitis or soft tissue infection with implanted extraarticular surgical hardware”⁽⁵³⁾. US of the area of interest “may be appropriate” as the next imaging examination for “suspected septic arthritis with arthroplasty or other implanted intraarticular surgical hardware” in the setting of normal radiographs or radiographic findings “suggestive of septic arthritis with arthroplasty or other implanted intraarticular surgical hardware”⁽⁵³⁾. US “may be appropriate” when radiographs show soft tissue gas, without a history of puncture wound, when there is clinical suspicion of necrotizing deep soft tissue infection, although these patients often undergo surgical exploration rather than additional imaging⁽⁵³⁾.

In the pediatric population, the ACR Appropriateness Criteria consider US of the area of interest as “usually appropriate” in children younger than five years of age with concern for osteomyelitis or septic arthritis of the extremity as the initial imaging, as well as the next imaging study following radiographs⁽¹⁹⁾. US of the area of interest is also considered “usually appropriate” in children 5 years of age or older with concern for osteomyelitis or septic arthritis involving an extremity⁽¹⁹⁾. US-guided aspiration is also considered “usually appropriate” in children with one or more clinical signs concerning for septic arthritis⁽¹⁹⁾.

On US, cellulitis (Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 8) typically manifests as dermal thickening and subcutaneous edema which shows streaks of hypoechoic or anechoic fluid, with indistinct tissue planes^(1,27,54). Color and power Doppler interrogation shows hypervascularity in the affected region. Thin, linear fluid deposits are frequently present along interlobular septa and along hyperechoic fat lobules, creating a “cobblestone” appearance^{(1,9,27–29,54–56)}. US is helpful to evaluate for associated deep venous thrombosis or superficial thrombophlebitis (Fig. 2), as well as underlying abscess formation (Fig. 2, Fig. 3)^(25,27,28). Thrombosed vessels (Fig. 2) are not compressible with transducer pressure. In acute thrombosis, the vessel is often distended by hypoechoic thrombus, and collateral vasculature is not present. In chronic thrombus, the vessel often exhibits an irregular, narrowed lumen containing echogenic thrombus, with surrounding collaterals frequently present.

On US, a phlegmon is a heterogeneous, ill-defined, often hypoechoic region within the soft tissue, typically with hyperemia⁽⁵⁴⁾. In contrast, an abscess (Fig. 2, Fig. 3) appears as a more well-marginated, focal fluid collection of mixed echogenicity depending on contents, with variable septations, and posterior acoustic enhancement. Abscesses are often surrounded by a thickened, hyperechoic wall which is hyperemic with color or power Doppler interrogation^{(9,20,27,55–57)}. There is typically edema and hyperemia in the adjacent soft tissues. If gas is present within the abscess or the adjacent soft tissues, it will appear as small echogenic foci with ring down artifact consistent with reverberation artifact (Fig. 4 C–E)^(29,56,57). Swirling purulent material may be noted with application of transducer pressure to the abscess^(9,56).

On US, intramuscular abscesses (Fig. 3) are focal fluid collections located within a muscle, often of mixed echogenicity with septations, and usually with a thickened hyperechoic and hyperemic margin^(1,18,29,33). The adjacent soft tissues are typically hyperemic and edematous. If gas is found within the abscess, hyperechoic foci with reverberation artifact/dirty shadowing may be present (Fig. 4 C–E)^(1,18).

Due to the high fatality rate without prompt diagnosis and treatment, patients suspected of having necrotizing deep soft tissue infection/fasciitis typically undergo immediate surgical evaluation rather than time-intensive imaging. Radiographs and CT can demonstrate soft tissue gas (Fig. 4 A–B).

With US, the affected fascia will be thickened and distorted, with hypoechoic fluid along the fascial layers (Fig. 4)^{(34,36,37,55)}. Lin et al. showed that fluid collections along the deep fascia greater than 2 mm in depth have an accuracy of approximately 73% in the diagnosis of necrotizing fasciitis⁽³⁶⁾. If soft tissue gas is present, there will be several hyperechoic foci with reverberation artifact/dirty shadowing (Fig. 4 C–E)^(29,37). Muscle edema may also be visualized.

On US, an infected bursa is surrounded by peribursal edema, and is distended, with mixed echogenicity fluid with possible internal debris and septations (Fig. 5)^(9,28). The bursal wall is typically thickened, with hyperemia noted on color or power Doppler evaluation (Fig. 5)^(1,9,29,57).

On US, a thickened tendon sheath distended with abnormal anechoic or hypoechoic collection indicates tenosynovitis (Fig. 6). The tendon may appear enlarged and hyperemic^(9,18,29). Simple fluid can be differentiated from synovitis using color and power Doppler interrogation, with associated hyperemia consistent with active tenosynovitis (Fig. 7)^(5,55). There is often thickening, edema, and hyperemia of the adjacent subcutaneous tissues⁽¹⁸⁾.

On US, a joint effusion is an abnormal hypoechoic or anechoic intraarticular collection that is compressible without detectable color or power Doppler signal⁽²¹⁾. Infected or inflamed joint effusions often have heterogeneous echogenicity with irregular, hyperechoic synovial thickening (Fig. 8)^(21,54). If active synovitis is present, the joint collection is typically hypoechoic, poorly compressible, with increased color or power Doppler signal, consistent with hyperemia and active inflammation (Fig. 8)⁽⁵⁾. Periarticular hyperemia may also be seen on color and power Doppler imaging.

In children, US can detect hip effusions and joint fluid as small as 1 ml; in patients with septic arthritis of the hip with symptoms of less than one day, the initial US may be falsely negative due to lack of accumulation of detectable fluid^(19,21). In pediatric US examinations, the distance between the anterior femoral neck cortex and the joint capsule should be less than 5 mm, and should not be more than 2 mm thicker than the contralateral side⁽²¹⁾. In pediatric patients, the unossified hypoechoic epiphysis should not be mistaken for joint fluid; comparison with the contralateral unaffected joint is helpful in avoiding this error^(18,21). In addition, cartilage is noncompressible and without Doppler signal⁽²¹⁾. In adults, if the iliofemoral ligament and joint capsule are not imaged perpendicular, this typical hyperechoic tissue may appear hypoechoic due to anisotropy and be mistaken for a joint effusion⁽⁵¹⁾. Post hip arthroplasty, joint effusions may be loculated more posteriorly and laterally⁽⁵¹⁾. Additionally, in the adult population, US can be potentially falsely negative in the diagnosis of small joint effusions, and a thorough evaluation of the posterior and lateral aspects of the joint, with a lower frequency transducer, may be helpful^(51,58).

US of osteomyelitis may demonstrate thickening and elevation of the periosteum with associated hyperemia on color/power Doppler evaluation⁽⁵⁹⁾. When present, a subperiosteal abscess typically appears as a spindle-shaped fluid collection along the osseous surface, displacing the periosteum outward (Fig. 9, Fig. 10)^{(9,14,18,50,59–61)}. There is often inflammation and hyperemia in the adjacent soft tissues (Fig. 10). In children, incompletely fused physes should not be mistaken as cortical irregularity from underlying osteomyelitis⁽²¹⁾. In chronic osteomyelitis, the periosteal reaction is typically thicker, with lack of hyperemia compared to periostitis occurring in acute osteomyelitis. A cloaca, an opening of the bone cortex that occurs in chronic osteomyelitis to allow the escape of pus, may be seen on US as a defect in the bone (Fig. 11). A sequestrum, a devitalized, sequestered bone fragment, can also be present in chronic osteomyelitis, and can be identified on US as an echogenic fragment of bone near the cloaca. Periosteal thickening may also be evident. Intraosseous and extraosseous abscesses may have fistulous communications with the skin surface (Fig. 12).