Sonography of bone and bone-related diseases of the extremities

Pictorial Essay

Sonography of Bone and Bone-RelatedDiseases of the Extremities

Kil-Ho Cho, MD,1 Young-Hwan Lee, MD,2 Sung-Moon Lee, MD,3 Muhammad Usman Shahid, MD,1

Kyung Jin Suh, MD,4 Joon Hyuk Choi, MD5

1Department of Diagnostic Radiology, College of Medicine, Yeungnam University, 317-1, Daemyung-Dong,Nam-Ku, Daegu, 705-717, Korea2Department of Diagnostic Radiology, College of Medicine, Daegu Catholic University, Daegu, Korea3Department of Diagnostic Radiology, College of Medicine, Keimyung University, Daegu, Korea4 Soo & Joo MR Clinic, Daegu, Korea5Department of Anatomical Pathology, College of Medicine, Yeungnam University, Daegu, Korea

Received 23 May 2003; accepted 29 July 2004

Radiography is the baseline modality in theevaluation of bone diseases, commonly fol-

lowed by radioisotope scanning, CT, or MRI.Accelerated development of MRI and the initiallylow-resolution imaging capability of sonographymay have resulted in the underutilization of sonog-raphy for bone diseases.1 However, MRI itselfdoes not have the fine resolution of plain radiog-raphy or CT to define cortical abnormalities ofbone. The use of sonography for evaluation of theskeletal system has been hampered by the mis-conception that the lack of propagation of ultra-sound through the bone and small field-of-viewimages are insurmountable obstacles to evaluatethe skeletal system, resulting in reduced use and alack of literature on musculoskeletal sonography(MSUS). Nevertheless, the high reflectivity ofsound at the bone–soft tissue interface and tomo-graphic nature of sonographymake it ideal for eval-uation of bone contours.2 High-resolution sonog-raphy can reveal subtle changes of the bone surfacenot detected on plain radiographs, such as tinyperiosteal reactions and subperiosteal fluid collec-tions, and can differentiate soft tissue lesions frombone lesions (Figure 1).

Using the extended-field-of-view function ofMSUS, a large lesion can now be displayed on a

single sonogram,3–5 and the relationship of thelesion to adjacent anatomic structures can bedepicted with osseous and articular landmarks, asis possible on radiographs. Recent technologic im-provements in ultrasound scanning and increasedawareness of the advantages of sonography overother imaging modalities have led to a resurgencein interest.6 Correlative imaging, however, remainsmandatory to avoid errors in interpretation.

TECHNICAL CONSIDERATIONS

The operator must have sufficient knowledge ofregional bone and soft tissue anatomy, includingnormal anatomic variants, and be familiar withspecific sonography-related artifacts. In additionto MSUS findings, results from other imagingstudies and laboratory tests should be consideredin making the diagnosis. Crucial information canbe obtained by history taking from the patients ortheir guardians, and by continued sonographic andphysical examination.

In general, high-frequency (10–15-MHz) linear-array transducers are the most appropriate choicesfor MSUS allowing detailed depiction of pertinentanatomic structures. Using a stand off pad or thickapplicationofacoustic couplinggelontheskin ishelp-ful for evaluating very superficial bones. Low-fre-quency (3–5-MHz) curved-array transducers havean advantage when the lesion is deep-seated in largeormuscular patients, but the resolution is inferior tothat of high-frequency transducers, and the operatorshould identifytheartifactualhypoechoicappearanceof the bone surface on each side of the sector image.

Correspondence to: K.-H. Cho

Grant Sponsor: Yeungnam University Academic Fund

J Clin Ultrasound 32:511–521, 2004; Published online in Wiley

InterScience (www.interscience.wiley.com).DOI:10.1002/jcu.20066

� 2004 Wiley Periodicals, Inc.

VOL. 32, NO. 9, NOVEMBER/DECEMBER 2004 511

Scanning methods for bone are similar to theaccepted protocol for MSUS.5–9 Examiners surveythe symptomatic area first, and then compare it withthe contralateral and usually asymptomatic side,helpingdifferentiateabnormal fromnormal findings,avoiding diagnosis of normal variants as pathologicand occasionally revealing unsuspected abnormal-ities crucial for diagnosis (Figure 2). Color and powerDoppler sonography show the vascularity associatedwith pathologic conditions and the relationshipbetween lesions and adjacent neurovascular bundles.

NORMAL BONE

The normal periosteum, a dense, fibrous connectivetissue, is adherent to the surfaceof thebone, attachedby Sharpey’s fiber, and currently cannot be recog-nized as a separate structure sonographically. Thus,the term ‘‘bone surface’’ is applied to describe theregular hyperechoic line at the interface betweenthebone and soft tissues, producedby a strong reflec-tionof sounddue to themarkeddifference in acousticimpedance of the soft tissues and bone. The acousticshadow deep to the hyperechoic bone surface repre-sents the normal appearance of the bone. Reverbera-

tion artifacts projecting in the shadow beyond thebone can be seen onboth longitudinal and transversescans.1,2,7–9

There are some pitfalls in the interpretation of thesonographic appearance of the normal bone surface(Table 1). The growth plate in the immature skele-ton, the canals for perforating vessels or grooves fornutrient arteries, and accessory ossicles may appearas interruptions along the continuity of the bone sur-face, mimicking fractures (Figure 3). The fascialthickening of the normal myelotendinous attach-ment sites onto the bonemay also result in irregular-ity of the bone surface.2 Right-left side comparison ofpaired structures and supplementary dynamic eval-uation are very helpful MSUS maneuvers wheneverthere is doubt regarding the normal appearance.

PATHOLOGIC CONDITIONS OF THE BONE

Diseasedbonemaypresent, sooner or later, as a bonealteration, a consequential soft tissue change, orboth. MSUS can diagnose lesions directly by depict-ing bone surface changes,whether caused by bone orperiosseous soft tissue disease, and indirectly bydemonstrating soft tissue changes in the case of

FIGURE 1. Myositis ossificans in a 37-year-old woman after trauma

about 1 month previously. (A) Longitudinal sonogram of the anterior

aspect of the proximal thigh shows the irregular hyperechoic line

(arrows), with posterior acoustic shadowing in the muscle juxta-

cortically. On dynamic examination, the calcific shadow could be dif-

ferentiated from the cortical surface (arrowheads) of the femur, which

is visible deep to the calcific shadow. (B) Lateral radiograph of the right

thigh obtained 1 day before the sonographic examination shows no

abnormality. (C) Lateral radiograph obtained 10 days later shows the

multipennate calcific density (arrows) in the soft tissues.

CHO ET AL

512 JOURNAL OF CLINICAL ULTRASOUND

bone diseases that have an effect on the adjacent softtissues.6–10

Bone surface changes can be categorized sonogra-phically as follows: thinning or thickening of thehyperechoic line; interruption of the bone continu-ity, including a step-off deformity, expansion, orexcavation; periosteal reactions; and cortical dis-

ruption, with visualization of intraosseous compo-nents. It is important to interpret sonographicallydocumented abnormalities of the bone surface inthe context of findings on plain radiographs. Cur-rently, sonography is unable to depict intraosseouschanges unless the cortex is sufficiently thinned ordestroyed.

FIGURE 2. A 64-year-old womanwith pain in the left hip for 2 weeks. Anteroposterior radiographs of the right (A) and left (B) hips show the transverse

sclerosis (arrow, B) at the left femoral neck. Anterior longitudinal sonogramsof the right (C) and left (D) hips show the abrupt interruption (white arrow,

D) of the cortical continuity at the upper portion of the left femoral neck. The contralateral image (C) shows the normal bone surface, with continuity.

(E) Fat-suppressed T2-weighted coronal MR image shows the hypointense transverse fracture line (arrow) and bone marrow edema.

SONOGRAPHY OF EXTREMITY BONES


Traumatic Lesions

MSUS is not the first-line imaging modality whenbone trauma is suspected. However, it is worthwhilefor detecting occult fractures that are not shownon radiographs,11–18 as it may avoid more costlyMRI.6,11 MSUS can detect rib fractures in 6 timesas many patients as radiography and will detect 10times more fractures overall.13 It can uncover frac-tures coincidentally, while being used to examinesoft tissue,14 and can be useful in further assessingfractures after initial radiography19 (Figure 4).Sonographically guided monitoring during closedreduction of fractures has reportedly yielded resultscomparable to those obtained using a conventionalradiographic technique.20,21

A fracture may be demonstrated sonograph-ically as an abrupt discontinuity of the bone sur-face, with or without a step-off deformity, anangular or buckle deformity of the cortex at thefracture site, hypoechoic subperiosteal blood col-

lection, and overlying soft tissue edema, with orwithout a soft tissue injury (Figure 2 and 3).

When pain, with or without swelling, is present innewborns and children after suspected bone traumaaround a joint, findings on physical examination areusually nonspecific and radiographs are commonlynondiagnostic because the nonossified epiphyses arenot visualized.6,17,18,22–24 In this situation, MSUSmay become a reliable substitute for the plain radio-graphs in selected cases,17,22 not only by visualizingthe unossified cartilaginous bone, but also by corre-lating the symptoms and physical signs with sono-graphic findings (Figure 5). Tenderness or painelicited from a suspected lesion as the transducerpasses over it is known as positive ‘‘sonographicpalpation.’’

Rotator cuff tears, arthritis, and rarely calcifictendinitis may cause periarticular bone erosion,which may reflect repetitive pressure, stress, ortraction force on the insertion site of tendons orlocal hyperemia due to inflammation.25–27 Thesebone changes sometimes may have an MSUSappearance similar to that of fractures. Becausea stress fracture may be chronic, a focally thickhyperechoic callus commonly overlies the corticalinterruption at the fracture site, a finding thatmay contribute to diagnosis in conjunction withthe findings on radiographs.

MSUS can be used to assess fracture healing in itsearly phase because radiographic findings are insuf-ficient. The initial hypoechoic appearance of thefracture is replaced by the image of a hyperechoiccallus bridging the fracture gap; this hyperechoicregion progressively increases in volume as the cal-lus matures and casts a greater posterior shadow.Serial correlation of histologic findings with

FIGURE 3. Stress fracture in a 22-year-old man suffering from heel pain for 20 days. (A) T2-weighted sagittal MR image of the ankle shows the

vertical fracture line (arrow) in the calcaneus. Longitudinal sonograms of the lateral aspect of the calcaneus show various features: (B) the step-off

deformity (arrow) of the bone surface; (C) anteroinferior to the step-off deformity, another cortical disruption (arrowhead) is seen, which

corresponds the canal (arrow) for a perforating vessel on color Doppler sonography (D).

TABLE 1

Common Pitfalls in Bone Sonography

Pitfall Cause

Technical

artifact

Incorrect position of transducer

Heterogeneity by geometric relationship

Mechanical

artifact

Anisotropy

Acoustic shadowing from fibrous septa or calcification

Anatomic

factors

Perforating canal or nutrient groove

Fascial thickening at the attachment to the bone

Discontinuity at the growth plate

Sesamoid

Patient

factors

Obesity or large physique

Deep-seated tumor

Limited motion and improper posture

CHO ET AL


sonographic appearance in a healing fracture inhumanshasnotbeenpossiblebecause itwouldbeun-ethical to biopsy the fracture site in patients who donothave any complication.28 In canines, thepresenceof a hyperechoic appearance at a fracture site report-edly represents neo-osteogenesis histologically.29

On serialMSUS examinations, the normal healingprocess of a fracture goes through 5 stages: (1) initialsonolucency at the fracture gap; (2) progressiveincrease of dot-like hyperechoic foci at the fracturesite; (3) formationofapoorlydefinedechogenicbridgeacross the fracture site (probable primary callus); (4)prominence of a thin hyperechoic line at the super-ficialaspectof theprimarycallusalongthe longaxisofthe bone; and (5) development of a thick hyperechoicregular line continuouswith theadjacentnormal cor-tex (probable secondary callus). ColorDoppler sonog-raphy may demonstrate progressive formation ofnew vessels at the site of the developing callus untilabout 100 days after surgery, from which time flow

signals decrease and bone remodeling continues.2,30

The resistance index tends to decrease in the earlyweeksaftersurgeryandthenincreaseslightlyastibialfractures heal. In contrast, a lack of development offlowsignals andpersistence of ahighresistance indexis observedwhen fracture healing is delayed.

Osteochondral injury can be evaluated sonogra-phically by assessing the subchondral bone andoverlying cartilage simultaneously.31 However, theintra-articular deep portion is difficult to examine.

MSUS in Patients with Orthopedic MetallicImplants/Hardware

MSUS has potential value stemming from its abilitytodemonstratenewbone formationandmeasure thedistraction gap in patients who undergo Ilizarovlimb-lengthening procedures. MSUS can demon-

FIGURE 4. A 40-year-old man complaining of ankle pain for 6 months

after treatment of multiple fractures of the tibia and foot. Radio-

graphs of the ankle obtained over the previous 6 months (not shown)

were unremarkable. (A) Coronal T2-weighted MR image shows a

small amount of low-signal material (arrow) between the lateral

malleolus (L) and lateral aspect of the talus (T). (B) Sonogram obtained

along the intact anterior talofibular ligament (small arrows) shows

the curved echogenic line (thick arrow) with posterior shadowing.

This line was surgically confirmed to correspond to a bone fragment.

After surgical removal of the fragment, the ankle pain was relieved.

FIGURE 5. A 2-year-old girl refusing to use her right arm. (A) Oblique

radiograph of the right elbow shows the equivocal curvilinear dense

area (arrow) in the lateral condyle of the distal humerus. (B) Lateral

longitudinal sonogram of the right elbow shows the focal cortical

disruption (small arrow) at the distal end of the metaphysis, periosteal

elevation (arrowhead), and separation (large arrow) of the meta-

epiphyseal junction. (C) Contralateral asymptomatic left elbow shows

intact bone surface and the junction between the metaphysis (M) and

epiphysis (E) of the distal humerus.



strate neo-osteogenesis several weeks before itbecomes evident on plain radiographs.32 Accuratemeasurement of neo-osteogenesis at the distractionsite is important to determine the appropriateadjustment rate of bone lengthening: Overly fastdistraction inhibits bone formation, and overly slowdistraction leads to premature consolidation. Sono-grams also can depict cyst formation at the distrac-tion site, enabling timely aspiration of persistentcysts (Figure 6).32–35However,MSUS isnot as usefulas radiography in detecting the angular deformity.34

Initially, an osteotomy site appears as a sonolucentarea.Hyperechoic foci representingneo-osteogenesisare visible as early as 4–14 days after corticotomy.New bone tissue, visualized as thin, echogenicstrands at the distraction gap, increases and showslongitudinal alignment in 14–28 days after surgery.

In3–6weeks, thedistractiongapbecomesmoreecho-genic, being filled with hyperechoic foci secondary tomineralization, but is still penetrable by ultrasound.At this time, plain radiographs may show an equivo-cal periosteal reaction.

Sonography can be a noninvasive predictor of‘‘boneregenerate strength’’ in theearly consolidationphase after cessation of lengthening, which mayreduce the need for repeat radiography.36 Fromboth ends of the corticotomy margins, there is pro-gressive bridging of the distraction gap. As the gap isfilled, it changes froman almost rectangular shape toa ‘‘V’’ shape.Theultrasound’s ability topenetrate thedistraction site is progressively limited by callus for-mation, and the signal is almost completely reflectedusually with in 5–9 weeks (mean, 7 weeks) aftersurgery,making sonographicmonitoring impossible.

FIGURE 6. A 22-year-old man undergoing Ilizarov bone lengthening of the tibia. (A) Anterior longitudinal sonogram at the distraction gap of the

tibial shaft shows a hypoechoic cyst (*) within the distraction gap of the tibia (T). Percutaneous needle aspiration was done. (B) Image obtained

15 days later shows the decreased size of the cyst. (C) Image obtained 10 days after image B shows no residual cyst. A hyperechoic line representing

the bone surface (arrows) is visualized along the surface of the distraction site. (D) Lateral radiograph of the lower leg contributes no additional

information about conditions at the corticotomy gap.

CHO ET AL


At this time, however, signs of mineralization at thedistraction gap become visible on radiographs.

Plain radiography is unsuitable for evaluation ofsoft tissue complications in patients with orthopedicmetallic implants because it cannot visualize thechanges in the soft tissues. CT and MRI are alsousually inadequate because of image degradationdue to artifacts from the metallic devices.37 MSUS,conversely, may visualize soft tissue complications,such as impingement by implants, cystic degenera-tion, hematoma formation, or infection after sur-gery, and often also provides information aboutosseous complications (Figure 7).37–39

Infection

MSUScan be used to diagnose acute osteomyelitis asearlyas24hours after theonset of fever, radiographyfindings become positive usually only after 7–10days. MSUS findings include deep soft tissue swel-ling adjacent to the bone, with a hypoechoic layerrepresenting pus collection beneath the periosteum,increasing the periosteal thickness beyond the nor-mal 2 mm. Serial scans show a progressive increaseof focal bone resorption. MSUS findings in acuteosteomyelitis represent a continuum of the evolvingpathologic processes, rather than discrete stages.Initially, the periosteummay be involved along only1 side of the bone. It is important, therefore, that theMSUS examination cover the entire bone circum-ference. The site of ‘‘point tenderness’’ often cor-responds to the site of the periosteal reaction.40

The subperiosteal anechoic or hypoechoic pus collec-tion is oftendifficult todifferentiate fromasubperios-teal fluid or blood collection, osteoid osteoma, and(rarely) tumor metastasis.40–43 If soft tissues areinterposed between the anechoic pus collectionand the bone surface, osteomyelitis is less likely.

Extensive abscess formation and multiple min-ute calcifications may be suggestive of tuberculousosteomyelitis,43 but not always. In chronic osteo-myelitis, MSUS can readily demonstrate inhomo-geneous cortical irregularity, abscess formation,and formation of a sinus fistula tract in the softtissues.2,7 However, it is not easy to determinewhether the bone infection is active or not, evenon MRI. Clinical and laboratory data, in conjunc-tion with radiographs or CT or MR images, maybe sufficient for diagnosis. If not, sonographicallyguided percutaneous needle aspiration or surgicalbiopsy is mandatory for definitive diagnosis.

Bone Neoplasms and Percutaneous NeedleBiopsy

The use of MSUS in diagnosing bone neoplasms isvery limited.However,MSUScanprovide important

information when the tumor metamorphoses at thebone surface, extends into soft tissue, or destroys orthins the cortex sufficiently for transmissionof sound

FIGURE 7. A 67-year-old woman with progressive soft tissue swelling

at the lateral aspect of the arm. Comminuted fracture around the

elbow had been surgically repaired several years previously.

(A) Anteroposterior radiograph of the elbow shows suspected soft

tissue swelling along the lateral aspect (arrow) in the soft tissues

and multiple Kirschner wires applied to the bone. (B and C) Split-

screen sonograms obtained by longitudinal scanning of the lateral

aspect of the arm show a comet-tail artifact (C, white arrow) caused by

the tip of the Kirschner wire (arrowhead), corresponding to the tip of

the Kirschner wire in A (arrowhead). Anechoic and hypoechoic

hemorrhage (black arrows) extends from the tip of the Kirschner

wire to the forearm along the forearm extensor muscles.



waves.1,7–9,10,44 Aneurysmal bone cysts and giant celltumors of the bonemay create a bulge on the surfaceof the bone, with cortical thinning sufficient to allowbeam penetration; sonography would reveal a cyst-like appearance, with intraosseous fluid-fluid levelsand septa.1,44–46 Sonography is also valuable in eval-uating the cartilaginous cap of osteochondroma,47

which appears as a hypoechoic layer superficial tothe highly reflective bone surface, with outpouch-ings. When the cartilaginous cap is thinner than1 cm, the tumor is usually benign, whereas a capthicker than 2 cm generally indicates malignancy.An irregularly contoured cartilaginous cap thickerthan 1 cm is regarded as a sign of borderlinemalignancy. With MSUS, it is easy to differentiate areal osseous overgrowth from enlargement due tohemorrhage or tumors of the soft tissues or adventi-tial bursae between the bone and soft tissue.1

Osteoid osteoma of the long bone shaft is similarto osteomyelitis sonographically and clinically.MSUS may reveal a mild convex deformity of thebone surface, with spur-like irregularity and fluidcollection between the bone surface and soft tis-sue.48–50 In the case of intra-articular osteoidosteoma, the nidus of the tumor is often overlookedat radiography because of minimal or absent reac-tive sclerosis and the nonspecificity of the clinicalfeatures, resulting in a delay of diagnosis formonths

or even years. Color and power Doppler imagingmay help define the nidus of the tumor.49,50 Find-ings from sonography must be combined with thosefrom radiography and with the patient history fordiagnosis. In subperiosteal osteoid osteoma, thenidus appears as a small round area or cortical dis-continuity; however, the findings may be similar tothose in arthritic bone erosion, osteochondritis dis-secans, and intra-articular fracture. MSUS may beable to aid in diagnosis by visualizing subtle perios-teal reactions of early stage bone tumors, which arenot visualizable on radiographs (Figure 8).

Otherwise, MSUS is less useful than radiographyand MRI in diagnosing, differentiating benign frommalignant, and staging bone tumors.45–52 Sonog-raphy is of great value in not only guiding percu-taneous needle biopsy of bone tumors with anextraosseous component, but also localizing specificsites for surgical biopsy,1,7,12,45,53–59 providing a safeand reliable alternative to fluoroscopy and CT.55,58

Themain advantages of sonographically guided nee-dle biopsy of bone tumors are as follows: (1) contin-uous real-time tracing of the tip of the movingneedle allows the practitioner to avoid major neuro-vascular structures within the portal; (2) color andpower Doppler functions are helpful for identifyingregions of viable tissue; and (3) sonography allowssimultaneous needle placement, imaging, and tissue

FIGURE 8. A 12-year-old girl with osteosarcoma of the distal femur. (A) Anteroposterior radiograph of the distal femur shows sclerosis (*) in the

medial aspect of the distal metaphysis, but no periosteal abnormality is evident. Longitudinal sonograms along the medial (B) and lateral (C)

aspects of the distal femur show the fine sawtooth appearance of periosteal reaction (arrows) and the smooth adjacent normal bone surface

(arrowheads). The cortical space (curved arrow, C) is the growth plate of the distal femur.

CHO ET AL


sampling, reducing time, cost, and patient manipu-lation.55 Percutaneous needle biopsy may representa viable alternative to surgical biopsy for the pri-mary histologic diagnosis of sarcoma and maybe sufficient for histologic subtyping in certaininstances.59 MSUS can be used to monitor fortumor recurrences by periodic re-examination ofresection sites, especially in patients with metallicimplants.37–39,53

Miscellaneous and Soft Tissue LesionsAffecting the Bone

Abnormalities of the bone and soft tissues, espe-cially in the articular and periarticular regions,may cause changes in the bone surface; these areseen in arthritides, intra-articular loose bodies,rotator cuff tears, habitual dislocation of theshoulder (eg, Hill-Sachs’ lesion of the shoulder),Osgood-Schlatter disease, and calcific tendini-tis.1,6–10,25–27,60 Surface contours of the bone mayin rare cases also be changed by bursitis, perioss-eous ganglia, myositis ossificans, giant cell tumorsof the tendon sheath, and various juxtacortical softtissue tumors. Therefore, bone abnormalities foundduring assessment of the soft tissues or joints, andvice versa, should be incorporated in differentialdiagnosis, as should information from radiographyand other imaging studies. So, for instance, in thosecases where myositis ossificans looks like a perios-teal reaction of the underlying bone (Figure 1),differentiation between the conditions is usuallypossible on dynamic MSUS examination.

In conclusion, high-frequency sonography, withits ‘‘low-power microscope–like’’ functionality, candemonstrate subtle cortical and juxtacortical ab-normalities related to bone disease. Sonographycan be employed as the principal imaging modal-ity in certain instances, although the potential ofMSUS with respect to bone tumors and purelyintraosseous lesions is still being investigated.The application of MSUS to bone diseases is likelyto be expanded as acceptance of and familiaritywith the technique grows.

Thus, MSUS might be routinely used to evaluatepatients with orthopedic hardware, trauma to thegrowing bone, surface cortical and juxtacorticalanatomy, and nonspecific pain in the case of normalor equivocal findings on radiography. MSUS mightalso be used to obtain information that supple-ments or complements that from other imagingstudies; to define the relationships between lesions,nerves, and vessels; and to guide percutaneous nee-dle aspiration procedures. As data accumulate, theapplication of sonography to bone diseases may

change themethodology used in the diagnostic imag-ing of skeletal pathologies.

ACKNOWLEDGMENT

We thank Dr. J. Antonio Bouffard for reviewingthis manuscript.

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Sonography of bone and bone-related diseases of the extremities

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