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European Journal of Radiology 83 (2014) 1529–1537

Contents lists available at ScienceDirect

European Journal of Radiology


journal homepage: www.elsevier.com/locate/ejrad

Musculoskeletal ultrasound in childhood


Kathrin Maurer ∗
Medical University Innsbruck, Department of Radiology, Anichstrasse 35, A-6020 Innsbruck, Austria

a r t i c l e i n f o a b s t r a c t

Article history: Ultrasonography is one of the first line imaging modalities for the evaluation of musculoskeletal disor-
Received 25 March 2014 ders in children. This article provides an overview of the most important pathologic entities in which
Accepted 7 April 2014 ultrasonography significantly contributes to the diagnostic workup.
© 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords:
Ultrasound
Musculoskeletal
Children

1. Introduction 2. Technical considerations

Ultrasonography (US) has emerged as an indispensable tool for As most indications refer to structures, that lie relatively super-
primarily evaluating a variety of musculoskeletal disorders in chil- ficial, high frequency probes can be used to achieve optimal special
dren. It has certain advantages over other imaging modalities – it is resolution. Linear probes are preferable due to the lack of distor-
a readily available, convenient and cost effective method. It is non- tion. In small children hockey stick transducers allow the access
invasive and there is no need for sedation even in small children. of many regions, where conventional linear transducers would
US is particularly well suited for the examination of the immature be too large. The use of a stand-off pad enables an optimal visu-
skeleton with its large portion of cartilaginous, non-ossified struc- alization of the area close to the body surface. In frightened
tures as it can readily distinguish soft tissue from cartilage and children it may contribute to calm the situation. An alternative
from bone. The capability of real time imaging allows the dynamic is the use of a water-bath, where the child puts the extremity
assessment of musculoskeletal structures during joint movement in and the transducer can be held close without touching the
and repetitive imaging in motion and at rest is possible. With US skin thus avoiding pain or anxious distress in the child. If neces-
it is easy to compare the symptomatic to the contralateral side. sary, a child can even be examined comfortably in the arms of a
The high sensitivity of US for fluid collections and joint effusions parent.
makes it an ideal tool for image guided puncture. By following In the sonographic evaluation of the musculoskeletal system
structures and using Color Doppler sonography (CDS), vessels and the amplitude of the echo is highly dependent on the angle of
nerves can be differentiated, and tissue vascularity can easily be insonation. Advances in ultrasound technologies have contributed
assessed too. to improvement of image quality. Compound imaging and beam-
There are some limitations for the use of US in musculoskele- steering decreases many image artifacts inherent in conventional
tal disease – US cannot penetrate bone and air, therefore certain sonography and are especially helpful to avoid anisotropic arti-
regions of the body such as the deeper parts of the pelvis or bone facts in tendons and ligaments. Compound imaging also results
marrow lesions cannot be assessed by US. The quality and consis- in improved tissue-plane definition due to speckle noise reduc-
tency of an US examination rely on the expertise, creativity and tion. Harmonic imaging aids in the differentiation of tissues, but
patience of the examiner – this may be seen as a disadvantage or also makes the borders between structures appear artificially
as a chance. thickened.
This article emphasizes the value of US in common developmen-
tal, infectious, inflammatory and traumatic conditions that affect 3. Developmental anomalies
the musculoskeletal system in children.
Developmental dysplasia of the hip (DDH) is the most common
indication for musculoskeletal US in children. It covers a spec-
∗ Tel.: +43 512 504 23571. trum of congenital abnormalities that ranges from immaturity and
E-mail address: kathrin.maurer@i-med.ac.at only instability to dislocation of the hip. Stabile positioning of

http://dx.doi.org/10.1016/j.ejrad.2014.04.003
0720-048X/© 2014 Elsevier Ireland Ltd. All rights reserved.
1530 K. Maurer / European Journal of Radiology 83 (2014) 1529–1537

the femoral head within the acetabulum is thought to propagate


acetabular development allowing for remodeling of acetabular dys-
plasia over time, this is used as a conservative treatment approach.
The maximum potential for effective treatment of DDH is in the
first 3 months after birth.
US is an excellent tool to assess the anatomical details of the
cartilaginous parts of the neonatal hip, and is much more informa-
tive than radiography in this age group. The accuracy and utility
of US in examining neonatal and infant hips is high. A combined
understanding of anatomy, pathology and sonography is required.
Since hip US was first described by Graf in 1980 several methods
for the assessment of morphology and stability of the neonatal
hip have been developed [1]. The method proposed by Graf is
widely used in central Europe. It assesses hip morphology, but
also takes account of hip stability (2). A standard coronal view
with the infant in the lateral position is acquired. The iliac bone
has to be straight and the acetabular labrum as well as the low-
est point of the acetabular part of the iliac bone has to be visible
(Fig. 1a). Measurement of alpha and beta angels allows classi-
fication into four main and 9 sub-types (Fig. 1b). A stress test
pushing the femur in a cranial and dorsal direction is added to
assess hip stability [2]. The combined use of a stability test in
conjunction with the assessment of the acetabular morphology
using a standard coronary view defined by Graf and measure-
ment of the alpha angle only was propagated by Rosendahl et al.
[3]. Harcke et al. developed a dynamic US examination of the
infant hip, which is widely used in the United States [4]. A four
step scanning technique is used based on transverse and coronal
planes in neutral and flexed position, at rest and during stress.
Hips are classified as normal, lax under stress, subluxed or dislo-
cated.
The femoral head coverage technique proposed by Morin and
modified by Terjesen assesses the lateralization of the femoral
head; it is used widely in France [5,6]. Femoral head coverage
by the bony acetabular rim of less than 50% is considered abnor-
mal.
Treatment is based on the reduction of a displaced hip (Fig. 1c)
and stabilization of the femoral head within the acetabular fossa.
Maintaining is achieved by several devices. With harnesses or
splints US follow up is the method of choice until shadowing
from the developing ossification center of the femoral head lim-
its its usefulness. With the ossified femoral head radiography can
be used to guide further treatment. MRI is helpful in those cases,
where hip reduction cannot be achieved by clinical manipulation
and for confirmation of femoral head position with spica casts in
situ.
A reduction in the rate of patients requiring surgery for DDH was
seen after the introduction of universal US screening in Austria and
Germany [7,8], but the value of universal US screening for DDH is
still under debate [9,10].
Recommendations for the sonographic evaluation of the neona-
tal hip were elaborated by the DDH Taskforce Group of the
European Society of Pediatric Radiology. The latest update was
issued in May 2011 [11].
The diagnosis of neonatal foot deformities is commonly based on
clinical evaluation and radiography. As tarsal bones are largely car- Fig. 1. Coronal US scan of the newborn hip (Graf’s technique): (a) Normal hip: On
tilaginous and many even lack an ossification center US is a valuable a standard view showing the deepest point of the ilium within the acetabular fossa
means for estimating the severity of the deformity. US can visualize (*), the straight upper part of the ilium (arrows) and the cetabular labrum (+). (b)
the alpha angle (˛) is >60◦ . (c) Dislocated hip: The fermoral head (F) is completely
the cartilaginous parts of the neonatal foot und evaluate alignment.
dislocated, the cartilage roof (C) is interposed.
The examination is based on a series of measurements, such as
the medial malleolus-navicular distance, the navicular alignment
with the talar head, talar length and the calcaneo-cuboid distance cartilaginous Anlage of the radius or fibula can be differentiated
[12,13]. (Fig. 2a and b).
The ability of US to visualize cartilage allows for further evalua- Anterior chest wall deformities in children are a common
tion of limb deformities, where radiographs show only one bone cause of parental concern. They are often caused by an abnor-
at the forearm or lower leg. Aplasia or hypoplasia with solely mal angulation of the cartilaginous rib which cannot be visualized
K. Maurer / European Journal of Radiology 83 (2014) 1529–1537 1531

Fig. 2. Three weeks old boy with Holt Oram syndrome. (a) Longitudinal US scan of the forearm. The cartilagineous Anlage of the radius is clearly visible, note that there is a
fusion of the radial head with the epiphysis of the humerus. (b) Radiograph of the right forearm: at the forearm there is only one bone visible, the ulna is abnormally bowed
and there is subluxation of the ulna at the elbow. Radial deviation of the hand.

on radiographs. US is a valuable tool in this setting to exclude


a tumor and confirm the benign nature of the condition (Fig. 3a
and b).
Cranial deformity in infants may result from premature cra-
niosynostosis or positional plagiocephaly. Sonography is a good
screening tool to distinguish fused from patent cranial sutures
(Fig. 4a and b), thus reducing the need for 3D-CT to patients with
inconclusive results on US and preoperative evaluation particularly
in complex cases [14,15].

4. Infection

4.1. Cellulitis and soft tissue abscess

Cellulitis is defined as an infection of skin and subcutaneous


tissue. US appearance initially resembles edema of subcutaneous
fat, showing swelling, increased echogenicity and blurring of tissue
planes. Further progression leads to hypoechoic strands between
hyperechoic fatty lobules. Increased vascularity on CDS suggests
an inflammatory process. Accumulation of pus and abscess forma-
tion can readily be detected by US and US-guided puncture can be
performed for diagnostic and therapeutic purposes.
Soft tissue abscesses are characterized by a collection of
necrotic tissue, neutrophils, inflammatory cells and bacteria sur-
rounded by a wall of highly vascular connective tissue. The US
appearance of the liquefied contents varies widely, from ane-
choic to hyperechoic (Fig. 5). To confirm the liquid nature gentle Fig. 3. (a) Excessive angulation of the cartilagineous part of a rib causing a thoracic
pump in a 5 years and 9 months old boy. (b) Normal rib.
pressure can be used to evoke fluctuation of the contents, the
1532 K. Maurer / European Journal of Radiology 83 (2014) 1529–1537

Fig. 4. (a) Patent cranial sutures in a 9 months old boy with plagiocephaly: hypoechoic gap (arrow) between hyperechoic calvarial bones. (b) Missing of the hypoechoic gap
in case of premature closure of the sagittal suture in a 1 month old girl with scaphocephaly. Bony ridge in the dorsal part of the sagittal suture.

through-transmission phenomenon must be observed, and CDS common causative organism. Diagnosis may be delayed as fever
shows absence of flow in the center and hyperemia of the abscess and malaise can be the only symptoms initially and localization of
wall [16]. pain may be difficult for the child especially with involvement of
pelvic muscles.
4.2. Necrotizing fasciitis Abscess formation can readily be shown by US in certain parts
of the body. When the full extent of the lesion is not clearly
Necrotizing fasciitis is a rapidly progressive infection of sub- demonstrated by US, MRI is the imaging modality of choice. MRI is
cutaneous tissue, fascia and surrounding soft tissue associated particularly useful to exclude bone involvement and in the evalua-
with a 30–70% mortality rate. Group A streptococci are the most tion of deeper body compartments such as the deep pelvic muscles
common offending organism in children. Previous Varicella zoster (Fig. 7a). Ultrasound is a valuable tool for image guided percuta-
virus infection seems to be a predisposing factor. Ultrasonography neous aspiration and drainage as well as for follow up examinations
shows soft tissue swelling, fascial thickening and accumulation of (Fig. 7b).
fluid along fascia (Fig. 6a) and can demonstrate gas bubbles in the
soft tissues (Fig. 6b). MRI is essential to document the extent of 4.4. Osteomyelitis
soft tissue involvement. Prompt extensive surgical debridement
and antibiotic therapy may stop the fatal course of the disease Osteomyelitis is an infection of bone marrow and bone usu-
[17]. ally caused by bacteria. Infection occurs through three possible
routes: hematogenous, which is by far the most common way in
4.3. Pyomyositis children, by contiguity, and by direct implantation. In children
more than 80% of cases of osteomyelitis occur due to hematoge-
Suppurative bacterial infection in striated muscle is rare. Chil- nous seeding after a transient episode of bacteremia. Due to
dren are affected in one third of cases. There is a predilection for the architecture of the supplying vessels the primary site of the
muscles in the thigh and pelvis. Staphylococcus aureus is the most infectious process is the metaphyseal region of the long bones. Fur-
ther spread varies according to age and depends on the vascular
anatomy of the metaphyseal–epiphyseal region [18]. Typical signs
and symptoms of acute osteomyelitis include fever, local pain and
tenderness. However initial signs may be vague and misleading
especially in infants, who may only present with pseudoparaly-
sis.
Radiographs should always be the first study obtained in
patients with suspected osteomyelitis. Deep soft tissue swelling
is visible as early as 2 days after onset of symptoms, but it is
often difficult to detect. Bone changes are not detectable until
after 7–10 days. Ultrasound may demonstrate features of acute
osteomyelitis within 48 h [19]. The earliest sign is juxtacortical soft
tissue swelling followed by periosteal elevation with a thin layer of
fluid. As periosteal attachment is loose in young children, subpe-
riosteal abscess formation rapidly occurs and is seen as hypoechoic
lenticular-shaped fluid collection along the cortex (Fig. 8a). In the
appropriate clinical setting this finding confirms acute osteomyeli-
Fig. 5. 7 years and 9 months old girl, 5 months after a penetrating injury by the
tis. After US-guided puncture to obtain material for cultivation of
brake handle in a bicycle accident. Turbid fluid collection within the subcutaneous
tissue of the thigh, centrally located there is an echogenic line with shadowing – the causative organism antibiotic therapy can be started imme-
abcess containing a little piece of cloth. diately. Cortical erosions can be seen later in the course of the
K. Maurer / European Journal of Radiology 83 (2014) 1529–1537 1533

Fig. 6. (a) Necrotizing fasciitis in a 2 years and 7 months old boy, a few weeks after a varicella zoster virus infection. Thickening of the tibialis anterior muscle with hyperechoic
changes and fluid accumulation within the deep fascia as compared to the contralateral side. (b) Necrotizing fasciitis of the abdominal wall in a 6 years and 10 months old
boy following appendectomy. Thickening of the subcutaneous tissue as well as the abdominal wall muscle. Hypoechoic strands and gas-bubbles between the muscle fibers.

disease and US is also useful in detecting fistula formation in chronic 5. Inflammatory disease
osteomyelitis [20] (Fig. 8b and c).
In children under the age of 2 years, blood vessels cross the 5.1. Juvenile idiopathic arthritis (JIA)
physis thus propagating spread of infection into the epiphysis and
into the joint space. This leads to septic osteoarthritis. US is an JIA is a heterogeneous group of diseases in children under
excellent tool to demonstrate joint effusion and therefore it is the age of 16 years, characterized by synovial inflammation of
extremely useful in neonates and infants suspected to have sep- unknown cause that persists for more than 6 weeks. JIA is the most
tic osteoarthritis allowing for immediate management by guided common chronic rheumatic disorder in children and is a leading
aspiration. cause of acquired disability in the pediatric age. Early therapeu-
Ultrasound has been found to be a fast and useful first line diag- tic intervention and the use of new disease-modifying therapeutic
nostic tool for early detection of acute osteomyelitis in children, agents have improved the outcome and have led to greater empha-
especially in newborns and infants [21]. As 50% of affected children sis on the accurate detection of disease activity. The presence of
are under the age of 3 years, the lack of need for sedation is a great extensive amounts of epiphyseal cartilage in children limits the
advantage. usefulness of conventional radiography in the early stages of the
But it has to be strongly emphasized that US cannot exclude disease.
osteomyelitis. In patients with suspected osteomyelitis and nega- Contrast enhanced MRI and US both are well suited for this
tive or inconclusive results on US urgent MRI is mandatory [22]. application. For pediatric patients US offers specific advantages
over MRI as it is non-invasive, there is no need for sedation, it allows
4.5. Septic arthritis for assessment of multiple joints in one session and real-time
dynamic imaging of tendons and joints helps to detect structural
Acute septic arthritis is a medical emergency as early diagnosis abnormalities during joint movement.
and treatment is mandatory to prevent joint destruction, growth US is more sensitive than clinical evaluation and radiography
disturbances and early degenerative disease. In children over the for the detection of synovial proliferation and effusion and is par-
age of 2 years it is mostly caused by hematogeneous seeding, less ticularly useful in the evaluation of small peripheral joints. In
frequently by contiguous spread from adjacent osteomyelitis. experienced hands US allows reliable assessment of further signs
The hip joint is most common involved; knee, shoulder and of disease like cartilage blurring, thinning and erosions as well as
elbow are other common preferred sites. The presenting symptoms bone erosions, enthesitis and tenosynovitis. The use of CDS provides
are fever, pain, inability of weight bearing, elevated erythrocyte information about synovial vascularity and hyperemia. Several
sedimentation rate and C-reactive protein. studies have demonstrated the ability of US to detect subclinical
Ultrasound is highly sensitive to detect joint effusion, but disease and its usefulness in evaluating response to intraarticular
neither seize and echogenicity of the effusion nor adjacent therapy [25,26].
hyperemia on CDS imaging allow distinguishing infectious from US evaluation in JIA has certain limits. In large joints visual-
non-infectious arthritis. Definite diagnosis of septic arthritis is ization of the entire articular surface may be hindered by bone
based on US-guided aspiration of joint fluid [23,24]. shadowing, there is insufficient resolution of anatomical details of
1534 K. Maurer / European Journal of Radiology 83 (2014) 1529–1537

Fig. 7. Pymoyositis in an 8 years old boy. (a) Axial MRI (contrast enhanced t1
weighted sequence) and (b) transverse US scan: Abscess within the external obtu-
rator muscle.
Fig. 8. (a) 6 years and 11 months old boy with increasing pain at the left ankle 24 h
after a minor trauma. Logitudinal scan of the distal fibula. Spindle shaped elevation
deeper structures, and US has high false negative rates in subtalar of the periosteum by a turbid fluid-collection (arrows). Osteomyelitis of the distal
disease. The complexity of the temporomandibular and the sacroil- fibula with subperiosteal abscess. (b) 13 months old girl refusing to bear weight
iac joints makes contrast-enhanced MRI the preferred method for on her left leg. Longitudinal scan along the medial aspect of the proximal tibia.
evaluation of these structures. Contrast-enhanced MRI is the most Lenticular shaped fluid accumulation attached to the metaphyseal cortex(arrows),
small abscess in the metaphyseal region (*) and cortical defect close to the physis
sensitive technique for detection of synovitis and the only modality
(arrowheads). Acute hematogeneous osteomyelitis of the proxmimal tibia. (c) 13
to demonstrate bone marrow edema [27]. The major draw-back for years old girl with pain at her ankle for the last 2 months. Axial scan at the lateral
its use in young children is the need for sedation. side of the ankle. Cloaca (arrow) at the metaphyseal region of the distal fibula with
a small bony sequestrum (*) within a soft tissue abscess(arrow heads) in chronic
bacterial osteomyelitis.
5.2. Transient synovitis of the hip

Transient synovitis is the most common cause of hip pain in


children aged 3–8 years. The clinical features are sudden onset A preceding viral infection is reported by many patients. It is a
of unilateral hip pain without a history of trauma, limping and benign, self-limiting disease. Definitive diagnosis can only be made
restriction of motion, sometimes accompanied by low grade fever. by exclusion of other disorders.
K. Maurer / European Journal of Radiology 83 (2014) 1529–1537 1535

Fig. 9. (a) Coronal MRT: Positioning of the US probe to demonstrate hip joint effusion in the anterior recess. (b) 6 years old boy with transient synovitis of the hip. US shows
fluid accumulation within the anterior recess of the hip joint.

US demonstrates joint effusion in the anterior recess of the hip performed immediately in cases where septic arthritis cannot be
joint. Normally the anterior and posterior parts of the joint capsule excluded.
are attached closely to each other. A linear echo located centrally
marks the interface between the two layers. With joint effusion the
anterior joint capsule assumes a convex shape and underlying fluid 6. Trauma
within the anterior recess can be visualized (Fig. 9a and b), which
may be anechoic or contain particles. This finding is nonspecific In animal models ultrasonography has not only comparable sen-
[23]. Ultrasound evaluation of the femoral epiphysis is mandatory sitivity to that of X-ray for the identification of limb fractures but is
to look for irregularities of the cartilage and ossification center in also equally effective for the diagnosis of fracture type and disloca-
case of Perthes disease or a physeal step in slipped upper femoral tion [28]. Recent studies have shown that distal forearm fractures
epiphysis (Fig. 10a–d). If one of these entities is suspected on US, in children can be safely and reliably diagnosed using only US thus
further evaluation by radiography and MRI will establish the extent avoiding radiation burden to the immature skeleton [29].
of the disease in detail. The most important differential diagnosis Although promising, this approach has several draw backs till
is septic arthritis due to the devastating consequences to the hip now – it is time consuming and positioning of the limb to eval-
joint in case of delayed diagnosis. Aspiration of joint fluid has to be uate the whole circumference of a bone might be difficult and

Fig. 10. (a) 4 years old boy. US of the left hip joint. Joint effusion (*), widening of the metaphysis with irregular contour (arrows), small irregular ossification center in the
femoral head (arrowhead) – Perthes disease. (b) Corresponding radiograph. (c) 12 years old boy. Hip joint effusion (*) and step at the physis (arrow). Slipped proximal femoral
epiphysis. (d) Corresponding radiograph.
1536 K. Maurer / European Journal of Radiology 83 (2014) 1529–1537

Fractures of phalanges, metacarpals and metatarsals often show


only subtle changes on radiographs, whereas on US an interruption
of the cortical continuity or a buckle can easily be seen (Fig. 11). In
a toddler, who refuses to bear weight it may be challenging for the
clinician to localize the region of interest. US allows screening for
a toddlers fracture on a whole extremity and even on both sides.
Detection of classical metaphyseal and rip fractures in child
abuse can be extremely difficult. The use of US may be helpful to
visualize the small displaced fragment of a corner fracture as well
as hematomas in the soft tissue around a rib fracture and fractures
within the cartilagineous part of the rib [31] (Fig. 12a–c).
A further indication is the search for non-radiopaque foreign
bodies (Fig. 5, Fig. 13 a). Here US is not only an elegant tool useful for
detection and US-guided removal [32], it furthermore often allows
to differentiate wood splinters form glass and other foreign bodies
Fig. 11. 2 years and 8 months old boy refusing to bear weight on his left leg. Longi-
by their US appearance.
tudinal scan of the lateral aspect of the left foot. Disruption of the cortical line and
small bony fragment close to the physis of the fifth metatarsal. Fracture of the fifth
metatarsal.
7. Tumor

In children with a tumor of the musculoskeletal system US often


painful. 24 hour availability of skilled examiners in a busy emer- is the first imaging modality. It can help to rule out abscess or
gency department might be a limitation too. hematoma as a cause of the regional swelling. Due to the possibil-
Therefore plain radiography still is the standard primary imag- ity of real time imaging it is especially useful to differentiate a solid
ing method in children with a history of trauma. However, there tumor from a venolymphatic vascular malformation. If a tumor is
are some instances where US can play an important role in the detected by US, MRI is the imaging method of choice to establish
diagnostic work-up. Due to the immaturity of bone with largely the extent of the lesion, as well as involvement of bone, vascular
cartilaginous epiphysis fractures at the region of the physis may be structures and nerves. US can be used for image guided puncture
undetectable by radiographs. US has proven an effective imaging and follow up.
modality in these settings especially in injuries around the elbow A special entity, where the diagnosis is readily established with
[30]. It can even be used for guiding repositioning maneuvers in US and further imaging evaluation or biopsy is rarely required
dislocated epiphysiolysis. is fibromatosis colli. It is a self-limiting disorder of neonates and

Fig. 12. (a) Left: normal proximal humerus in a young child. Right: 2 months old boy. Longitudinal scan on the left humerus. Small dislocated fragment at the metaphysis
with subperiosteal hematoma. Classic metaphyseal fracture in child abuse. (b) 7 months old boy. Longitudinal paravertebral scan on the left side of the thorax. Intercostal
soft tissue hematomas due to rib fractures in child abuse. (c) Midthoracic axial scan. 3 months old girl. Fracture within the cartilagineous part of the rib (arrow). Surrounding
hematoma (*). Child abuse.
K. Maurer / European Journal of Radiology 83 (2014) 1529–1537 1537

Conflicts of interest

None.

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