Abstract
Ultrasonography (US) is usually the first imaging examination performed to evaluate palpable or visible superficial soft tissue lesions that are common in children. Although clinical assessments, such as age at presentation, clinical course, and overlying skin discoloration, are important for the differentiation of pediatric soft tissue lesions, US allows a specific diagnosis of some typical benign lesions and helps in guiding further investigation since it provides detailed information about the lesion location, characterization including solid versus cystic, vascularity, and compressibility. Therefore, sufficient knowledge of the normal anatomy, proper ultrasonographic techniques, and the imaging findings of common and uncommon soft tissue lesions in children are crucial for accurate assessment and management of patients. In this article, we review the techniques and imaging findings focusing on the ultrasonographic features of a variety of superficial soft tissue lesions detected in children.
Keywords: Ultrasonography, MRI, Soft-tissue lesion, Soft-tissue tumor, Children
INTRODUCTION
Although most of the superficial soft-tissue lesions in children are benign, clinical findings are often nonspecific, requiring further imaging evaluation (1,2). Ultrasonography (US) is usually the initial study requested and has many benefits such as easy accessibility, no need for sedation, lack of radiation and superior resolution for soft tissue lesion (3,4,5). While some soft-tissue lesions can readily be diagnosed by clinical information and typical US findings, most of the solid lesions are non-specific and US can be used to determine the necessity of additional imaging such as MRI, and/or biopsy or surgical resection, and whether it can be left alone or followed (3,6).
In this article, we review the ultrasonographic technique and imagining findings of common and uncommon superficial soft-tissue lesions encountered in the pediatric population.
US Technique for Evaluation of Superficial Soft-Tissue Lesions
Before starting an US scan, it may be helpful to check the appearance of the lesion such as skin color change in well-illuminated environment and verify the clinical history, including age of onset, time course of the lesion, multiplicity, and symptoms (4).
Superficial soft-tissue lesions should be examined using a high frequency (> 10 MHz) linear transducer for maximal spatial resolution of superficial structures and detailed information of the layers of skin and subcutaneous tissues (Fig. 1). US parameters including gain, time gain compensation, depth and number of the focal zones, frequency, gray scales, and dynamic range must be properly optimized (4,5). It is important not to distort the lesion by applying sufficient amount of gel on the lesion and not pressing the lesion excessively.
Echogenicity of the lesion should be compared to the adjacent subcutaneous fat or muscle (7,8). US is very helpful in differentiating between cystic and solid lesion. An anechoic mass with posterior acoustic enhancement is the hallmark of a cystic lesion. Also, when pressed with a probe, cystic lesions are better pressed than solid lesions, although some cystic lesions do not deform on compression (7). Color Doppler scan is needed to confirm the vascular, solid or cystic nature of a mass. The sensitivity of the color Doppler scan can be improved by decreasing the scale level or pulse repetition frequency, increasing the color gain until color noise appears, and decreasing probe pressure on the lesion to avoid compressing small vessels. Spectral Doppler scan includes the type of waveform (arterial or venous), the magnitude of velocities, and resistive index (8).
Vascular Tumors
According to the International Society for the Study of Vascular Anomalies (ISSVA) classification for vascular anomalies, which updated in 2018, vascular anomalies are divided into vascular tumors and vascular malformations (9,10).
Vascular tumors can be classified as benign, locally aggressive or borderline, and malignant (9,10). Benign vascular tumors include infantile hemangioma, congenital hemangioma, tufted angioma, and lobular capillary hemangioma (9). Infantile hemangioma is not present at birth and may begin to grow in the first week to months, reaching its maximum size at 1 year of age followed by slow involution (11,12). On US, an infantile hemangioma during the proliferative phase usually appears as a well-defined mass located in subcutaneous tissue showing variable echogenicity and color Doppler shows increased internal vascular flow (Fig. 2) (12). After reaching its maximum size, the infantile hemangioma starts an involuting phase characterized by decrease in size, increase in echogenicity and decrease of internal vascular flow as a result of fibro-fatty replacement (10,12).
Congenital hemangiomas are present at birth by definition (11,12). According to their behavior after birth, congenital hemangiomas are classified as rapidly involuting congenital hemangioma (RICH), non-involuting congenital hemangioma (NICH), or partially involuting congenital hemangioma (PICH) (9,12). Compared to infantile hemangioma, congenital hemangioma is relatively rare, negative for glucose transporter 1 (GLUT1) and, at US, more often show inhomogeneous echogenicity with relatively large intralesional vessels, which are visible on gray-scale imaging (Fig. 3) (10,12).
Lobular capillary hemangioma is common in patients older than 6 months and most of the lesions can be diagnosed clinically. They present as a rapidly growing vascular skin lesion with bleeding (12). On US, they tend to be small in size, hypoechoic compared to subcutaneous fat and show increased vascular flow with high velocity on color Doppler scans (Fig. 4) (12,13).
Kaposiform hemangioendothelioma is a locally aggressive vascular neoplasm with infiltrative growth pattern, composed of spindle-shaped endothelial cells, and abnormal lymphatics. It mostly affects infants and commonly appears as a growing, red to purple plaque, which can be tender (10,12). On US, it appears as an ill-defined, heterogeneous lesion and can be focal or diffuse, confined to subcutaneous fat or involving all soft-tissue planes (Fig. 5) (10,12). It may be associated in cases more than 50% with profound sustained consumptive coagulopathy (Kasabach-Merritt phenomenon) (10,12,14).
Vascular Malformations
Vascular malformations can be mainly categorized histologically into lymphatic, capillary, venous, arteriovenous, or mixed malformations (9,15,16).
Venous malformation (VM) is the most common vascular malformation, presents in 1% of the general population (17,18). They usually present as palpable lesions and may show bluish skin color change or enlarged vessels. On US, VM appears as a well-defined mass with spongiform appearance (Fig. 6). They may have internal fluid-fluid levels due to very slow blood flow with blood stagnation and formation of hematocrit levels (17,19). The detection of intralesional calcifications representing phleboliths is very helpful in diagnosis of VM but phleboliths are uncommon in children (17). Color Doppler scan shows vascular flow with slow velocity, although it is not uncommon to have difficulty demonstrating intralesional vascularity in actual practice (17).
Lymphatic malformation (LM) can be divided into macrocystic, microcystic, and mixed types (20). Macrocystic lesions which are composed of cysts larger than 1–2 cm appear as multiseptated cysts on US (Fig. 7) and effectively decrease in size with aspiration or sclerotherapy (20). While venous spaces in a VM can be collapsed with compression, cystic spaces in a LM can be deformed but usually do not entirely collapse with compression (15). Microcystic LM often appears as solid hyperechoic lesions due to numerous tiny cysts that are too small to be seen by probe resolution and some scattered cysts may also be seen (17).
Adipocytic Tumors and Other Fat-Containing Mass-Like Lesions
US finding of fat-containing lesions can vary depending on the proportion of fat component. While lesions composed of pure fat tend to be hypoechoic on US, lesions with a mixture of fat and other soft-tissue components show increased echogenicity (21). Therefore, MRI including fat suppression sequences is often needed to confirm the presence of fat within a lesion.
Although lipoma composed of mature fat is common in the adult, it comprises only 4% of all soft-tissue tumor in children (22). On US, lipomas show various appearances depending on the composition ratio of the intralesional fat and water and tumor location. It usually appears as a homogeneous mass with variable echogenicity relative to adjacent structure (Fig. 8) (4,21).
Lipoblastoma, a benign tumor composed of both mature and immature adipocytes, occurring typically within the first 3 years of age, is the second most common adipocytic tumor accounting for about 30% and it often presents in the extremities with varying size (4–13 cm) (3,21,23). On US, lipoblastoma appears as a well-defined, predominantly homogeneous hyperechoic mass (Fig. 9), though it can be hypoechoic or isoechoic or mixed echogenic lesions with some internal cystic spaces due to variable components including fibro-myxoid components (21). They tend to be encapsulated with internal septa on MRI (23,24,25).
Subcutaneous fat necrosis is a benign entity that can often present with a palpable subcutaneous nodule of the torso or extremities (21,26). They can appear as a well-defined, isoechoic mass with a surrounding hypoechoic halo or a poorly defined hyperechoic lesion on US (Fig. 10) (21,27). Subcutaneous fat necrosis of the newborn is a rare, transient complication of birth asphyxia, hypothermia, and trauma. It is usually self-limiting condition but may result in serious complication such as hypercalcemia (26).
Fibroblastic and Myofibroblastic Lesions
Nodular fasciitis is an uncommon benign lesion, which grows rapidly due to local fibrous proliferation, accompanied by pain and can be mistaken for a malignant tumor or infection clinically and histologically (28,29,30). On US, it often appears as an ovoid mass located in the deep subcutaneous fat showing contiguity with a muscle facial plane (fascial tail sign), has a hypoechoic appearance with internal echogenic foci or peripheral hyperechoic nodules, and quite often does not show internal vascular flow (Fig. 11) (28).
Fibrous hamartoma of infancy is a rare benign soft-tissue tumor that usually occurs in the first 2 years of life (3). It presents as a painless mass in the subcutaneous layer and may show rapid growth. It shows ill-defined or lobulated margin located in the dermal and subcutaneous layer showing a combination of hyperechoic and hypoechoic area with a “serpentine pattern” due to presence of fat and fibrous tissue and poor vascularity on color Doppler (Fig. 12) (31).
Pericytic (Perivascular) Tumors
Infantile myofibroma or myofibromatosis is the most common fibrous tumors in infancy (32). They can be divided into three groups: solitary, multicentric without visceral involvement, and generalized with both cutaneous and visceral involvement (33). The solitary type is the most common, accounting for 50–80% of all cases and the multicentric form involves the subcutaneous fat, muscle, and bone (33). On US, infantile myofibromatosis typically appears as a hypovascular solid masses with variable echogenicity (Fig. 13) and, often, anechoic central portion due to central necrosis (33).
Neurogenic Lesions
Peripheral nerve sheath tumors are benign or malignant tumors of Schwann cell origin and include schwannomas, neurofibromas, and malignant peripheral nerve sheath tumors (MPNSTs) (34). US reveals a round or oval, homogeneous hypoechoic mass relative to adjacent muscle and exhibits posterior acoustic enhancement (Fig. 14) (34). Schwannoma is rare in children and neurofibroma appears as concentric, well-demarcated hypoechoic nodular lesions that do not displace the nerve fascicle but interfere with them. Neurofibroma tends to be more homogeneous than schwannoma and may show typical feature known as “target sign.” “Target sign” refers to the layered appearance of hyperechoic center and peripheral hypoechoic rim and it is due to the ultrastructure of neurofibroma with a fibrocollageneous center surrounded by a myxomatous periphery (34,35). Plexiform neurofibroma, which is pathognomonic for neurofibromatosis type 1, diffusely involves a nerve segment and its branches, giving a “bag of worms” appearance (34,36). Malignant transformation from plexiform neurofibroma to MPNST occurs in up to 50% of neurofibromatosis patients. MPNSTs present with pain, rapid growth, and neurologic deficit (34,37). While US cannot reliably distinguish benign from malignant lesions, MRI is useful in distinguishing MPNST from benign lesion with imaging features including loss of “target sign” on T2-weighted image, presence of peripheral enhanced pattern, perilesional edema like zone, and intratumoral cystic lesion or necrosis (38). Increased uptake on fluorodeoxyglucose-positron emission tomography scan can also be helpful (36,39,40).
So-Called Fibrohistiocytic Tumors
Giant cell tumor of the tendon sheath often appears as a painless soft-tissue mass composed of multinucleated giant cells, histiocytes, and xanthoma cells (4). On US, it is hypoechoic and appears as a well-defined mass surrounding the normal tendon and shows independent movement of the tendon and soft-tissue mass (Fig. 15) (4).
Other Benign Lesions
In children, ectodermal (epidermal and dermal) inclusion cysts are often congenital and are found in sites of embryological fusion (near sutures and midline). They contain keratin debris surrounded by a wall of stratified squamous epithelium (41). US shows well-circumscribed, ovoid-shaped, mildly echogenic masses with occasional linear anechoic and/or echogenic reflection, increased through-transmission, hypoechoic rim, and no color Doppler flow (Fig. 16). When the epidermal inclusion cysts rupture, they show lobulated shape, slightly poorly defined boundary, and intermediate grades of lesion vascularity (Fig. 17) (42,43).
Pilomatricoma is a benign, superficial tumor of the hair follicle (3). It is the third most commonly resected superficial mass in children after dermoid/epidermoid cysts and lymph nodes (3). Lesions are typically located on the head, neck, face, and upper extremities and are typically very hard on palpation. On US, the lesion appears as a small, ovoid, heterogeneous or predominantly echogenic mass with internal bright echogenic foci corresponding to calcification. They may show peripheral or internal flow on color Doppler imaging (Fig. 18) (44,45).
Ganglia typically present with pain or palpable abnormality, most commonly on the hand or wrist (4). On US, ganglia are usually anechoic (50%); they can be hypoechoic (35%) (Fig. 19) or mixed anechoic and hypoechoic (15%) (46,47). They are usually well-defined and show multiple lobulations. The most important finding is an association with joint or tendon sheath indicating the anatomic origin of the mass (6).
Malignant Soft-Tissue Tumors
Rhabdomyosarcoma (RMS) is the most common pediatric soft-tissue sarcoma (48,49). On US, RMS usually appears as a well-defined, slightly hypoechoic inhomogeneous mass that can show significantly increased vascular flow on color Doppler US (Fig. 20) (48).
Synovial sarcoma, the second most common pediatric soft-tissue sarcoma, usually appears as a juxta-articular, well-demarcated, solid mass (Fig. 21) (3,49). Typical MRI findings include a juxta-articular mass with triple signal pattern areas that are hypointense, isointense, and hyperintense to fat on T2-weighted image (50). Synovial sarcoma may sometimes be mistaken for a benign lesion when it is small at initial presentation (51).
Infantile or congenital fibrosarcoma is usually found in children younger than 2 years of age, accounting for 12% of soft-tissue malignancies in infancy (33). It shows much more favorable prognosis than the classic adult fibrosarcoma and frequently involves the extremities, trunk, head and neck regions. US typically shows a heterogeneous, hypervascular mass that may mimic hemangioma (Fig. 22) (33). Subcutaneous panniculitis-like T-cell lymphoma is a rare subtype of peripheral T-cell lymphoma, presented with multiple palpable nodules on the trunk, extremities, and face (52). On US, it appears as poorly defined, hyperechoic lesions in the subcutaneous fat layer. (Fig. 23) (52,53).
Multiple, subcutaneous nodules in neonates and infants should raise a concern for underlying malignancy. In a study of 280 neonates with cutaneous metastasis, leukemia was the most common (35%), followed by Langerhans cell histiocytosis (21%), neuroblastoma (17%), rhabdoid tumor (11%), and RMS (6%) (54). Superficial soft tissue metastases appear as well-demarcated, hypoechoic, solid nodules in the subcutaneous fat, often simulating benign lesions due to small size (Fig. 24) (55,56).
Therefore, size and margin of soft-tissue lesions are not considered as significant factors indicating malignancy. Definite benign lesions appear as a pure cyst or as a fat-only lesion (lipoma) and without such typical findings, possibility of malignancy cannot be excluded (48,55,57,58). Size greater than 5 cm, involvement of deep fascial layer and the presence of internal necrosis or hemorrhage can be significant markers of malignant tumors (58,59).
CONCLUSION
As a frequent initial workup of pediatric superficial soft-tissue tumors and tumor-like lesions, US is able to provide a specific diagnosis in some benign conditions, narrow the differential diagnosis and identify lesions which need additional imaging or biopsy, while US findings should always be considered in the context of clinical presentation. Knowledge of US technique and key imaging finding of a variety of soft tissue lesions encountered in children will facilitate establishing the correct diagnosis and guiding the management.
Footnotes
Conflicts of Interest: The authors have no potential conflicts of interest to disclose.
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