Infantile Fibrosarcoma—A Clinical and Histologic Mimicker of Vascular Malformations: Case Report and Review of the Literature

Abstract

Infantile fibrosarcoma is a rare soft tissue tumor that usually presents either at birth or in the 1st year of life. Here we describe a case of a 4-month-old female who presented with a congenital right axillary mass. The initial clinical impression was benign vascular/lymphatic malformation. The core biopsy showed a spindle cell lesion with abundant vasculature represented by small vascular channels. However, immunohistochemical analysis did not support a diagnosis of vascular lesion/tumor. Polymerase chain reaction study for ETS Translocation Variant 6/neurotrophic tyrosine kinase receptor, type 3 fusion transcript was positive, and the diagnosis of infantile fibrosarcoma was established. The patient underwent resection of the axillary mass. Microscopic examination of the resection specimen showed numerous vascular channels. Intermixed there were also cellular areas composed of spindle cells similar to those seen in the biopsy material. Molecular studies were repeated and confirmed the diagnosis of infantile fibrosarcoma. Infantile fibrosarcoma has been previously reported in the literature to clinically masquerade as hemangioma. In addition, this case proves that infantile fibrosarcoma could also mimic vascular malformations on clinical, radiologic, and pathologic exams. In fact, the vascular component of the tumor is very unusual in our patient and represents a histologic feature that has not been described before. The case highlights the diagnostic challenges at clinical, radiologic, and pathologic levels in some cases of infantile fibrosarcoma and raises awareness among clinicians and pathologists related to another peculiar pattern that can be encountered in this disease.

Keywords

infantile fibrosarcoma vascular malformation ETV6/NTRK3 fusion product

INTRODUCTION

Infantile fibrosarcoma is a rare soft tissue tumor that is usually congenital or develops in the 1st year of life. Clinically it presents as a localized, well-delineated swelling after birth, with progressive growth. Sometimes a prominent vascular component is present within the tumor. In these cases, the mass could be clinically interpreted as a vascular lesion, in particular congenital hemangioma [1 –11]. Herein we present a case of infantile fibrosarcoma misinterpreted clinically and radiologically as a vascular malformation. Even on histologic examination the vascular component was very prominent and unusual. The rarity of this tumor, as well as its potential to mimic other entities, may render a diagnostic challenge that can result in misdiagnosis and subsequent inappropriate patient management. This case raises awareness among clinicians and pathologists of another rare pattern that infantile fibrosarcoma can exhibit.

CASE REPORT

The patient was a 4-month-old female who came to medical attention for a right axillary mass. The lesion had been present since birth and had grown considerably since then. The patient had no significant medical history otherwise. No signs of infection were noted. At physical examination her neck was supple and she had no lymphadenopathy. There was a 2-cm, smooth, well-defined soft mass on the right lateral chest wall at the lower border of the axilla. There was no tenderness, redness, or drainage from the area. The ultrasound examination revealed a cyst in the subcutaneous fat layer, consistent with a lymphangioma.

A biopsy of the lesion was performed. During the procedure a large amount of blood was drained from the lesion, and, in fact, the mass decreased in size following biopsy. These findings were supportive again of a vascular/lymphatic process. The touch imprints showed blood and clusters of monotonous spindle cells with elongated nuclei with rounded ends, finely dispersed chromatin, and inconspicuous nucleoli (Fig. 1A). In correlation with the cytology, microscopic examination of the biopsy cores revealed a cellular lesion with abundant vasculature. The lesion was composed of spindle cells with few admixed inflammatory cells (lymphocytes and plasma cells) and mainly small-sized vessels (Fig. 1B). The spindle cells were mildly pleomorphic and did not show a particular architectural arrangement (Fig. 1C). Rare mitotic figures were seen. The vessels were lined by bland endothelial cells. The initial impression, based on light microscopy, was of kaposiform hemangioendothelioma. However, immunohistochemical stains did not support this diagnosis: CD31 and smooth muscle antigen (SMA) immunostains highlighted only the vascular spaces and were negative in the tumor cells; glucose transporter 1 (GLUT-1), D2-40 (podoplanin), desmin, and activin receptor-like kinase 1 immunostains were also negative. Given the clinical presentation, as well as prior reports of infantile fibrosarcoma mimicking hemangiomas, polymerase chain reaction studies for ETS Translocation Variant 6/neurotrophic tyrosine kinase receptor, type 3 (ETV6/NTRK3) fusion transcript were performed and were positive. These findings were consistent with the diagnosis of infantile (congenital) fibrosarcoma.

Figure 1.

Microscopic examination of the biopsy. (A) Touch imprints showing blood and clusters of monotonous spindle cells with elongated nuclei with rounded ends, finely dispersed chromatin, and inconspicuous nucleoli (Diff-Quick stain, ×200). (B) The lesion is composed of spindle cells with few admixed inflammatory cells and small-sized vessels (hematoxylin and eosin stain, ×100). (C) The spindle cells are mildly pleomorphic and do not show a particular architectural arrangement. Rare mitotic figures are seen. The vessels are lined by bland endothelial cells (hematoxylin and eosin stain, ×400).

Two weeks later, the patient underwent excision of the axillary lesion. Gross examination of the resection specimen showed a 4.4 × 4.0 × 3.0–cm, well-delineated mass with a variegated aspect, composed predominantly (∼70%) of cystic spaces filled with blood alternating with solid soft, dark red areas occupying about one third of the mass (Fig. 2A). Microscopic examination revealed a well-demarcated, deep-seated lesion with a predominant vascular component, different from the one observed on the biopsy material. This time the vessels were medium to large in size, ectatic, and creating anastomosing channels, mostly with a thin wall (Fig. 2B) showing occasional SMA-positive bundles of smooth muscle (Fig. 2C,D). Within the walls of the vascular channels there were plump spindled cells with elongated nuclei and a fair amount of eosinophilic cytoplasm, similar to the lesional cells present in the biopsy. The cells showed low-grade nuclear pleomorphism and low mitotic activity. The solid component resembled the biopsy sample and consisted of similar lesional cells (Fig. 2E). Repeated immunohistochemical studies revealed a pattern of staining analogous to that seen on the biopsy material, with CD31 and SMA stains highlighting the vascular spaces and being negative in the tumor cells (Fig. 2F,G). Molecular studies (reverse transcriptase–polymerase chain reaction) for ETV6/NTRK3 fusion product were repeated and again were positive. Based on these findings a final diagnosis of infantile fibrosarcoma with a prominent vascular component was rendered.

Figure 2.

Gross and microscopic findings of the resection specimen. (A) Macroscopic appearance of the resection specimen showing a well-delineated mass with a variegated aspect on cut section, composed of solid, soft, dark red areas alternating with cystic spaces filled with blood. (B) The lesion contains numerous ectatic vessels that are medium to large in size, creating anastomosing channels (hematoxylin and eosin stain, ×40). (C) These large vessels are thin-walled, and some are surrounded by a small amount of smooth muscle (arrow) (hematoxylin and eosin stain, ×200). (D) Smooth muscle actin (SMA) immunostain highlights wisps of smooth muscle bundles within the vessel walls (×400). (E) The hypercellular areas are composed of plump spindled cells with elongated nuclei and a fair amount of eosinophilic cytoplasm, similar to the lesional cells present in the biopsy (hematoxylin and eosin stain, ×200). (F) CD31 immunostain highlights the vessels; tumor cells are negative (×200). (G) SMA immunostain highlights the vessels; tumor cells are negative (×200).

DISCUSSION AND LITERATURE REVIEW

Congenital infantile fibrosarcoma is an indolent, slow-growing, malignant spindle cell tumor that is present at birth or occurs in the infancy period. It presents as a well-defined lesion that is usually located on the extremities, but head/neck area and trunk are also common locations.

Clinically, infantile fibrosarcoma can mimic other entities. It has been reported [12] to be misdiagnosed as teratoma. However, the most frequently reported clinical masquerader of infantile fibrosarcoma is a vascular proliferation, in particular hemangioma [1 –11], with only one other case being clinically misinterpreted as vascular malformation [7]. Moreover, infantile fibrosarcoma can present with massive bleeding from the tumor and a clinical picture of Kasabach-Merrit syndrome [1,4,8], creating confusion with a kaposiform hemangioendothelioma [8].

Our present case shows that infantile fibrosarcoma can mimic vascular/lymphatic malformations in addition to hemangiomas not only on physical and radiologic exam but also histologically. The patient presented clinically with what appeared to be a vascular proliferation. The differential diagnosis for a congenital enlarging vascular lesion usually includes a number of common entities, such as hemangiomas or vascular malformations; malignancies are less likely to be considered. Radiology studies have shown poor discrimination between highly vascularized malignant soft tissue lesions and benign vascular proliferations [13]. This fact is also illustrated by our case as well as by prior reports [1 –10,Table 1], in which the radiologic techniques commonly detected a mass with prominent vessels, sometimes with a cystic, hemorrhagic appearance similar to that seen in our case [1,8] and could not establish the correct diagnosis, misinterpreting the tumor as being a benign vascular proliferation. The upper extremities (including the shoulder/axillary region) seemed to be the most common location in these cases. There appears to be an equal distribution between male and female patients in this case study. With the exception of 2 cases [3,9], all of the other lesions were present at birth.

Table 1.

A review of prior infantile fibrosarcoma cases mimicking vascular lesions

Reference	Patient age	Patient gender	Location	Size (cm)	Clinical impression	Radiologic impression	Histologic findings	Final pathologic diagnosis
Boon et al. [1]	Case 1: lesion present at birth	Female	Right cervico-occipital region	Same size as cranium	Hemangioma with KM	US: eccentric cystic component consistent with hemorrhage surrounded by more solid-appearing tissue	N/A	Congenital fibrosarcoma
	Case 2: congenital	Male	Right scapula	9	Hemangioma with KM	US and CT: hypervascular tumor fed by large-caliber vessels; the center of the tumor appeared cystic; solid at the periphery	N/A	Congenital fibrosarcoma
Cisse et al. [2]	Congenital lesion	N/A	Sole of the left foot	N/A	Congenital hemangioma (RICH)	N/A	Initial histopathologic examination suggested highly remodeled immature infantile hemangioma. Reanalysis of the histology slides resulted in a diagnosis of infantile fibrosarcoma; positive for the ETV6/NTRK3 translocation	Infantile fibrosarcoma
Jain et al. [3]	6 Months old	Female	Right shoulder	6	Hemangioma	US: heterogeneous, lobulated hypoechoic mass with increased vascularity	Highly cellular tumor with closely packed fascicles of spindle cells; prominent hemangiopericytoma-like vascular pattern	Infantile fibrosarcoma
Kagawa et al. [4]	Present at birth	Female	Left upper anterior thigh	17.5	Hemangioma with KM	CT: large mass in the soft tissue not involving the bone; the angiogram showed small vessels coursing through the lesion	Neoplastic cells arranged in fascicles	Infantile fibrosarcoma
Kerl et al. [5]	Newborn	Female	Left elbow/upper arm	10	Capillary hemangioma	Prenatal ultrasound: the mass was interpreted as extrafetal dead twin; MRI: differential diagnosis was capillary hemangioma, hemangioendothelioma, or fibromyosarcoma	Spindle cell mesenchymal tumor with moderately chromatin dense nuclei; positive for the ETV6/NTRK3 translocation	Infantile fibrosarcoma
Kimura et al. [6]	Congenital	Male	Right hand	10	Hematoma/hemangioma	MRI: the tumor was solid, irregularly enhanced by contrast, and had low vascularity and unclear margins	Tumor composed of dense, complicated arrangement of spindle cells with a partial herringbone pattern; abnormal mitoses were seen	Infantile fibrosarcoma
Mnif et al. [7]	Newborn	Male	Right forearm	10	Lymphatic/vascular malformation	MRI: mass with low signal intensity on T1-weighted images with focal areas of high signal intensity due to hemorrhage; high signal on T2-weighted images	Sheets of closely packed spindle cells arranged in bundles, prominent mitosis	Infantile fibrosarcoma
Muzaffar et al. [8]	Seen on US at 33 wk gestation	Female	Left hand	5.4	Kaposiform hemangioen dothelioma	MRI: solid neoplasm with isolated cystic areas interpreted as being consistent with hemangioma or lymphangioma	Spindle cell tumor with 2 patterns: areas with myxoid stroma and elongated stellate cells with no striations and other regions with plump spind and roimd cells with vesicular nuclei and eosinophilic cytoplasm; positive for the ETV6/NTRK3 translocation	Infantile fibrosarcoma
Sukop et al. [9]	2 mo	Female	Left forearm	4	Organizing hematoma	US: richly vascularized tumor, suspected to be a combination of hemangioma and hematoma	Positive for the ETV6/NTRK3 translocation	Infantile fibrosarcoma
Yan et al. [10]	Case 1: congenital	Male	Right palm	N/A	Ulcerated hemangioma	MRI: soft tissue mass peripheral filling followed by central filling, consistent with vascular malformation	Hypervascular tumor with spindle cells; positive ETV6/NTRK3 fusion gene	Infantile fibrosarcoma
	Case 2: present at birth	Male	Right hand	5.5	Ulcerated hemangioma	N/A	Densely arranged spindle cells with multiple mitoses	Infantile fibrosarcoma
	Case 3: present at birth	Male	Left hand	3.5	Ulcerated hemangioma	N/A	Hypercellular spindle cell tumor with necrosis, low mitotic activity; positive for the ETV6/NTRK3 translocation	Infantile fibrosarcoma
Present case	Present at birth	Female	Right axilla/trunk	4.4	Lymphatic/vascular malformation	CT: cyst in the subcutaneous fat layer, consistent with a lymphangioma	Spindle cell lesion with small vascular channels on biopsy; large vessels on resection specimen; positive for the ETV6/NTRK3 translocation	Infantile fibrosarcoma

KM indicates Kasabach-Merrit; US, ultrasound; N/A, not applicable; CT, computed tomography; RICH, rapidly involuting congenital hemangioma; ETV6, ETS Translocation Variant 6; NTRK3, neurotrophic tyrosine kinase receptor, type 3; MRI, magnetic resonance imaging.

In all cases, the definitive diagnosis relied on histopathological characteristics. Typically the microscopic appearance of infantile fibrosarcoma is that of a cellular tumor composed of uniform spindle cells arranged in fascicles, sometimes with a herringbone arrangement. Hemangiopericytoma-like vessels could be seen within the lesion. However, there is an impressive histologic diversity of these tumors: some can show a poorly organized pattern of immature and even primitive mesenchymal cells; others can have a variable number of admixed inflammatory cells. Our case also exhibited an unusual histologic pattern and represented a diagnostic challenge. After reviewing the biopsy material, the 1st impression was of kaposiform hemangioendothelioma, given the small elongated vascular spaces and slightly atypical spindle cells, with rare mitosis admixed with occasional plasma cells, although other soft features seen in kaposiform hemagioendothelioma (cytoplasmic hyaline globules, fragmented red blood cells, and platelet thrombi) were not detected in our case. Another consideration was an infantile hemangioma in the proliferative phase, but the lobular architecture of this lesion was not apparent in our patient. However, the diagnosis of a vascular tumor was not supported by the immunohistochemistry studies (negative CD31, podoplanin, GLUT-1 stains). Only the patient's age, clinical presentation, and previous reports of infantile fibrosarcoma misdiagnosed as vascular lesions prompted us to perform molecular studies, which confirmed the diagnosis. The resection specimen was very puzzling as well: it also had a prominent vascular component representing about 70% of the lesion, characterized this time by large, thin-walled vascular channels, some with smooth muscle within the walls. No hemangiopericytoma-like vessels were present. Lymphatics were also absent, as D2-40 immunostain was negative. In the absence of a previous diagnosis (such as in our case, in which infantile fibrosarcoma had already been diagnosed by molecular studies performed on the biopsy material), one can easily misinterpret this type of lesion as a vascular (in particular, a venous/arterio-venous) malformation. The morphologic appearance of this vascular component is very unusual in infantile fibrosarcoma; commonly, the vessels seen within this tumor have a hemangiopericytomatous appearance. Microscopy in 2 of the prior cases [2,10: case 1] also revealed a hypervascular lesion, but in contrast to our case, the histologic exam resembled more closely a hemangioma [2]. In fact, both of these cases required reevaluation of the pathology slides for a correct diagnosis. The morphology in the remaining cases was straightforward, and a final diagnosis of congenital/infantile fibrosarcoma was rendered.

As is shown by the present case, molecular studies are very helpful in those instances with peculiar morphologic appearance. Infantile fibrosarcoma has a distinctive reciprocal translocation, t(12;15)(p13;q25), resulting in ETV6/NTRK3 gene fusion. This rearrangement, described by Knezevich and colleagues [14], fuses the ETV6 (also known as the TEL) gene from 12p13 with the NTRK3 gene (also known as TrkC) on 15q25. ETS Translocation Variant 6 is a member of the E 26 family of transcription factors and is essential for developmental processes such as hematopoiesis and yolk-sac angiogenesis; NTRK3 is a transmembrane surface receptor for neurotrophin-3, has protein tyrosine kinase activity, and is primarily expressed in the central nervous system, where it is involved in growth, development, and cell survival. The ETV6/NTRK3 chimeric protein has been linked to multiple signaling cascades, including Ras-MAP kinase and PI3K-AKT, through the IRS-1 adaptor protein [15]. It has been shown to have potent in vivo and in vitro transforming activity in several cell lineages, including fibroblasts [16], hematopoietic cells [17], and breast epithelial cells [18]. As such, it is not surprising to find this translocation as a recurrent phenomenon in infantile fibrosarcoma. In one review [19], the chimeric gene was observed in 10 of 11 cases and helped distinguish congenital fibrosarcoma from other spindle cell lesions encountered in children. The same translocation has also been detected in other tumors, some of which are seen in childhood, namely, congenital mesoblastic nephroma [20] and acute myelogenous leukemia [21], as well as in secretory carcinoma of the breast [18].

Interestingly, neurotrophin-3 (the NTRK3 ligand) has recently has been demonstrated [22] to be a novel angiogenic factor capable of neovascularization in a mouse model of limb ischemia. This finding might explain the prominent vasculature in some cases of infantile fibrosarcoma: it is possible that constitutive activation of the NTRK3 tyrosine kinase function due to ETV6/NTRK3 fusion leads to development of numerous vascular channels within the tumor. The relationship between the neoplastic cells of infantile fibrosarcoma and the vascular component of the lesion is probably even more intriguing: in a case report by Miura and colleagues [23], congenital fibrosarcoma showed regression during the course of the disease and transformation to hemagiopericytomatous tissue that lost expression of the ETV6/NTRK3 fusion gene. Based on these findings, one might wonder if infantile fibrosarcoma has a vascular origin. In fact, the histogenesis of this disease is not well understood, but morphologic similarities between congenital fibrosarcoma, infantile myofibromatosis, and congenital hemangiopericytoma point to the fact that these entities are histogenetically related [24,25]. In a study by Blizniukov and colleagues [26], ultrastructural analysis revealed well-differentiated collagen-forming neoplastic fibroblasts in about half of the infantile fibrosarcoma cases; immature embryonic-like fibroblasts closely resembling perichondrial fibroblasts of the embryonic limb at 6 weeks of development were also identified.

Generally, infantile fibrosarcoma has an excellent prognosis and a very low metastatic rate. Initial optimal treatment is complete surgical excision, which is associated with a survival rate of about 90% in long-term studies [27]. The role of preoperative chemotherapy hasn't been well defined, but this therapy can be used when the tumor is located in a difficult surgical area to decrease tumor size and facilitate the surgery. Postoperative chemotherapy can be used when the microscopic surgical margins are positive for tumor. Radiation therapy is usually avoided as a result of its associated growth disturbances.

The findings presented here highlight the importance of considering less-likely entities when an infant presents with what appears to be clinically and radiologically a vascular lesion. In fact, many conditions that can masquerade as infantile hemangioma were reported [28], some of which are malignant and require immediate and appropriate management. Infantile fibrosarcoma is one of them and should be considered in the differential diagnosis of congenital tumors with a prominent vascular component. This challenging case also points to a peculiar, novel histologic appearance of infantile fibrosarcoma with prominent larger caliber vascular channels without a hemangiopericytomatous look. This pattern can impose diagnostic challenges to the unaware pathologist and proves that congenital fibrosarcoma can be mistaken for a vascular lesion even on morphologic exam.

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