- Email: [email protected]
Nodular fasciitis: a retrospective study of 272 cases from China with clinicopathologic and radiologic correlation
Annals of Diagnostic Pathology 19 (2015) 180–185
Contents lists available at ScienceDirect
Annals of Diagnostic Pathology
Radiologic-Pathologic Correlation
Nodular fasciitis: a retrospective study of 272 cases from China with clinicopathologic and radiologic correlation Linhui Lu, MD a,c, I Weng Lao, MD a,c,1, Xiaohang Liu, MD b,c, Lin Yu, MD a,c, Jian Wang, MD a,c,⁎ a b c
Department of Pathology, Fudan University Shanghai Cancer Center, Shanghai, China Department of Radiology, Fudan University Shanghai Cancer Center, Shanghai, China Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China 200032
a r t i c l e
i n f o
Keywords: Nodular fasciitis Radiology Myofibroblast Immunohistochemistry
a b s t r a c t Our aim is to describe the largest series of nodular fasciitis (NF) with emphasis on the clinicopathologic and radiologic correlation. A total of 272 cases of NF were diagnosed between 2004 and 2014 at our institution. There were 160 males and 112 females with age ranging from newborn to 77 years (mean, 36 years). The upper extremity was the most common location (34%), followed by the head and neck region (24%), trunk (21%), and lower extremity (14%). By radiology, the lesion appeared as well-defined homogeneous mass with low or isodensity on computed tomography, homogenous hypointense or isointense on T1-weighted sequences, and heterogeneous intermediate-to-high signal on T2-weighted sequences. Although all cases were composed of short intersecting fascicles of uniform plump spindle cell, the cellularity and stromal components varied considerably between different cases. In intramuscular or deeply seated NFs, extension into adjacent skeletal muscles or structures was often noted. Immunohistochemically, all cases showed diffuse staining for smooth muscle actin and calponin, with consistent negativity for desmin, h-caldesmon, and β-catenin. Of patients with available followed up information, only 1 experienced local recurrence due to incomplete excision. Our comprehensive study further demonstrated that NF had a wide clinicopathologic spectrum. Correlation with the radiologic features may help pathologists in arriving at an accurate diagnosis. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Nodular fasciitis (NF) is a benign myofibroblastic proliferation that occurs predominantly in the subcutaneous tissue of young to middleaged adults [1]. It typically presents as a fast-growing nodule that usually reaches 2 to 3 cm in size within few weeks. The most common site is the upper extremities, followed by the trunk, head and neck region [2-6]. Occasionally, the lesion may arise in unusual locations including the salivary gland, breast, mesentery, and vulva [7-11]. In most instances, it develops in the subcutaneous tissue and underlying fascia and appears as a well-defined nodule. On rare occasions, it may also occur in the dermis or arises within the skeletal muscles, vessels, joints, and peripheral nerves [12-25]. Because of the rapid growth, high cellularity, remarkable mitotic activity, local infiltration into adjacent tissues, and unusual clinical settings in some instances, misdiagnosing NF as a sarcomatous lesion continues to be a challenge for pathologists, which may lead overtreatment to the patients. A multidisciplinary study combining the clinical, pathologic, and radiologic characteristics on NF
⁎ Corresponding author at: Department of Pathology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai 200032. Tel.: +86 21 64175590 88325; fax: +86 21 64046007. E-mail address: [email protected] (J. Wang). 1 Dr I Weng Lao contributed equally in this study and thus be considered as cofirst author. http://dx.doi.org/10.1016/j.anndiagpath.2015.03.013 1092-9134/© 2015 Elsevier Inc. All rights reserved.
is sparse. In this study, we undertake a retrospective review of the largest series of NF with emphasis on the clinical, pathologic, and radiologic correlation. 2. Materials and methods A retrospective study design was formulated, and institutional review board approval was obtained. Between January 2004 and December 2014, a total of 272 cases with NF were diagnosed at our institution. Special variants of NF such as cranial fasciitis, intravascular fasciitis, and ischemic fasciitis were excluded from the study. Clinical presentations, tumor site and size, radiologic appearance, and treatment information were obtained from the medical record, radiology and pathology reports, and discharge summary. The follow-up information was conducted via medical records or from the referring pathologists. Four-micrometer-thick hematoxylin and eosin–stained section was reexamined. Representative paraffin blocks or unstained slides containing tumor material from each case were selected for immunohistochemical study. The primary antibodies used in the study include smooth muscle actin (1A4, dilution 1:200; DAKO), desmin (D33, dilution 1:100; Dako), calponin (CALP, dilution 1:150; Maixin), CD10(SP67, ready to use; VENTANA), h-caldesmon (h-CD, dilution 1:300; DAKO), CD34 (QBEnd 10, dilution 1:100; DAKO), CD68 (KP1, dilution 1:600; Changdao), β-catenin (β-catenin1, dilution 1:200; DAKO), and cytokeratin (AE1/AE3, dilution 1:50; DAKO). Pretreatment was
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
carried out according to manufacturer's recommendation. Omission of primary antibody and substitution by nonspecific immunoglobins were used as negative controls. Appropriate positive controls were run concurrently for all antibodies tested.
181
surgery. In patients with follow-up information (ranging from 2 to 110 months), none of them experienced local recurrence except one after incomplete excision. 3.2. Imaging studies
3. Results 3.1. Clinical findings There were 160 males and 112 females with a ratio of 1.4:1. The patient's age at presentation ranged from newborn to 77 years. The newborn presented with a mass arising in the dorsal aspect of ulnar side of his left hand, whereas the oldest is a 77-year-old man who had a mass in his left shoulder. The mean and median ages were both 36 years. Approximately 65% of patients were in their third to fifth decades, whereas children (aged b10 years, 9 cases) and elderly patients (aged N60 years, 16 cases) accounted for 3.3% and 5.9%, respectively (Fig. 1). Clinically, most patients presented with a solitary subcutaneous nodule, which grew rapidly within 2 weeks or 1 month before surgical excision. However, patients with a preoperative duration of several months were not uncommon. One patient presented with 1-year history. Approximately three-fourths of patients were associated with slight pain or tenderness on palpation. Two patients with intraneural NF presented with symptoms of peripheral neuropathy. The patient with a tumor arising within the lateral cord of the left brachial plexus complained of left shoulder pain associated with numbness of the left thumb and index finger. Another patient with a tumor of the right median nerve complained of pain and numbness with decreased sensation of the right hand. History of antecedent trauma was not documented in all cases. With regard to the anatomic site, 92 cases (34%) were located in the upper extremities especially the forearm, 65 cases (24%) in the head and neck region, 56 cases (21%) in the trunk, 37 cases (14%) in the lower extremities especially the thigh, 9 cases (3.3%) in the breast, 8 cases (2.9%) in the groin, and 5 cases (1.8%) in the vulva. Of the upper extremities, 45 cases were located in the volar aspect of the forearms, followed by shoulder (n = 18), upper arm (n = 11), elbow (n = 8), hand (n = 7, 5 in the palm and back of hand, 2 in the finger), and axillary (n = 3). Of the head and neck region, tumor occurred in the neck (n = 36); cheek (n = 11); supraclavicular region (n = 5); external ear region (n = 4); orbit (n = 4); temple (n = 2); and forehead, eyelid, and oral cavity (1 case each). Of the trunk, 26 cases were located in the chest wall, followed by back (n = 20), waist (n = 5), and abdominal wall (n = 5). Of the lower extremities, 20 cases were located in the thigh, followed by hip (n = 9), knee (n = 4), leg (n = 2), and foot (n = 2, 1 each in the heel and plantar). All patients were treated by
Of 29 patients with recorded examinations, 15 patients had ultrasonography only before excision. Ultrasound scan usually showed a welldefined hypoechoic or isoechoic lesion situated in the subcutaneous tissues. Computed tomography (CT) or magnetic resonance imaging (MRI) was available in 14 cases. The lesion usually appeared as a fascia-based well-defined oval mass (Fig. 2A). A few intramuscular lesions were relatively large with ill-defined margins. On CT, it was low or isodense compared with adjacent muscles. In cases with cystic and mucoid degeneration, contrast-enhanced CT scan showed heterogeneous appearance with prominent peripheral rim-like enhancement in some cases (Fig. 2B). On MRI, it was homogenous hypointense or isointense on T1-weighted (T1WI) and heterogeneous intermediate to hyperintense on T2-weighted (T2WI) with enhancement after gadolinium administration (Fig. 2C-F). 3.3. Pathologic features All lesions were solitary. Apart from 1 intradermal case, 1 periosteal case, and 16 intramuscular cases (5.9%), all the remaining cases were subcutaneous. They were described as wellcircumscribed soft, rubbery-to-firm nodules or masses with glistening appearance on cut section (Fig. 3). The excised specimens measured from 0.5 to 7.0 cm in maximum diameter, with a mean and median size of 2.3 and 2.0 cm, respectively. Of note, the lesion in 238 cases (87.5%) was smaller than 4 cm. Those with a greatest dimension larger than 4 cm were mostly deeply seated or intramuscular lesions. At low-power magnification, most were well circumscribed but unencapsulated (Fig. 4A and B), whereas a minority of cases had poorly defined borders with infiltration into the surrounding adipose tissue, skeletal muscle, or parotid gland (Fig. 4C-E). Entrapped nerve fascicles were noted in 2 intraneural NFs (Fig. 4F). On high power, typical cases were composed of uniform bland spindle cells that arranged in short intersecting fascicles within a loose stroma with extravasated erythrocytes and scattered lymphocytes (Fig. 5A). However, the cellularity and the stroma components varied considerably between cases, ranging from hypercellular with less stromal material, highly myxoid with abundant mucoid matrix to heavily hyalinized with deposition of keloid-like collagen fibers (Fig. 5B-D). Cases with combined areas were not uncommon (Fig. 5E). Mucoid degeneration was a frequent feature, which was prominent in a few cases creating a broken fish net-like appearance (Fig. 5F). Approximately 10% of cases contained scattered multinucleated giant cells. These giant cells had more eosinophilic cytoplasm. Compared with the classic osteoclasts, these giant cells were relatively smaller and could contain only 2 to 3 nuclei. Their presence ranged from scarce that could be easily ignored to numerous (Fig. 5G and H). Generally, mitotic figures were not difficult to find (ranging from 1 to 10/10 high-power field), but cytologic pleomorphism and nuclear atypia were absent. 3.4. Immunohistochemical study
Fig. 1. Age and sex distribution in 272 patients with NF.
The spindle cells showed diffuse expression of smooth muscle actin (Fig. 6A). They were also positive for calponin, muscle specific actin, and CD10. Intralesional histiocytes and small multinucleated giant cells were positive for CD68 (Fig. 6B). Other markers including desmin, h-caldesmon, β-catenin AE1/AE3, CD34, and S-100 protein were all negative.
182
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
Fig. 2. A fascia-based oval mass in the occipital region with heterogeneous intermediate-to-high signal on T2-weighted sequences (A). Cystic and mucoid degeneration with prominent peripheral rim-like enhancement on contrast-enhanced CT scan in an intramuscular NF (B). Nodular fasciitis of the left brachial plexus (C and D) and left fourth finger (E and F) showing homogenous T1 signal isointense to adjacent skeletal muscles and heterogeneous intermediate-to-high signal on T2-weighted sequences.
4. Discussion Nodular fasciitis is a benign self-limited process, which was originally reported by Konwaller et al [1] in 1955. Although a history of antecedent trauma has been documented in a small proportion of cases, the
Fig. 3. Intramuscular NF appeared as a well-circumscribed firm nodule with glistening appearance on cut section.
etiology remains uncertain. For a long time, it has been considered as a reactive lesion. However, recent molecular cytogenetic study revealed a recurrent MYH9-USP6 fusion gene, indicating a clonal neoplastic disorder of NF [26]. Nodular fasciitis is also well known as pseudosarcomatous fasciitis because it was frequently mistaken for a sarcomatous lesion due to the rapid growth, high cellularity, brisk mitotic activity, and locally infiltrative growth pattern. It may be not difficult to make a diagnosis of NF when the lesion arises in common locations and exhibits typical features. However, it may become a diagnostic challenging for pathologists when the lesion occurs in unusual clinical settings. In such instances, misdiagnosis will lead to inappropriate treatment. Therefore, familiar with the clinical and pathologic spectrum of NF is very important for pathologists. In this series, we embrace 272 cases of NF, which represents the largest one that has ever been reported. Our study demonstrates that NF occurred over a wide age range, from a male newborn to a 77-year-old man. Similar to previously reported series [2-6], NF is predominant in young to middle-aged adults between 20 and 50 years with a peak incidence in the fourth decade. The mean and median age in this series is both 36 years. It is rare in children younger than the age of 10 years (3.3%) or in adults older than 60 years (5.9%). There is a slight male predominance, with a male-to-female ratio of approximately 1.4:1. In keeping with previous studies, the vast majority of NF occurs in the subcutaneous tissue and underlying fascia, often presenting as a rapidly growing nodule. Approximately 5.9% of cases are intramuscular.
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
183
Fig. 4. Subcutaneous NF (A) and intramuscular NF (B) showing relatively well-defined borders. Nodular fasciitis showing extension into adjacent adipose tissue (C), skeletal muscle (D), parotid gland (E), or entrapping nerve fascicles (F).
However, this incidence may be underestimated in our series, as some of our consultation cases were not stated clearly as either subcutaneous or intramuscular at diagnosis. Mild pain and tenderness are noted in approximately 3 quarters of cases. The clinical duration is generally short with most cases being less than 1 to 2 months. However, cases with a longer preoperative interval (6 months to 1 year) were not uncommon [16]. In accordance with previous reports, NF arises predominantly in the upper extremities (34%), followed by head and neck region (24%) and trunk (21%). Less frequently, the lesion occurs in the lower extremity (14%), especially the thigh. Occurrence in the hands and feet is less
frequent with fewer than 20 cases being reported thus far [27-30]. This series added 9 additional cases of NF occurring in the acral regions, with 5 in the palm, 2 in the finger, and 1 each in the heel and plantar. It is worthy to note that acral NF may pose diagnostic pitfalls especially on cytologic specimen [31]. Occasional cases develop in the breast, mesentery, groin, and vulva (b8%) [9-11]. In this series, there are 9 cases (3.3%) in the breast, 8 cases (2.9%) in the groin, and 5 cases (1.8%) in the vulva, respectively. In these unusual sites, NF may be not considered in the diagnosis particularly those with unusually long clinical history [32]. Nodular fasciitis may also arise within the joints. Approximately 24 cases
Fig. 5. Typical NF composed of uniform bland spindle cells that arranged in short intersecting fascicles within a loose stroma accompanied by extravasated erythrocytes and scattered lymphocytes (A). Hypercellular (B), myxoid (C), and heavily hyalinized (D) forms of NF. Occasional cases containing combined areas (E). Stromal mucoid degeneration with formation of a broken fish net-like appearance (F). Small multinucleated giant cells ranging from scarce (G) to numerous (H).
184
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
Fig. 6. Spindled myofibroblasts showing diffuse staining with smooth muscle actin (A). CD68 highlighting intralesional histiocytes and small multinucleated giant cells (B).
have been described in the English literature [15-20]. Most developed in the knee with occasional occurrence in the hand, ankle, hip, and shoulder. Compared with conventional NF, intraarticular form had a longer preoperative history (median, 6 months). Most patients complained of joint pain with palpable mass. Few patients reported antecedent trauma. Besides the typical features, intraarticular NF was histologically characterized by the presence of extensive stromal hyalinization and peripheral hemosiderin deposition [16]. Another uncommon setting is intraneural presentation of NF. Up to present, only 6 cases of intraneural NF have been reported [21-25]. Involved nerves include ulnar nerve (2 cases), sciatic nerve (2 cases), obturator nerve (1 case), and median nerve (1 case). Patients often presented with symptoms related to nerve deficits, including numbness of the hand, decreased sensation in the fingers, and severe sciatica. This series added 2 additional cases with one arising within the median nerve and another one involving the lateral cord of the left brachial plexus, a site that has not been described thus far. Nodular fasciitis typically presents as a small nodule, although as large as 8 or 9 cm has been reported in the literature [33]. Approximately 87.5% of cases in the current series were smaller than 4 cm. The overall mean and median diameter was 2.3 and 2.0 cm, respectively. It has been noted that intramuscular lesions tend to be slightly larger than those found in the subcutaneous tissue. The diagnosis of NF larger than 4 cm should be based on the exclusion of any other types of fibrous tumors that may mimic NF. All cases manifest as a solitary lesion. Multiple NF should be diagnosed with caution [30]. Because of subcutaneous location, most patients had sonography only before surgery. On sonography, NF often appears as a hypoechoic mass [34]. Radiologic studies on NF are relatively scant and often of limited cases [34-36]. It is usually fascia based, oval in shape with homogeneous low to isodensity on CT scan. In cases with myxoid change, contrast-enhanced CT scan shows heterogeneous appearance with prominent peripheral nodular or rim-like enhancement [37]. On MRI, the lesion often appears as homogenous T1 signal isointense to adjacent skeletal muscles [37,38] and shows heterogeneous intermediate-tohigh signal with different enhancement patterns on T2- or STIRweighted sequences attributable to the variable components and cellularity on histology. Some cases may demonstrate distinct and discrete internal and central high T2-weighted signal areas with lower T2weighted signal intensity peripheral rim, which represents reticulated perilesional soft tissue edema on fluid-sensitive sequences [39]. Besides subcutaneous and intramuscular presentations, paracortical or paraarticular location is present in occasional cases. Irregular shape, relatively a large size with transcompartmental spread, intraarticular extension, cortical destruction with intraosseous involvement may lead to misdiagnosis of a sarcomatous lesion [40,41]. Currently, misdiagnosing NF as a high-grade sarcoma such as undifferentiated pleomorphic sarcoma or fibrosarcoma is considerably rare. However, misinterpreting NF as low-grade spindle cell neoplasms is not uncommon. In particular, intramuscular NF with focal extension
into adjacent skeletal muscles may be confused with a low-grade myofibroblastic sarcoma (LGMFS). In contrast to NF, LGMFS is more cellular and composed of long fascicles that infiltrate the muscles in a destructive pattern. Although pleophism is not a feature of LGMFS, the tumor exhibits at least mild nuclear atypia. Clinically, LGMFS is characterized by a high rate of local recurrence. Another neoplasm that may cause diagnostic confusion with NF is desmoid tumor, especially when dealing with biopsy specimens. Desmoid tumor is composed of elongated spindle cells arranged in sweeping bundles with frequent invasion of muscle tissues. Besides histologic difference, desmoid tumor can be distinguished from NF by nuclear staining for β-catenin. Another unexpected condition that may cause diagnostic pitfall is intraneural form of NF. As a matter of fact, 1 of our 2 intraneural NFs was initially misdiagnosed as malignant peripheral nerve sheath tumor. However, diffuse staining with smooth actin muscle and negative staining for S100 protein and SOX-10 denied the diagnosis of malignant peripheral nerve sheath tumor. Apart from the morphology and immunohistochemistry, detection of the recently identified USP6 gene rearrangement by molecular assay may serve as an important tool in the diagnosis and differential diagnosis of NF [42-44]. In conclusion, NF has a wide clinical and pathologic spectrum. Awareness of the rare occurrence of NF in unusual sites as well as in uncommon clinical settings is very important for both clinicians and pathologists. Although the radiologic appearance in NF is nonspecific, correlation with the clinical history and histologic features may help pathologists arrive at an accurate diagnosis.
References [1] Konwaller BE, Keasbey LE, Kaplan L. Subcutaneous pseudosarcomatous fibromatosis (fasciitis): report of 8 cases. Am J Clin Pathol 1955;25:241–52. [2] Price Jr EB, Silliphant WM, Shuman R. Nodular fasciitis: a clinicopathologic analysis of 65 cases. Am J Clin Pathol 1961;35:122–36. [3] Allen PW. Nodular fasciitis. Pathology 1972;4:9–26. [4] Meister P, Bückmann FW, Konrad E. Nodular fasciitis (analysis of 100 cases and review of the literature). Pathol Res Pract 1978;162:133–65. [5] Bernstein KE, Lattes R. Nodular (pseudosarcomatous) fasciitis, a nonrecurrent lesion: clinicopathologic study of 134 cases. Cancer 1982;49:1668–78. [6] Shimizu S, Hashimoto H, Enjoji M. Nodular fasciitis: an analysis of 250 patients. Pathology 1984;16:161–6. [7] Chen KT, Bauer V. Nodular fasciitis presenting as parotid tumor. Am J Otolaryngol 1987;8:179–81. [8] Gibson TC, Bishop JA, Thompson LD. Parotid gland nodular fasciitis: a clinicopathologic series of 12 cases with a review of 18 cases from the literature. Head Neck Pathol 2014 [[Epub ahead of print] PubMed PMID:25472697]. [9] Brown V, Carty NJ. A case of nodular fasciitis of the breast and review of the literature. Breast 2005;14:384–7. [10] Shiga M, Okamoto K, Matsumoto M, Maeda H, Dabanaka K, Uemura S, et al. Nodular fasciitis in the mesentery, a differential diagnosis of peritoneal carcinomatosis. World J Gastroenterol 2014;7(20):1361–4. [11] O'Connell JX, Young RH, Nielsen GP, Rosenberg AE, Bainbridge TC, Clement PB. Nodular fasciitis of the vulva: a study of six cases and literature review. Int J Gynecol Pathol 1997;16:117–23. [12] Goodlad JR, Fletcher CD. Intradermal variant of nodular “fasciitis”. Histopathology 1990;17:569–71.
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185 [13] Mazura JC, Matrai C, Spigland N, Brill PW, Kovanlikaya A. Intramuscular nodular fasciitis of the rectus abdominis muscle in an 11-year-old girl. Skeletal Radiol 2013;42: 147–50. [14] Patchefsky AS, Enzinger FM. Intravascular fasciitis: a report of 17 cases. Am J Surg Pathol 1981;5:29–36. [15] Yamamoto T, Nagira K, Noda M, Kurosaka M. Intra-articular nodular fasciitis. Arthroscopy 2001;17:E38. [16] Hornick JL, Fletcher CD. Intraarticular nodular fasciitis—a rare lesion: clinicopathologic analysis of a series. Am J Surg Pathol 2006;30:237–41. [17] Hagino T, Ochiai S, Sato E, Watanabe Y, Senga S, Kondo T, et al. Intraarticular nodular fasciitis causing limitation of knee extension: a case report. Knee 2010;17:424–7. [18] Harish S, Kuruvilla M, Alowami S, DeNardi F, Ghert M. Intra-articular nodular fasciitis of the shoulder: a case report and review of the literature. Skeletal Radiol 2011;40: 1383–6. [19] Stražar K, Drobnič M, Zupanc O, Jović V, Pižem J. Intraarticular nodular fasciitis of the hip. Arch Orthop Trauma Surg 2013;133:537–40. [20] Gans I, Morrison III MJ, Chikwava KR, Wells L. Intra-articular nodular fasciitis of the knee in a pediatric patient. Orthopedics 2014;37:e313–6. [21] Mahon JH, Folpe AW, Ferlic RJ. Intraneural nodular fasciitis: case report and literature review. J Hand Surg [Am] 2004;29:148–53. [22] Ikeda K, Hagiwara N, Funaki K, Tomita K, Sudo Y. Nodular fasciitis of the ulnar nerve at the palm. Scand J Plast Reconstr Surg Hand Surg 2005;39:249–51. [23] Parrett BM, Orgill DP, Marsee DK, Freedman AS, Raut CP. Novel presentation of intraneural nodular fasciitis of the sciatic nerve. J Peripher Nerv Syst 2007;12:61–3. [24] Kakutani K, Doita M, Nishida K, Akisue T, Maeno K, Zhang Z, et al. Intractable sciatica due to intraneural nodular fasciitis detected by positron emission tomography. Spine (Phila Pa 1976) 2010;35:E1137–40. [25] Yano K, Kazuki K, Yoneda M, Ikeda M, Fukushima H, Inoue T. Intraneural nodular fasciitis of the median nerve: case report and literature review. J Hand Surg [Am] 2011; 36:1347–51. [26] Erickson-Johnson MR, Chou MM, Evers BR, Roth CW, Seys AR, Jin L, et al. Nodular fasciitis: a novel model of transient neoplasia induced by MYH9-USP6 gene fusion. Lab Invest 2011;91:1427–33. [27] Singh R, Sharma AK. Nodular fasciitis of the thumb: a case report. Hand Surg 2004;9: 117–20. [28] Kijima H, Okada K, Ito H, Shimada Y, Nanjo H, Itoi E. Nodular fasciitis of the finger. Skeletal Radiol 2005;34:121–3. [29] Khan K, Farahani KD, Roberts EJ, D'Antoni AV, Cavazos J, Della Corte M. Pedal occurrence of nodular fasciitis: a case report. J Foot Ankle Surg 2012;51:241–5.
185
[30] Kotha GK, Bj V, Maryada VR, Jawalkar H. Multifocal nodular fasciitis of the hand and shoulder: case report. J Hand Surg [Am] 2014;39:2468–71. [31] Plaza JA, Mayerson J, Wakely Jr PE. Nodular fasciitis of the hand: a potential diagnostic pitfall in fine-needle aspiration cytopathology. Am J Clin Pathol 2005;123: 388–93. [32] Biedrzycki OJ, Singh N, Faruqi A. Nodular fasciitis of the vulva with an unusually long clinical history; the importance of making this unexpected diagnosis in such an unusual site. Histopathology 2007;51:547–50. [33] Nakagawa T, Sugimoto T, Komiyama S, Yamamoto T, Uemura T. Giant tumor formed by nodular fasciitis of the pharynx: a case report. Auris Nasus Larynx 1994;21: 196–9. [34] Khuu A, Yablon CM, Jacobson JA, Inyang A, Lucas DR, Biermann JS. Nodular fasciitis: characteristic imaging features on sonography and magnetic resonance imaging. J Ultrasound Med 2014;33:565–73. [35] Coyle J, White LM, Dickson B, Ferguson P, Wunder J, Naraghi A. MRI characteristics of nodular fasciitis of the musculoskeletal system. Skeletal Radiol 2013;42:975–82. [36] Meyer CA, Kransdorf MJ, Jelinek JS, Moser Jr RP. MR and CT appearance of nodular fasciitis. J Comput Assist Tomogr 1991;15:276–9. [37] Wang XL, De Schepper AM, Vanhoenacker F, De Raeve H, Gielen J, Aparisi F, et al. Nodular fasciitis: correlation of MRI findings and histopathology. Skeletal Radiol 2002;31:155–61. [38] Kim ST, Kim HJ, Park SW, Baek CH, Byun HS, Kim YM. Nodular fasciitis in the head and neck: CT and MR imaging findings. AJNR Am J Neuroradiol 2005;26:2617–23. [39] Dinauer PA, Brixey CJ, Moncur JT, Fanburg-Smith JC, Murphey MD. Pathologic and MR imaging features of benign fibrous soft-tissue tumors in adults. Radiographics 2007;27:173–87. [40] Hourani R, Taslakian B, Shabb NS, Nassar L, Hourani MH, Moukarbel R, et al. Fibroblastic and myofibroblastic tumors of the head and neck: comprehensive imagingbased review with pathologic correlation. Eur J Radiol 2015;84:250–60. [41] Le Corroller T, Kovacs TJ, Champsaur P. Nodular fasciitis with cortical involvement. Joint Bone Spine 2009;76:101–3. [42] Oliveira AM, Chou MM. USP6-induced neoplasms: the biologic spectrum of aneurysmal bone cyst and nodular fasciitis. Hum Pathol 2014;45:1–11. [43] Amary MF, Ye H, Berisha F, Tirabosco R, Presneau N, Flanagan AM. Detection of USP6 gene rearrangement in nodular fasciitis: an important diagnostic tool. Virchows Arch 2013;463:97–8. [44] Chen J, Ye X, Li Y, Wei C, Zheng Q, Zhong P, et al. Chromosomal translocation involving USP6 gene in nodular fasciitis. Zhonghua Bing Li Xue Za Zhi 2014;43:533–6 [Chinese].
Contents lists available at ScienceDirect
Annals of Diagnostic Pathology
Radiologic-Pathologic Correlation
Nodular fasciitis: a retrospective study of 272 cases from China with clinicopathologic and radiologic correlation Linhui Lu, MD a,c, I Weng Lao, MD a,c,1, Xiaohang Liu, MD b,c, Lin Yu, MD a,c, Jian Wang, MD a,c,⁎ a b c
Department of Pathology, Fudan University Shanghai Cancer Center, Shanghai, China Department of Radiology, Fudan University Shanghai Cancer Center, Shanghai, China Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China 200032
a r t i c l e
i n f o
Keywords: Nodular fasciitis Radiology Myofibroblast Immunohistochemistry
a b s t r a c t Our aim is to describe the largest series of nodular fasciitis (NF) with emphasis on the clinicopathologic and radiologic correlation. A total of 272 cases of NF were diagnosed between 2004 and 2014 at our institution. There were 160 males and 112 females with age ranging from newborn to 77 years (mean, 36 years). The upper extremity was the most common location (34%), followed by the head and neck region (24%), trunk (21%), and lower extremity (14%). By radiology, the lesion appeared as well-defined homogeneous mass with low or isodensity on computed tomography, homogenous hypointense or isointense on T1-weighted sequences, and heterogeneous intermediate-to-high signal on T2-weighted sequences. Although all cases were composed of short intersecting fascicles of uniform plump spindle cell, the cellularity and stromal components varied considerably between different cases. In intramuscular or deeply seated NFs, extension into adjacent skeletal muscles or structures was often noted. Immunohistochemically, all cases showed diffuse staining for smooth muscle actin and calponin, with consistent negativity for desmin, h-caldesmon, and β-catenin. Of patients with available followed up information, only 1 experienced local recurrence due to incomplete excision. Our comprehensive study further demonstrated that NF had a wide clinicopathologic spectrum. Correlation with the radiologic features may help pathologists in arriving at an accurate diagnosis. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Nodular fasciitis (NF) is a benign myofibroblastic proliferation that occurs predominantly in the subcutaneous tissue of young to middleaged adults [1]. It typically presents as a fast-growing nodule that usually reaches 2 to 3 cm in size within few weeks. The most common site is the upper extremities, followed by the trunk, head and neck region [2-6]. Occasionally, the lesion may arise in unusual locations including the salivary gland, breast, mesentery, and vulva [7-11]. In most instances, it develops in the subcutaneous tissue and underlying fascia and appears as a well-defined nodule. On rare occasions, it may also occur in the dermis or arises within the skeletal muscles, vessels, joints, and peripheral nerves [12-25]. Because of the rapid growth, high cellularity, remarkable mitotic activity, local infiltration into adjacent tissues, and unusual clinical settings in some instances, misdiagnosing NF as a sarcomatous lesion continues to be a challenge for pathologists, which may lead overtreatment to the patients. A multidisciplinary study combining the clinical, pathologic, and radiologic characteristics on NF
⁎ Corresponding author at: Department of Pathology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai 200032. Tel.: +86 21 64175590 88325; fax: +86 21 64046007. E-mail address: [email protected] (J. Wang). 1 Dr I Weng Lao contributed equally in this study and thus be considered as cofirst author. http://dx.doi.org/10.1016/j.anndiagpath.2015.03.013 1092-9134/© 2015 Elsevier Inc. All rights reserved.
is sparse. In this study, we undertake a retrospective review of the largest series of NF with emphasis on the clinical, pathologic, and radiologic correlation. 2. Materials and methods A retrospective study design was formulated, and institutional review board approval was obtained. Between January 2004 and December 2014, a total of 272 cases with NF were diagnosed at our institution. Special variants of NF such as cranial fasciitis, intravascular fasciitis, and ischemic fasciitis were excluded from the study. Clinical presentations, tumor site and size, radiologic appearance, and treatment information were obtained from the medical record, radiology and pathology reports, and discharge summary. The follow-up information was conducted via medical records or from the referring pathologists. Four-micrometer-thick hematoxylin and eosin–stained section was reexamined. Representative paraffin blocks or unstained slides containing tumor material from each case were selected for immunohistochemical study. The primary antibodies used in the study include smooth muscle actin (1A4, dilution 1:200; DAKO), desmin (D33, dilution 1:100; Dako), calponin (CALP, dilution 1:150; Maixin), CD10(SP67, ready to use; VENTANA), h-caldesmon (h-CD, dilution 1:300; DAKO), CD34 (QBEnd 10, dilution 1:100; DAKO), CD68 (KP1, dilution 1:600; Changdao), β-catenin (β-catenin1, dilution 1:200; DAKO), and cytokeratin (AE1/AE3, dilution 1:50; DAKO). Pretreatment was
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
carried out according to manufacturer's recommendation. Omission of primary antibody and substitution by nonspecific immunoglobins were used as negative controls. Appropriate positive controls were run concurrently for all antibodies tested.
181
surgery. In patients with follow-up information (ranging from 2 to 110 months), none of them experienced local recurrence except one after incomplete excision. 3.2. Imaging studies
3. Results 3.1. Clinical findings There were 160 males and 112 females with a ratio of 1.4:1. The patient's age at presentation ranged from newborn to 77 years. The newborn presented with a mass arising in the dorsal aspect of ulnar side of his left hand, whereas the oldest is a 77-year-old man who had a mass in his left shoulder. The mean and median ages were both 36 years. Approximately 65% of patients were in their third to fifth decades, whereas children (aged b10 years, 9 cases) and elderly patients (aged N60 years, 16 cases) accounted for 3.3% and 5.9%, respectively (Fig. 1). Clinically, most patients presented with a solitary subcutaneous nodule, which grew rapidly within 2 weeks or 1 month before surgical excision. However, patients with a preoperative duration of several months were not uncommon. One patient presented with 1-year history. Approximately three-fourths of patients were associated with slight pain or tenderness on palpation. Two patients with intraneural NF presented with symptoms of peripheral neuropathy. The patient with a tumor arising within the lateral cord of the left brachial plexus complained of left shoulder pain associated with numbness of the left thumb and index finger. Another patient with a tumor of the right median nerve complained of pain and numbness with decreased sensation of the right hand. History of antecedent trauma was not documented in all cases. With regard to the anatomic site, 92 cases (34%) were located in the upper extremities especially the forearm, 65 cases (24%) in the head and neck region, 56 cases (21%) in the trunk, 37 cases (14%) in the lower extremities especially the thigh, 9 cases (3.3%) in the breast, 8 cases (2.9%) in the groin, and 5 cases (1.8%) in the vulva. Of the upper extremities, 45 cases were located in the volar aspect of the forearms, followed by shoulder (n = 18), upper arm (n = 11), elbow (n = 8), hand (n = 7, 5 in the palm and back of hand, 2 in the finger), and axillary (n = 3). Of the head and neck region, tumor occurred in the neck (n = 36); cheek (n = 11); supraclavicular region (n = 5); external ear region (n = 4); orbit (n = 4); temple (n = 2); and forehead, eyelid, and oral cavity (1 case each). Of the trunk, 26 cases were located in the chest wall, followed by back (n = 20), waist (n = 5), and abdominal wall (n = 5). Of the lower extremities, 20 cases were located in the thigh, followed by hip (n = 9), knee (n = 4), leg (n = 2), and foot (n = 2, 1 each in the heel and plantar). All patients were treated by
Of 29 patients with recorded examinations, 15 patients had ultrasonography only before excision. Ultrasound scan usually showed a welldefined hypoechoic or isoechoic lesion situated in the subcutaneous tissues. Computed tomography (CT) or magnetic resonance imaging (MRI) was available in 14 cases. The lesion usually appeared as a fascia-based well-defined oval mass (Fig. 2A). A few intramuscular lesions were relatively large with ill-defined margins. On CT, it was low or isodense compared with adjacent muscles. In cases with cystic and mucoid degeneration, contrast-enhanced CT scan showed heterogeneous appearance with prominent peripheral rim-like enhancement in some cases (Fig. 2B). On MRI, it was homogenous hypointense or isointense on T1-weighted (T1WI) and heterogeneous intermediate to hyperintense on T2-weighted (T2WI) with enhancement after gadolinium administration (Fig. 2C-F). 3.3. Pathologic features All lesions were solitary. Apart from 1 intradermal case, 1 periosteal case, and 16 intramuscular cases (5.9%), all the remaining cases were subcutaneous. They were described as wellcircumscribed soft, rubbery-to-firm nodules or masses with glistening appearance on cut section (Fig. 3). The excised specimens measured from 0.5 to 7.0 cm in maximum diameter, with a mean and median size of 2.3 and 2.0 cm, respectively. Of note, the lesion in 238 cases (87.5%) was smaller than 4 cm. Those with a greatest dimension larger than 4 cm were mostly deeply seated or intramuscular lesions. At low-power magnification, most were well circumscribed but unencapsulated (Fig. 4A and B), whereas a minority of cases had poorly defined borders with infiltration into the surrounding adipose tissue, skeletal muscle, or parotid gland (Fig. 4C-E). Entrapped nerve fascicles were noted in 2 intraneural NFs (Fig. 4F). On high power, typical cases were composed of uniform bland spindle cells that arranged in short intersecting fascicles within a loose stroma with extravasated erythrocytes and scattered lymphocytes (Fig. 5A). However, the cellularity and the stroma components varied considerably between cases, ranging from hypercellular with less stromal material, highly myxoid with abundant mucoid matrix to heavily hyalinized with deposition of keloid-like collagen fibers (Fig. 5B-D). Cases with combined areas were not uncommon (Fig. 5E). Mucoid degeneration was a frequent feature, which was prominent in a few cases creating a broken fish net-like appearance (Fig. 5F). Approximately 10% of cases contained scattered multinucleated giant cells. These giant cells had more eosinophilic cytoplasm. Compared with the classic osteoclasts, these giant cells were relatively smaller and could contain only 2 to 3 nuclei. Their presence ranged from scarce that could be easily ignored to numerous (Fig. 5G and H). Generally, mitotic figures were not difficult to find (ranging from 1 to 10/10 high-power field), but cytologic pleomorphism and nuclear atypia were absent. 3.4. Immunohistochemical study
Fig. 1. Age and sex distribution in 272 patients with NF.
The spindle cells showed diffuse expression of smooth muscle actin (Fig. 6A). They were also positive for calponin, muscle specific actin, and CD10. Intralesional histiocytes and small multinucleated giant cells were positive for CD68 (Fig. 6B). Other markers including desmin, h-caldesmon, β-catenin AE1/AE3, CD34, and S-100 protein were all negative.
182
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
Fig. 2. A fascia-based oval mass in the occipital region with heterogeneous intermediate-to-high signal on T2-weighted sequences (A). Cystic and mucoid degeneration with prominent peripheral rim-like enhancement on contrast-enhanced CT scan in an intramuscular NF (B). Nodular fasciitis of the left brachial plexus (C and D) and left fourth finger (E and F) showing homogenous T1 signal isointense to adjacent skeletal muscles and heterogeneous intermediate-to-high signal on T2-weighted sequences.
4. Discussion Nodular fasciitis is a benign self-limited process, which was originally reported by Konwaller et al [1] in 1955. Although a history of antecedent trauma has been documented in a small proportion of cases, the
Fig. 3. Intramuscular NF appeared as a well-circumscribed firm nodule with glistening appearance on cut section.
etiology remains uncertain. For a long time, it has been considered as a reactive lesion. However, recent molecular cytogenetic study revealed a recurrent MYH9-USP6 fusion gene, indicating a clonal neoplastic disorder of NF [26]. Nodular fasciitis is also well known as pseudosarcomatous fasciitis because it was frequently mistaken for a sarcomatous lesion due to the rapid growth, high cellularity, brisk mitotic activity, and locally infiltrative growth pattern. It may be not difficult to make a diagnosis of NF when the lesion arises in common locations and exhibits typical features. However, it may become a diagnostic challenging for pathologists when the lesion occurs in unusual clinical settings. In such instances, misdiagnosis will lead to inappropriate treatment. Therefore, familiar with the clinical and pathologic spectrum of NF is very important for pathologists. In this series, we embrace 272 cases of NF, which represents the largest one that has ever been reported. Our study demonstrates that NF occurred over a wide age range, from a male newborn to a 77-year-old man. Similar to previously reported series [2-6], NF is predominant in young to middle-aged adults between 20 and 50 years with a peak incidence in the fourth decade. The mean and median age in this series is both 36 years. It is rare in children younger than the age of 10 years (3.3%) or in adults older than 60 years (5.9%). There is a slight male predominance, with a male-to-female ratio of approximately 1.4:1. In keeping with previous studies, the vast majority of NF occurs in the subcutaneous tissue and underlying fascia, often presenting as a rapidly growing nodule. Approximately 5.9% of cases are intramuscular.
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
183
Fig. 4. Subcutaneous NF (A) and intramuscular NF (B) showing relatively well-defined borders. Nodular fasciitis showing extension into adjacent adipose tissue (C), skeletal muscle (D), parotid gland (E), or entrapping nerve fascicles (F).
However, this incidence may be underestimated in our series, as some of our consultation cases were not stated clearly as either subcutaneous or intramuscular at diagnosis. Mild pain and tenderness are noted in approximately 3 quarters of cases. The clinical duration is generally short with most cases being less than 1 to 2 months. However, cases with a longer preoperative interval (6 months to 1 year) were not uncommon [16]. In accordance with previous reports, NF arises predominantly in the upper extremities (34%), followed by head and neck region (24%) and trunk (21%). Less frequently, the lesion occurs in the lower extremity (14%), especially the thigh. Occurrence in the hands and feet is less
frequent with fewer than 20 cases being reported thus far [27-30]. This series added 9 additional cases of NF occurring in the acral regions, with 5 in the palm, 2 in the finger, and 1 each in the heel and plantar. It is worthy to note that acral NF may pose diagnostic pitfalls especially on cytologic specimen [31]. Occasional cases develop in the breast, mesentery, groin, and vulva (b8%) [9-11]. In this series, there are 9 cases (3.3%) in the breast, 8 cases (2.9%) in the groin, and 5 cases (1.8%) in the vulva, respectively. In these unusual sites, NF may be not considered in the diagnosis particularly those with unusually long clinical history [32]. Nodular fasciitis may also arise within the joints. Approximately 24 cases
Fig. 5. Typical NF composed of uniform bland spindle cells that arranged in short intersecting fascicles within a loose stroma accompanied by extravasated erythrocytes and scattered lymphocytes (A). Hypercellular (B), myxoid (C), and heavily hyalinized (D) forms of NF. Occasional cases containing combined areas (E). Stromal mucoid degeneration with formation of a broken fish net-like appearance (F). Small multinucleated giant cells ranging from scarce (G) to numerous (H).
184
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185
Fig. 6. Spindled myofibroblasts showing diffuse staining with smooth muscle actin (A). CD68 highlighting intralesional histiocytes and small multinucleated giant cells (B).
have been described in the English literature [15-20]. Most developed in the knee with occasional occurrence in the hand, ankle, hip, and shoulder. Compared with conventional NF, intraarticular form had a longer preoperative history (median, 6 months). Most patients complained of joint pain with palpable mass. Few patients reported antecedent trauma. Besides the typical features, intraarticular NF was histologically characterized by the presence of extensive stromal hyalinization and peripheral hemosiderin deposition [16]. Another uncommon setting is intraneural presentation of NF. Up to present, only 6 cases of intraneural NF have been reported [21-25]. Involved nerves include ulnar nerve (2 cases), sciatic nerve (2 cases), obturator nerve (1 case), and median nerve (1 case). Patients often presented with symptoms related to nerve deficits, including numbness of the hand, decreased sensation in the fingers, and severe sciatica. This series added 2 additional cases with one arising within the median nerve and another one involving the lateral cord of the left brachial plexus, a site that has not been described thus far. Nodular fasciitis typically presents as a small nodule, although as large as 8 or 9 cm has been reported in the literature [33]. Approximately 87.5% of cases in the current series were smaller than 4 cm. The overall mean and median diameter was 2.3 and 2.0 cm, respectively. It has been noted that intramuscular lesions tend to be slightly larger than those found in the subcutaneous tissue. The diagnosis of NF larger than 4 cm should be based on the exclusion of any other types of fibrous tumors that may mimic NF. All cases manifest as a solitary lesion. Multiple NF should be diagnosed with caution [30]. Because of subcutaneous location, most patients had sonography only before surgery. On sonography, NF often appears as a hypoechoic mass [34]. Radiologic studies on NF are relatively scant and often of limited cases [34-36]. It is usually fascia based, oval in shape with homogeneous low to isodensity on CT scan. In cases with myxoid change, contrast-enhanced CT scan shows heterogeneous appearance with prominent peripheral nodular or rim-like enhancement [37]. On MRI, the lesion often appears as homogenous T1 signal isointense to adjacent skeletal muscles [37,38] and shows heterogeneous intermediate-tohigh signal with different enhancement patterns on T2- or STIRweighted sequences attributable to the variable components and cellularity on histology. Some cases may demonstrate distinct and discrete internal and central high T2-weighted signal areas with lower T2weighted signal intensity peripheral rim, which represents reticulated perilesional soft tissue edema on fluid-sensitive sequences [39]. Besides subcutaneous and intramuscular presentations, paracortical or paraarticular location is present in occasional cases. Irregular shape, relatively a large size with transcompartmental spread, intraarticular extension, cortical destruction with intraosseous involvement may lead to misdiagnosis of a sarcomatous lesion [40,41]. Currently, misdiagnosing NF as a high-grade sarcoma such as undifferentiated pleomorphic sarcoma or fibrosarcoma is considerably rare. However, misinterpreting NF as low-grade spindle cell neoplasms is not uncommon. In particular, intramuscular NF with focal extension
into adjacent skeletal muscles may be confused with a low-grade myofibroblastic sarcoma (LGMFS). In contrast to NF, LGMFS is more cellular and composed of long fascicles that infiltrate the muscles in a destructive pattern. Although pleophism is not a feature of LGMFS, the tumor exhibits at least mild nuclear atypia. Clinically, LGMFS is characterized by a high rate of local recurrence. Another neoplasm that may cause diagnostic confusion with NF is desmoid tumor, especially when dealing with biopsy specimens. Desmoid tumor is composed of elongated spindle cells arranged in sweeping bundles with frequent invasion of muscle tissues. Besides histologic difference, desmoid tumor can be distinguished from NF by nuclear staining for β-catenin. Another unexpected condition that may cause diagnostic pitfall is intraneural form of NF. As a matter of fact, 1 of our 2 intraneural NFs was initially misdiagnosed as malignant peripheral nerve sheath tumor. However, diffuse staining with smooth actin muscle and negative staining for S100 protein and SOX-10 denied the diagnosis of malignant peripheral nerve sheath tumor. Apart from the morphology and immunohistochemistry, detection of the recently identified USP6 gene rearrangement by molecular assay may serve as an important tool in the diagnosis and differential diagnosis of NF [42-44]. In conclusion, NF has a wide clinical and pathologic spectrum. Awareness of the rare occurrence of NF in unusual sites as well as in uncommon clinical settings is very important for both clinicians and pathologists. Although the radiologic appearance in NF is nonspecific, correlation with the clinical history and histologic features may help pathologists arrive at an accurate diagnosis.
References [1] Konwaller BE, Keasbey LE, Kaplan L. Subcutaneous pseudosarcomatous fibromatosis (fasciitis): report of 8 cases. Am J Clin Pathol 1955;25:241–52. [2] Price Jr EB, Silliphant WM, Shuman R. Nodular fasciitis: a clinicopathologic analysis of 65 cases. Am J Clin Pathol 1961;35:122–36. [3] Allen PW. Nodular fasciitis. Pathology 1972;4:9–26. [4] Meister P, Bückmann FW, Konrad E. Nodular fasciitis (analysis of 100 cases and review of the literature). Pathol Res Pract 1978;162:133–65. [5] Bernstein KE, Lattes R. Nodular (pseudosarcomatous) fasciitis, a nonrecurrent lesion: clinicopathologic study of 134 cases. Cancer 1982;49:1668–78. [6] Shimizu S, Hashimoto H, Enjoji M. Nodular fasciitis: an analysis of 250 patients. Pathology 1984;16:161–6. [7] Chen KT, Bauer V. Nodular fasciitis presenting as parotid tumor. Am J Otolaryngol 1987;8:179–81. [8] Gibson TC, Bishop JA, Thompson LD. Parotid gland nodular fasciitis: a clinicopathologic series of 12 cases with a review of 18 cases from the literature. Head Neck Pathol 2014 [[Epub ahead of print] PubMed PMID:25472697]. [9] Brown V, Carty NJ. A case of nodular fasciitis of the breast and review of the literature. Breast 2005;14:384–7. [10] Shiga M, Okamoto K, Matsumoto M, Maeda H, Dabanaka K, Uemura S, et al. Nodular fasciitis in the mesentery, a differential diagnosis of peritoneal carcinomatosis. World J Gastroenterol 2014;7(20):1361–4. [11] O'Connell JX, Young RH, Nielsen GP, Rosenberg AE, Bainbridge TC, Clement PB. Nodular fasciitis of the vulva: a study of six cases and literature review. Int J Gynecol Pathol 1997;16:117–23. [12] Goodlad JR, Fletcher CD. Intradermal variant of nodular “fasciitis”. Histopathology 1990;17:569–71.
L. Lu et al. / Annals of Diagnostic Pathology 19 (2015) 180–185 [13] Mazura JC, Matrai C, Spigland N, Brill PW, Kovanlikaya A. Intramuscular nodular fasciitis of the rectus abdominis muscle in an 11-year-old girl. Skeletal Radiol 2013;42: 147–50. [14] Patchefsky AS, Enzinger FM. Intravascular fasciitis: a report of 17 cases. Am J Surg Pathol 1981;5:29–36. [15] Yamamoto T, Nagira K, Noda M, Kurosaka M. Intra-articular nodular fasciitis. Arthroscopy 2001;17:E38. [16] Hornick JL, Fletcher CD. Intraarticular nodular fasciitis—a rare lesion: clinicopathologic analysis of a series. Am J Surg Pathol 2006;30:237–41. [17] Hagino T, Ochiai S, Sato E, Watanabe Y, Senga S, Kondo T, et al. Intraarticular nodular fasciitis causing limitation of knee extension: a case report. Knee 2010;17:424–7. [18] Harish S, Kuruvilla M, Alowami S, DeNardi F, Ghert M. Intra-articular nodular fasciitis of the shoulder: a case report and review of the literature. Skeletal Radiol 2011;40: 1383–6. [19] Stražar K, Drobnič M, Zupanc O, Jović V, Pižem J. Intraarticular nodular fasciitis of the hip. Arch Orthop Trauma Surg 2013;133:537–40. [20] Gans I, Morrison III MJ, Chikwava KR, Wells L. Intra-articular nodular fasciitis of the knee in a pediatric patient. Orthopedics 2014;37:e313–6. [21] Mahon JH, Folpe AW, Ferlic RJ. Intraneural nodular fasciitis: case report and literature review. J Hand Surg [Am] 2004;29:148–53. [22] Ikeda K, Hagiwara N, Funaki K, Tomita K, Sudo Y. Nodular fasciitis of the ulnar nerve at the palm. Scand J Plast Reconstr Surg Hand Surg 2005;39:249–51. [23] Parrett BM, Orgill DP, Marsee DK, Freedman AS, Raut CP. Novel presentation of intraneural nodular fasciitis of the sciatic nerve. J Peripher Nerv Syst 2007;12:61–3. [24] Kakutani K, Doita M, Nishida K, Akisue T, Maeno K, Zhang Z, et al. Intractable sciatica due to intraneural nodular fasciitis detected by positron emission tomography. Spine (Phila Pa 1976) 2010;35:E1137–40. [25] Yano K, Kazuki K, Yoneda M, Ikeda M, Fukushima H, Inoue T. Intraneural nodular fasciitis of the median nerve: case report and literature review. J Hand Surg [Am] 2011; 36:1347–51. [26] Erickson-Johnson MR, Chou MM, Evers BR, Roth CW, Seys AR, Jin L, et al. Nodular fasciitis: a novel model of transient neoplasia induced by MYH9-USP6 gene fusion. Lab Invest 2011;91:1427–33. [27] Singh R, Sharma AK. Nodular fasciitis of the thumb: a case report. Hand Surg 2004;9: 117–20. [28] Kijima H, Okada K, Ito H, Shimada Y, Nanjo H, Itoi E. Nodular fasciitis of the finger. Skeletal Radiol 2005;34:121–3. [29] Khan K, Farahani KD, Roberts EJ, D'Antoni AV, Cavazos J, Della Corte M. Pedal occurrence of nodular fasciitis: a case report. J Foot Ankle Surg 2012;51:241–5.
185
[30] Kotha GK, Bj V, Maryada VR, Jawalkar H. Multifocal nodular fasciitis of the hand and shoulder: case report. J Hand Surg [Am] 2014;39:2468–71. [31] Plaza JA, Mayerson J, Wakely Jr PE. Nodular fasciitis of the hand: a potential diagnostic pitfall in fine-needle aspiration cytopathology. Am J Clin Pathol 2005;123: 388–93. [32] Biedrzycki OJ, Singh N, Faruqi A. Nodular fasciitis of the vulva with an unusually long clinical history; the importance of making this unexpected diagnosis in such an unusual site. Histopathology 2007;51:547–50. [33] Nakagawa T, Sugimoto T, Komiyama S, Yamamoto T, Uemura T. Giant tumor formed by nodular fasciitis of the pharynx: a case report. Auris Nasus Larynx 1994;21: 196–9. [34] Khuu A, Yablon CM, Jacobson JA, Inyang A, Lucas DR, Biermann JS. Nodular fasciitis: characteristic imaging features on sonography and magnetic resonance imaging. J Ultrasound Med 2014;33:565–73. [35] Coyle J, White LM, Dickson B, Ferguson P, Wunder J, Naraghi A. MRI characteristics of nodular fasciitis of the musculoskeletal system. Skeletal Radiol 2013;42:975–82. [36] Meyer CA, Kransdorf MJ, Jelinek JS, Moser Jr RP. MR and CT appearance of nodular fasciitis. J Comput Assist Tomogr 1991;15:276–9. [37] Wang XL, De Schepper AM, Vanhoenacker F, De Raeve H, Gielen J, Aparisi F, et al. Nodular fasciitis: correlation of MRI findings and histopathology. Skeletal Radiol 2002;31:155–61. [38] Kim ST, Kim HJ, Park SW, Baek CH, Byun HS, Kim YM. Nodular fasciitis in the head and neck: CT and MR imaging findings. AJNR Am J Neuroradiol 2005;26:2617–23. [39] Dinauer PA, Brixey CJ, Moncur JT, Fanburg-Smith JC, Murphey MD. Pathologic and MR imaging features of benign fibrous soft-tissue tumors in adults. Radiographics 2007;27:173–87. [40] Hourani R, Taslakian B, Shabb NS, Nassar L, Hourani MH, Moukarbel R, et al. Fibroblastic and myofibroblastic tumors of the head and neck: comprehensive imagingbased review with pathologic correlation. Eur J Radiol 2015;84:250–60. [41] Le Corroller T, Kovacs TJ, Champsaur P. Nodular fasciitis with cortical involvement. Joint Bone Spine 2009;76:101–3. [42] Oliveira AM, Chou MM. USP6-induced neoplasms: the biologic spectrum of aneurysmal bone cyst and nodular fasciitis. Hum Pathol 2014;45:1–11. [43] Amary MF, Ye H, Berisha F, Tirabosco R, Presneau N, Flanagan AM. Detection of USP6 gene rearrangement in nodular fasciitis: an important diagnostic tool. Virchows Arch 2013;463:97–8. [44] Chen J, Ye X, Li Y, Wei C, Zheng Q, Zhong P, et al. Chromosomal translocation involving USP6 gene in nodular fasciitis. Zhonghua Bing Li Xue Za Zhi 2014;43:533–6 [Chinese].