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| Year : 2009 | Volume
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| Issue : 1 | Page : 29-33 |
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| Morphological spectrum of peripheral nerve sheath tumors: A series of 126 cases |
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Sushma Kashinath Gabhane1, Mrunamayi Nishikant Kotwal2, Sudhakar K Bobhate2
1 Department of Pathology, Mahatma Gandhi Institute of Medical Sciences, Sevagram, Wardha, India
2 Government Medical College, Nagpur, India
Click here for correspondence address and email
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 Abstract | | |
By convention, soft tissue tumors include the peripheral nerve sheath tumor (PNST) although they arise from neuroectoderm. PNSTs display a wide spectrum of morphology and biological behavior. Malignant transformation in benign tumors, especially neurofibroma, is an acknowledged phenomenon.This article describes clinico-pathological features of 126 PNSTs with their morphological variants and those associated with neurofibromatosis 1 (NF1) encountered in a single center over a 6-year period. Benign PNSTs were more common [118 (93.65%)] when compared with their malignant counterparts [8 (6.34%)]. Histological variants including plexiform schwannomas and diffuse, plexiform and pigmented forms of neurofibromas, though rare, were observed. Eleven (8.73%) patients with NF1 showed a strong association with plexiform neurofibroma. A malignant transformation in pre-existing neurofibroma was seen in 1 patient with NF1. This series highlights the clinico-pathological spectrum of PNSTs, their morphological variants and the incidence of associated NF1. The importance of detecting plexiform variants lies in their vastly different prognostic implications particularly when occurring in the setting of NF1 Keywords: MPNST, neurofibroma, neurofibromatosis 1, peripheral nerve sheath tumor, schwannoma
How to cite this article:
Gabhane SK, Kotwal MN, Bobhate SK. Morphological spectrum of peripheral nerve sheath tumors: A series of 126 cases. Indian J Pathol Microbiol 2009;52:29-33 |
How to cite this URL:
Gabhane SK, Kotwal MN, Bobhate SK. Morphological spectrum of peripheral nerve sheath tumors: A series of 126 cases. Indian J Pathol Microbiol [serial online] 2009 [cited 2023 May 29];52:29-33. Available from: https://www.ijpmonline.org/text.asp?2009/52/1/29/44958 |
| Introduction | |  |
Peripheral nerve sheath tumors (PNSTs) are the neoplasms that most often arise in anatomically discernible peripheral nerves and have a wide spectrum of histological features. The two most common benign PNSTs include schwannoma and neurofibroma, but from both a clinical and histological perspective, the most enigmatic is the malignant PNST. [1]
A review of published literature shows a few articles enumerating the incidence of the entire spectrum of benign and malignant PNSTs including their variants from a single center. Most studies describe specific histological variants of benign tumors or the malignant peripheral nerve sheath tumour (MPNST). Hruban, et al ., [1] Ducatman, et al ., [2] and Kar, et al . [3] have studied malignant PNSTs clinicopathologically in relation to their treatment outcome and prognosis. White, et al . [4] have discussed exclusively the cellular variant of schwannoma. Erlandson, et al . [5] described the electron microscopic features of 43 PNSTs in search of histogenesis. Mohan, et al . [6] have described some uncommon variants of PNSTs in a short series.
This article is a comprehensive clinicopathological study of a large series of PNSTs, with special emphasis on their morphological variants and those associated with neurofibromatosis 1 with stress on their prognostic significance.
| Materials and Methods | | |
All PNSTs encountered over a period of 6 years (1999-2004) in the Department of Pathology of a medical college were retrieved from archives and clinical and demographic details obtained from medical records were reviewed with special attention to features of neurofibromatosis, neurodeficit and deformities. Tumor location, size, presence of necrosis, mitotic activity and the method of treatment were studied in relation to outcome in cases of MPNSTs.
In all cases, H and E stained sections were studied. Special stains such as Masson Fontana and Toludine blue were employed, if indicated. The tumors were categorized and classified in accordance with the classification of soft tissue tumors proposed by Weiss and Goldblum.[7] For a diagnosis of MPNST, we used the following criteria (1) a tumor originating from a nerve demonstrated either during surgery or by gross examination or on microscopic examination or (2) a tumor arising from a pre-existing neurofibroma. [2] The criteria laid down by the National Institute of Health in Consensus Development Conference Statement were used for the diagnosis of NF1. [8]
| Results | | |
PNSTs accounted for 1.63% of all tumors diagnosed during a 6-year period (1999-2004) in the surgical pathology department of our institute. Benign PNSTs were more common than MPNSTs [Table 1]. The most common presenting symptoms in decreasing order of frequency were: mass lesion (100%), pain (38.15%) and neurological deficit (7.93%). Benign PNSTs involved the head and neck most commonly (39.83%) followed by upper extremities (27.11%), lower extremities (18.64%) and trunk (11.86%). In contrast, MPNSTs involved lower extremities (62.50%) followed by upper extremities (25%) and trunk (12.50%). The nerve of origin could be identified (grossly, microscopically, or radiologically) in 40.47% of the cases. The brachial plexus was the most common nerve plexus involved in 25.49% of cases followed by the ulnar nerve and the sciatic nerve in 11.76% of cases each.
Schwannoma
These tumors were encapsulated, grey-white and firm with degenerative changes in almost all tumors, the most common being cystic change (85.18%), hyalinization (72.22%), necrosis (59.25%) and myxoid change (24.07%). Verocay bodies were seen in 70.37% of the tumors. Four morphological variants were identified, as shown in [Table 2].
Cellular schwannomas were encapsulated, firm and mostly solid tumors composed predominantly of Antoni A areas (without Verocay bodies) with intersecting fascicles and whorls or herringbone pattern. Plexiform schwannomas exhibited multinodular architecture with marked cellularity dominated by Antoni A pattern with plenty of Verocay bodies. In contrast to both of these variants, ancient schwannomas showed marked degenerative changes and very few Antoni A areas. Some ancient schwannomas showed hyperlobated, irregular, atypical looking nuclei of Schwann cells.
Neurofibroma
These tumors were grey-white, well-defined, circumscribed, or lobulated masses, histologically showing interlacing bundles of spindle or stellate cells with wavy, buckled, or serpentine nuclei embedded in a loose fibromyxoid matrix. The presence of capsule (14%) and myxoid changes (18%) were rarely found. Three neurofibromas (5.55%) showed the presence of melanin pigment [Table 3].
The gross and microscopic appearance of plexiform and diffuse neurofibroma was quite characteristic. On gross examination, plexiform neurofibroma showed enlarged, tortuous nerves having a fusiform and nodular appearance resembling a 'bag of worms'. Histologically, the tumor showed tortuous masses of expanded nerve branches with a prominent increase in the endoneurial myxomatous matrix separating axons and disorderly proliferation of fusiform Schwann cells and fibroblasts as well as perineurial fibrous thickening [Figure 1] and [Figure 2].
Diffuse neurofibromas were soft, raised, plaque-like masses that had a glistening, gelatinous, pink-grey nodular appearance with the replacement of normal subcutaneous tissue and dermis. Microscopically, they showed characteristic laminated bodies resembling Wagner-Meissner tactile corpuscles in the background of short fusiform neoplastic Schwann cells and fine fibrillary collaginous matrix [Figure 3].
MPNST
A total of 8 cases (6.34%) of malignant PNSTs were seen. The size of these tumors ranged from 5.5 x 3.1 x 2.6 cm to 20 x 15.5 x 15.2 cm (the mean was 11.7 cm). Grossly, capsule was identified in 37.50% of the tumors with most of the tumors being firm and fleshy. Degenerative changes like hemorrhage (75%), necrosis (75%) and cystic changes (50%) were also seen. Rudimentary tactoid differentiation was present in one tumor (12.5%). Heterologous elements e.g., osteoid and cartilaginous metaplasia were seen in 25% of the tumors. Metastasis to the lungs and pleura were seen in two patients (25%). A rare feature noted was hyalinized nodule in one case [Figure 4] and [Figure 5].
Neurofibromatosis 1
A total of 11 cases of NF1 were observed in the present study with a mean age of 8.5 years at the time of the first diagnosis. A slight female preponderance was noted with a M:F ratio of 1:1.75. The presence of multiple neurofibromas and cafe au lait spots were the two most common criteria fulfilled by all the patients. Apart from the usual type of neurofibroma, variants were also observed: plexiform neurofibroma (27.27%) and diffuse neurofibroma (18.18%). MPNSTs were seen in two cases (18.18%), one of them showing malignant transformation in pre-existing neurofibroma.
| Discussion | | |
Neurofibroma and schwannoma are common benign PNSTs that occur as isolated sporadic lesions, but have their major clinical impact on the neurocutaneous diseases NF1 and NF2. MPNSTs may originate de novo or in a neurofibroma or a plexiform neurofibroma associated with neurofibromatosis, but malignant transformation of a schwannoma is exceptionally rare. [9],[10] The incidence of MPNSTs in the general population is 0.001%; however, it increases to 4-4.6% in patients with neurofibromatosis 1. [2],[6],[9]
The Schwann cell was regarded by most investigators as the cell of origin for both neurofibroma and schwannoma. Erlandson, et al. [5] in their electron microscopic study of 43 cases of PNSTs confirmed that schwannoma is principally composed of cells that resemble differentiated Schwann cell but neurofibroma is composed of an admixture of Schwann cells, perineurial cells, fibroblasts and entrapped axons. Since the origin of MPNSTs is less clear and the malignant change in schwannoma is a rare event, other authors proposed MPNST as a better designation than malignant schwannoma. [5],[11],[12]
The frequent sites of involvement of benign PNSTs are the head and neck, followed by the flexor aspects of the upper extremities.[6] MPNSTs, in contrast to benign PNSTs, are more common in the proximal portions of the limbs and trunk than in the head and neck region. [1],[2],[6] In benign tumors, schwannomas occur in people 20 to 50 years of age, in contrast to neurofibromas that occur a decade earlier i.e., 20 to 30 years.
Schwannomas are often asymptomatic, moveable and typically attached to the nerve. The spinal roots and the cervical, sympathetic and vagus nerves are commonly involved. The diagnosis of the usual type of schwannoma is easy but diagnosis of variants like cellular, ancient and plexiform schwannomas is sometimes difficult. [8],[9]
Cellular schwannoma with its herringbone pattern may be mistaken for MPNST, fibrosarcoma, or leiomyosarcoma. However, increased cellularity in this tumor is disproportionately high compared with the levels of mitosis and atypia. Encapsulation, perivascular hyalinization and strong, diffuse reactivity for S-100 protein should suggest a benign diagnosis. [4],[9],[10],[13]
Plexiform schwannoma is a rare nodular variant except for its multinodular or plexiform architecture and has the same histological features as the usual schwannoma but with marked cellularity dominated by the Antoni type A pattern. [9],[10],[13] Ancient schwannoma sometimes may give a malignant look grossly because of large size, the presence of marked degenerative changes such as cystic changes or hemorrhage. Microscopically, they may show irregular, hyperlobated and hyperchromatic nuclei of Schwann cells but the presence of Verocay bodies and the absence of mitoses rule out the malignant diagnosis. [9],[10],[13]
In our series, we observed five cases each of cellular and ancient variants and three cases of the plexiform variant of schwannomas.
Solitary neurofibroma is far more common than the inherited counterpart associated with NF1. When associated with NF1, neurofibromas are multiple or segmental in distribution, deeply located and more likely to undergo a malignant transformation.[9],[10]
In our series, apart from 37 usual types of neurofibromas, we observed three pigmented neurofibromas, six plexiform neurofibromas showing a strong association with neurofibromatosis 1 (in 50% of the cases) and 11 diffuse neurofibromas; two that were associated with NF1 (18.18%). However, malignant changes were not noted in any of these variants.
Pigmented neurofibroma is a usual type of solitary neurofibroma that shows the presence of melanin pigment in the cytoplasm of Schwann cells. The proposed theories for the presence of melanin in this nerve sheath tumor are either phagocytosis by Schwann cells or proliferation of two different cell types (Schwann cell and melanocytes). Embryologically, melanocytes and peripheral nerve elements have a common origin from the neural crest stem cells. These cells at their genomic level retain their capacity to produce pigment, which explains the presence of melanin in these nerve sheath tumors. [1],[6],[12]
Plexiform neurofibroma (PNF) should be distinguished from plexiform schwannoma and mucosal neuroma. PNF hypocellular has a prominent myxoid matrix and contains a disorderly array of Schwann cells, fibroblasts and axons with wiry cytoplasmic processes within and often outside the perineurium. Mucosal neuromas consist of disorganized and tortuous nerve fibers surrounded by thickened perineurium without any loose myxoid stroma. Malignant transformations occur in 10-15% of PNF cases in NF1, most often in large, deeply and centrally located tumors with a peak incidence in the third decade of life. [9],[10],[13]
Diffuse neurofibroma (D-NF) is distinguished from PNF by its highly infiltrative growth pattern, rounded to slightly fusiform cells that are uniformly distributed within a delicate collaginous background and sheets of laminated bodies resembling Wagner- Meissner corpuscles. These features distinguish D-NF from tumors with a similar infiltrative pattern, namely, spindle cell lipoma and dermatofibrosarcoma protuberans. [9],[10],[13]
Unlike PNF, which is associated with NF1 in most cases, only 10% of DNF cases have this association. [9],[10],[13]
MPNST is the principal malignancy of the peripheral nerves and usually involves the major nerve trunks of the proximal extremities, neck and trunk. [14] MPNST developing in patients with NF1 behaves more aggressively than de novo tumors and metastasizes within 2 years of diagnosis. [1],[2] A 78% recurrence rate and 63% metastatic rate (most commonly to the lungs, liver, bone and subcutaneous tissue) have been reported. [14] Saleh, et al. [14] reported a case of MPNST metastatic to the lungs on fine needle aspiration cytology, which was further confirmed by histology and positivity for S-100 protein.
In our series, we observed that MPNSTs predominantly involved lower extremities; two cases were associated with NF 1. We also reported two cases of MPNST metastatic to the lungs and pleura on fine needle aspiration cytology (FNAC) and confirmed by biopsy.
The differential diagnosis of MPNST includes fibrosarcoma, malignant fibrous histiocytoma, leiomyosarcoma, monophasic synovial sarcoma, lesions with striated muscle differentiation and rhabdomyosarcoma. In the absence of proved neural origin, a contagious neurofibroma should be sought. In addition, certain morphologic features, such as wavy cytoplasmic and nuclear configuration, cellular palisading, geographic areas of necrosis and the presence of heterogeneous elements strongly suggest a Schwann cell derivation. [2],[9]
Neurofibromatosis type 1, also known as von Recklinghausen's disease, is a multifocal neurocutaneous disease affecting 1 in 3,000 people. It is inherited as an autosomal dominant disease and the genetic defect has been localized to a gene on chromosome 17. [8],[9],[11],[15]
MPNST is often associated with von Recklinghausen's disease; incidences range from 2-29%. It is a fact that 3-6% of von Recklinghausen's neurofibromas transform spontaneously (without irradiation) to malignant nerve sheath tumors and usually before the fourth decade of life. [2]
Patients with NF1 are more susceptible to the oncogenic effect of radiation than patients without this genetic defect. Perhaps this is why patients with neurofibromatosis type 1 have a high risk of developing neoplasia such as neuroblstoma, ganglioneuroma, nephroblastoma, leukemia, paraganglioma and other tumors. Hence, such patients, if receiving radiation, should be informed of the increased risk of MPNST and other post irradiation sarcomas. Also, such patients should be followed-up closely throughout their life. [11],[16]
Tumors arising from peripheral nerves may cause difficulties in clinical diagnosis, in classification and in treatment. In neurofibromatosis, careful judgment is necessary in deciding which tumors must be removed and which can be left alone. Also, such patients need advice about the risk of a malignant transformation of a benign tumor and about risks of transmission of the disease to their children. [17]
In conclusion, this series highlights many variants of benign PNSTs and the association of MPNST with neurofibromatosis 1. It is essential to be familiar with all these variants and entities and establish their accurate histopathological diagnosis in view of their varying biological behavior.
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Correspondence Address:
Sushma Kashinath Gabhane
6-A, Forest Colony, Near New M.L.A., Hostel, Civil Lines, Nagpur 440 001
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0377-4929.44958
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3] |
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