Neurofibromatosis type 1 and malignancy in childhood
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1 Clin Genet 2016: 89: Printed in Singapore. All rights reserved Short Report 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd CLINICAL GENETICS doi: /cge Neurofibromatosis type 1 and malignancy in childhood Varan A., Şen H., Aydın B., Yalçın B., Kutluk T., Akyüz C. Neurofibromatosis type 1 and malignancy in childhood. Clin Genet 2016: 89: John Wiley & Sons A/S. Published by John Wiley & Sons Ltd, 2015 Neurofibromatosis type 1 (NF1) is an autosomal dominant hereditary neurocutaneous syndrome characterized by multi-system involvement and an increased incidence of both benign and malignant tumors. In this study, we evaluated the clinical presentation and prognosis and malignancy. Between 1975 and 2013, 26 (5%) of the 473 patients with NF1 at our center developed non- neoplasms. The patient files of 26 subjects with tumors, other than optic glioma, were analyzed retrospectively to evaluate clinical features and treatment results. The age at ranged from 3 months to 16 years (median 5.5 years). The age range at tumor was years (median 8 years) in these 26 patients. The tumor histological subtypes included the following: 12 soft-tissue tumors (6 malignant peripheral nerve sheath tumors (MPNST), 5 rhabdomyosarcomas (RMS) and 1 malignant fibrous histiocytoma), 11 brain tumors (6 low-grade gliomas, 3 high-grade gliomas, and 2 medulloblastoma), 2 neuroblastomas and 1 non-hodgkin s lymphoma. Twelve of 26 patients were alive at the time of the study. Although benign brain tumors with NF1 are more common, high-grade brain tumors also occur. Thus, careful and regular follow-up is crucial for early detection of malignancy in NF1 patients. Conflictofinterest The authors declare no conflict of interest. A. Varan, H. Şen, B. Aydın, B. Yalçın, T. Kutluk and C. Akyüz Department of Pediatric Oncology, Hacettepe University, Cancer Institute, Ankara, Turkey Key words: brain tumors malignant peripheral nerve sheath tumors tosis outcome Corresponding author: Ali Varan, MD, Professor of Pediatric and Pediatric Oncologist, Department of Pediatric Oncology, Hacettepe University, Cancer Institute, Ankara, Turkey. Tel.: ; fax: ; avaran@hacettepe.edu.tr Received 30 March 2015, revised and accepted for publication 11 June 2015 Neurofibromatosis type 1 (NF1) is one of the most common neurocutaneous disorders. It is caused by a mutation in 17q11.2 and affects approximately 1 in 2000 to 1 in 5000 people (1). Patients with NF1 have a life expectancy that is reduced by 15 years compared with the healthy population. The reduced longevity is mostly due to malignancy (2). Half of the cases are transmitted by autosomal dominant inheritance. The other cases are caused by de novo mutations resulting from the high rate of spontaneous mutation in the NF1 gene. The disease penetrance is 100% for patients with mutation, and NF1 shows wide phenotypic variability with an increased predisposition to benign and malignant tumors compared with the healthy population (3). The responsible gene encodes the protein neurofibromin, which regulates the Ras proto-oncogene. This mutation causes increased proliferation and tumorigenesis, especially in neurocutaneous tissue (4). There is an association between NF1 and the following malignant tumors: gliomas, malignant peripheral nerve sheath tumor (MPNST), leukemias, pheochromocytomas, rhabdomyosarcoma (RMS), gastrointestinal stromal tumors, breast cancers, melanomas, non-hodgkin lymphomas and carcinoid tumors (5). In younger populations, brain tumors and soft-tissue tumors have been found to be closely associated with NF1 (6, 7). Malignant tumors remain a major cause of mortality and morbidity in patients with NF1, and close follow-up is important for the early detection of malignancy. Twenty-six cases with NF1 and malignant tumors are described here for their clinical features, treatment, and follow-up. Materials and methods Patients with NF1 followed-up between 1975 and 2013 were identified by an electronic search of the hospital 341
2 Varan et al. information system accessed from our department. A total of 473 patients met two or more of the following diagnostic criteria for NF1: six or more café-au-lait spots >5 mm in diameter in prepubertal individuals or >15 mm in diameter in postpubertal individuals, two or more s of any type or 1 plexiform, axillary or inguinal freckling, optic glioma, two or more iris hamartomas (Lisch nodules), a distinctive osseous lesion such as sphenoid wing dysplasia or thinning of long bone cortex, and a first-degree relative with NF1 (8). Two or more diagnostic criteria were required. There were tumors other than optic gliomas in 26 patients. The medical records of these 26 patients were reviewed retrospectively for age, gender, family history, clinical features, radiologic features, histopathological findings, treatments, and follow-up data. Results n- neoplasms excluding optic gliomas were detected in 26 (5%) of 473 patients. The male/female ratio for the 26 patients was 16/10. The age at was between 3 months and 16 years (median 5.5 years), and of malignancy was between 1.5 and 33 years (median 8 years). There were 16 patients diagnosed with NF1 and malignancy simultaneously. Intracranial tumors were detected in 11 (2.3%) of 473 patients, and the age of of intracranial tumors ranged from 2 to 16 years (median 8 years) (Table 1). The most common complaints of patients with intracranial tumors were headache and vomiting. The histologic tumor subtypes included six low-grade gliomas, three high-grade gliomas, and two medulloblastomas. There were no patients with a history of radiotherapy exposure. The tumors were located in the cerebral hemisphere (five), posterior fossa (three), tectal plate (one), basal ganglia (one) and cervical spine (neck) (one). All high-grade gliomas were located in the cerebral hemisphere. Five of 11 patients died with disease despite treatment. There were three cases of high-grade glioma in the cerebral hemisphere, and one case with low-grade glioma. The other death had medulloblastoma and died after aspiration. Twelve of 26 children were diagnosed with soft-tissue sarcomas, and the histologic subtypes included the following: six MPNSTs, five RMS, and one malignant fibrous histiocytoma (Table 2). The age range at MPNST was years (median 15.5 years.) The tumors were primarily located in the extremities (three), axial (two), and head/neck region (one). Four patients showed rapid growth in pre-existing s. There was a painful fast-growing new mass observed in two patients. MPNST was detected in the follow-up period in five NF1 patients and simultaneously with NF1 in one patient. A complete tumor resection was performed in three patients, and a subtotal resection was performed in two patients. A tumor biopsy was performed in one patient. Three patients were treated with chemotherapy only, and two patients were treated with chemotherapy and radiotherapy. There was one patient treated with radiotherapy alone. The follow-up period ranged from 8 to 32 months (median 25 months). Five of the six patients died due to tumor progression, and one remained in remission for 32 months. The age range for RMS was years (median 2.5 years). The RMS tumors were primarily located in the pelvic region in three cases, vagina in one case, and neck region in one patient. A total resection was performed in two cases, and subtotal resection was performed in one case. The resections were performed at the time of. The two other patients were diagnosed using biopsy. All patients were treated with chemotherapy, and radiotherapy was administered to four patients. Three of the five patients were in remission during the follow-up period of 15 days to 14.5 years (median 8 years). One patient with pelvic RMS died because of neutropenia, and the one case with a cervical tumor died because of tumor progression. One patient with malignant fibrous histiocytoma of the occipital bone was treated with chemotherapy and radiotherapy Table 1. Clinical findings and outcomes of brain tumors of brain tumor Symptoms Histology Location Outcome 1 Male Headache, vomiting High-grade Occipital Died 18 2 Male 2 2 Seizures High-grade Temporal Died Male 8 8 Headache High-grade Frontal Died 15 4 Female 5 5 Seizures Astrocytoma Temporal Died 7 5 Male Headache, seizures Astrocytoma Basal ganglia Remission Male 4 4 Headache, vomiting Astrocytoma Parietal Alive with disease Male 9 15 Headache Astrocytoma Cerebellum Remission Male 4 4 Headache, vomiting Medulloblastoma Posterior fossa Died 1 9 Female 9 9 Headache, vomiting Medulloblastoma Posterior fossa Remission Male 2 8 Cervical pain, upper Cervical Cervical 4-7 Remission 28 extremity weakness vertebrae 11 Female 6 6 Walleye Tectal glioma Tectum Remission 4.1 NF1, tosis type
3 Neurofibromatosis type 1 and malignancy in childhood Table 2. Soft-tissue sarcomas: clinical findings and outcome of malignancy Symptoms Histology Location Outcome 1 Female 5 18 Rapid growing MPNST Thoracic 11-lumbar Died 15 3 vertebrae 2 Female 8 8 New mass with pain MPNST Psoas muscle Died 23 3 Female 5 19 Rapid growing MPNST Lumbar Died 30 4 Female 8 33 Rapid growing MPNST Face-neck Died 28 5 Male 1 13 Rapid growing MPNST Thigh Died 8 6 Male 0,25 1,6 New mass with pain MPNST Rectus femoris Remission 31 7 Male 2,5 2,5 Stomach ache RMS Pelvis Remission 98 8 Male 8 8 Dysuria RMS Pelvis Died Female Neck swelling RMS Cervical Died Male 1,5 1,5 Dysuria RMS Pelvis Remission Female 2,5 2,5 Vaginal bleeding RMS Vaginal Remission Male 7 15 Swelling on occipital area Malignant fibrous histiocytoma Occipital bone Remission 216 MPNST, malignant peripheral nerve sheath tumor; NF1, tosis type 1; RMS, rhabdomyosarcoma. Table 3. Other tumors associated with NF1 of brain tumor Symptoms Histology Location Present status 1 Female 8 8 Stomach ache NBL Surrenal Remission 98 2 Male 5,5 5,5 Leg pain NBL Surrenal Alive with disease Male 4 4 Cervical lymphadenopathy NHL Cervical, mediasten Died 9.8 NBL, neuroblastoma; NF1, tosis type 1; NHL, non-hodgkin s lymphoma. after total resection and was in remission after 18 years follow-up. Table 3 shows the features of other tumors associated with NF1. Neuroblastoma was detected in two patients. The first patient was treated with intensive chemotherapy, but surgery could not be performed because of the risk of high morbidity. Radiotherapy was administered, and the patient was in remission for 8 years with a residual tumor. The second patient had advanced stage disease with multiple bone involvement and was given intensive chemotherapy. High-dose chemotherapy and autologous stem cell transplantation were also performed. However, the treatments could not prevent disease relapse, and the patient was alive with disease. The last patient had T lymphoblastic lymphoma with cervical and mediastinal involvement. The patient initially responded to treatment but later had a relapse of disease in the central nervous system and died. Discussion The frequencies of benign and malignant tumor development are increased in children with NF1 compared with the healthy population. In a recent study, the incidence of malignancy in children younger than 16 years was 14.7% (9). Children under 10 years of age are most susceptible to the development of intracranial tumors and soft-tissue sarcomas, which are closely associated with NF1 in childhood (6, 7). In this study, malignancy occurred between 1.5 and 33 years (median 8 years) of age. Intracranial tumors occur in 20% of patients with NF1 (10) and have a better prognosis than their sporadic counterparts (11). Gliomas are the most common intracranial tumors and are the second most common tumor type after s. The majority of gliomas are pilocytic s, and these tumors generally arise from the optic pathway and brain stem (5). The other brain tumors associated with NF1 are medulloblastoma and malignant schwannoma (12, 13). Furthermore, high-grade gliomas have also been reported, and the prognosis of these tumors is poor. Cerebral hemisphere and posterior fossa tumors are uncommon and occur at a rate of approximately 1% each (14). Medulloblastomas are rarely associated with NF1 (15 17). In this study, three patients were identified with posterior fossa tumors. The incidence of high-grade tumors in NF1 is unclear but must be suspected in cases of unexpected localization and aggressive behavior (15). All five patients with high-grade intracranial tumors were diagnosed with NF1 343
4 Varan et al. simultaneously. Of the five high-grade tumors in this study, two were medulloblastomas located in posterior fossa, and the other three were high-grade gliomas of the cerebral hemispheres with no history of radiotherapy. These features distinguish the tumors from the studies reported in the literature. Three patients died due to tumor progression despite multimodal treatment. The risk of developing soft-tissue sarcomas in NF1 is higher than in the normal population. In this group, MPNST and RMS are closely associated with NF1, and MPNST is the most common soft-tissue malignant tumor associated with NF1. MPNST is a rare tumor in the general population, and approximately half of MPNST is associated with NF (7). In patients with NF, the lifetime risk of developing MPNST is estimated to be 8 13% (18). The most common complaint is new pain with growth of a new mass or the rapid growth of the pre-existing mass (18). The complaints of six patients in the current study with MPNST were painful rapid growing new masses in two patients and rapid growth in pre-existing s in four patients. Neurofibroma may be differentiated from MPNST with magnetic resonance imaging (MRI). MRI findings of MPNST are hemorrhage, necrosis and edema. However, MRI has a low sensitivity and specificity (19). In cases where MRI is not able to differentiate benign and MPNST, clinicians need to use positron emission tomography (PET) scans. The treatment of choice is complete surgical resection with wide tumor-free margins (7), but this strategy may lead to functional loss. Additionally, doxorubicin- and ifosfamide-based protocols are recommended (20), and radiotherapy after surgery can provide local control. Five of the six patients showed no response to chemotherapy, which is consistent with other studies in the literature. The number of patients followed in the present study was less than our estimate because MPNST is more common in adulthood and these patients are lost to follow-up. As a result, MPNST should be suspected in cases of fast-growing masses and new pain. RMS associated with NF1 is reported infrequently (21, 22). The prevalence of RMS in NF1 patients ranged from 1.4% to 6% (22, 23). The important features of RMS in NF1 patients included the following: embryonal histology, genitourinary or pelvic location, and young patients less than 3 years of age (24). Similar to other studies, all patients in the current study had an embryonal histology with a median age of 2.5 years at the time of. The tumors had genitourinary or pelvic locations in four patients. Three of the five patients were alive with a follow-up period ranging from 15 days to 14.5 years (median 8 years) in the present study. A few case reports of malignant fibrous histiocytoma in NF1 have been reported mostly in adulthood (25). The association between NF1 and neuroblastoma has been rarely reported including the coincidence of these disorders in familial neuroblastoma (26). The existence of lymphoid neoplasms in patients with NF1 has been infrequently reported in a population-based study by Stiller et al. (27), which showed there is a 10-fold increase in the relative risk of lymphoma. NF is an inherited tumor predisposition syndrome that leads to an increased incidence of malignancy, which is a major cause of mortality and morbidity. Clinical behavior and treatment response of malignant tumors in NF1 patients differ from sporadic cases. Close and regular follow-up is crucial for early detection of malignancy in NF1 patients. References 1. Rasmussen SA, Friedman JM. NF1 gene and tosis 1. Am J Epidemiol 2000: 151: Zoller M, Rembeck B, Akesson HO, Angervall L. Life expectancy, mortality and prognostic factors in tosis type 1. A twelve-year follow-up of an epidemiological study in Goteborg, Sweden. Acta Derm Venereol 1995: 75: Riccardi VM, Lewis RA. Penetrance of von Recklinghausen tosis: a distinction between predecessors and descendants. Am J Hum Genet 1988: 42: Basu TN, Gutmann DH, Fletcher JA, Glover TW, Collins FS, Downward J. Aberrant regulation of ras proteins in malignant tumour cells from type 1 tosis patients. Nature 1992: 356: Yohay K. Neurofibromatosis type 1 and associated malignancies. Curr Neurol Neurosci Rep 2009: 9: Sorensen SA, Mulvihill JJ, Nielsen A. Long-term follow up of von Recklinghausen tosis. Survival and malignant neoplasms. N Engl J Med 1986: 314: Ducatman BS, Scheithauer BW, Piepgras DG et al. Malignant peripheral nerve sheath tumors. A clinicopathologic study of 120 cases. Cancer 1986: 57: Friedman JM. Neurofibromatosis 1: clinical manifestations and diagnostic criteria. J Child Neurol 2002: 17: McKeever K, Shepherd CW, Crawford H, Morrison PJ. An epidemiological, clinical and genetic survey of tosis type 1 in children under sixteen years of age. Ulster Med J 2008: 77: Rosser PRT. Intracranial neoplasms in children with tosis 1. J Child Neurol 2002: 17: Jett K, Friedman JM. Clinical and genetic aspects of tosis 1. Genet Med 2010: 12: Korf BR. Malignancy in tosis type 1. Oncologist 2000: 5: Cohen BH, Kaplan AM, Packer RJ. Management of intracranial neoplasms in children with tosis type 1 and 2. The Children s Cancer Study Group. Pediatr Neurosurg : 16: Pascual-Castroviejo I, Pascual-Pascual SI, Viaño J et al. Posterior fossa tumors in children with tosis type 1 (NF1). Childs Nerv Syst 2010: 26: Rosenfeld A, Listernick R, Charrow J et al. Neurofibromatosis type 1 and high-grade tumors of the central nervous system. Childs Nerv Syst 2010: 26: Perilongo FCG, Meadows A, well P et al. Sequential development of wilms tumor, T-cell acute lymphoblastic leukemia, medulloblastoma, and myeloid leukemia in a child with type 1 tosis: a clinical and cytogenetic case report. Leukemia 1993: 7: Martinez-Lage SCJ, Poza M. Medulloblastomas in tosis type 1. Case report and literature review. Neurocirugia 2002: 13: Evans DG, Baser ME, McGaughran J et al. Malignant peripheral nerve sheath tumours in tosis 1. J Med Genet 2002: 39: Mautner VF, Friedrich RE, von Deimling A et al. Malignant peripheral nerve sheath tumours in tosis type 1: MRI supports the of malignant plexiform. Neuroradiology 2003: 45: Ferner RE, Gutmann DH. International consensus statement on malignant peripheral nerve sheath tumors in tosis. Cancer Res 2002: 62: Coffin CM, Cassity J, Viskochil D et al. n-neurogenic sarcomas in four children and young adults with tosis type 1. Am J Med Genet A 2004: 127: Reich S, Overberg-Schmidt US, Leenen A, Henze G. Neurofibromatosis 1 associated with embryonal rhabdomyosarcoma of the urinary bladder. Pediatr Hematol Oncol 1999: 16:
5 Neurofibromatosis type 1 and malignancy in childhood 23. Lampe AK, Seymour G, Thompson PW et al. Familial tosis microdeletion syndrome complicated by rhabdomyosarcoma. Arch Dis Child 2002: 87: Sung L, Anderson JR, Arndt C et al. Neurofibromatosis in children with rhabdomyosarcoma: a report from the Intergroup Rhabdomyosarcoma Study IV. J Pediatr 2004: 144: Papagelopoulos PJ, Mavrogenis AF, Galanis EC et al. Malignant fibrous histiocytoma of bone associated with type-1 tosis. A case report. J Bone Joint Surg Am 2005: 87: Maris JM, Weiss MJ, Mosse Y. Evidence for a hereditary neuroblastoma predisposition locus at chromosome 16p Cancer Res 2002: 62: Stiller CA, Chessells JM, Fitchett M. Neurofibromatosis and childhood leukaemia/lymphoma: a population-based UKCCSG study. Br J Cancer 1994: 70: Sharif FRS, Birch J, Gillespie J et al. Second primary tumors in tosis 1 patients treated for optic glioma: substantial risks after radiotherapy. J Clin Oncol 2006: 24:
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