Oncologist. The. Neuro-Oncology. Case Report: An Unusual Case of Adrenal Neuroblastoma in Pregnancy
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1 The Oncologist Neuro-Oncology Case Report: An Unusual Case of Adrenal Neuroblastoma in Pregnancy MARWAN M. REFAAT, a SHEREENE Z. IDRISS, b LAWRENCE S. BLASZKOWSKY a,c a Department of Medicine, b Department of Dermatology, and c Division of Hematology-Oncology, Massachusetts General Hospital, Boston, Massachusetts, USA Key Words. Adrenal Adult Neuroblastoma Pregnancy Disclosure: No potential conflicts of interest were reported by the authors, planners, reviewers, or staff managers of this article. ABSTRACT Neuroblastomas are the fourth most common malignancy of childhood and account for most adrenal tumors in children. However, they are rarely reported in adults. We present herein an extremely rare case of adrenal neuroblastoma occurring in a 25-year-old woman during her first trimester of pregnancy. She had a spontaneous abortion secondary to chorioamnionitis and she was operated on for an incidentaloma. Her tumor was curatively resected. She presented with right lower quadrant abdominal pain CASE PRESENTATION A 25-year-old woman was in her usual state of health until she presented in her 10th week of pregnancy complaining of abdominal cramping and vaginal bleeding. She had a spontaneous abortion as a result of chorioamnionitis. Physical exam revealed a nontender palpable firm mass in her right lower abdomen. As part of the evaluation, a transvaginal ultrasound was performed, revealing a cm mass adjacent to the right adrenal gland. Magnetic resonance imaging (MRI) of the mass without contrast confirmed a heterogeneous right adrenal mass (Fig. 1). Urine levels of vannilyl mandelic acid (VMA), dopamine, total metanephrines, and normetanephrine were all elevated, at 28.4 mg (reference range, 8 mg), 553 g (age-adjusted female range, g), months after her operation and there was evidence of local tumor recurrence without metastasis. Adult adrenal neuroblastoma is an uncommon malignancy and, to our knowledge, there was no case of this tumor occurring in pregnancy ever described in the English literature. The case presentation is followed by a general discussion with an emphasis on the diagnosis, treatment, and follow-up of neuroblastoma and its association with pregnancy. The Oncologist 2008;13: g (age-adjusted female range, g), and 477 g (age-adjusted female range, g), respectively, in 24 hours. Because of the biochemical compatibility, the incidentaloma was initially diagnosed as a pheochromocytoma. During right adrenalectomy, a rounded mass measuring 11.5 cm was found near the right lobe of the liver and originating in the right adrenal gland. Surrounded by residual adrenal gland tissue, the mass was excised, and the examined resection margins were negative for tumor (Fig. 2). Direct extra-adrenal extension was not identified. Areas of cystification and necrosis were noted within the mass. No complications were encountered during the postoperative period, and the 24-hour urine catecholamines were within the normal range. Correspondence: Marwan Refaat, M.D., Massachusetts General Hospital, Department of Medicine, GRB 740, 55 Fruit Street, Boston, Massachusetts 02114, USA. Telephone ; Fax: ; rifaatmarwan@hotmail.com Received October 30, 2006; accepted for publication December 23, AlphaMed Press /2008/$30.00/0 doi: /theoncologist The Oncologist 2008;13:
2 Refaat, Idriss, Blaszkowsky 153 Figure 1. Magnetic resonance imaging scan of the mass without contrast confirmed an cm heterogeneous right adrenal mass with areas of hemorrhage, high signal on T1-weighted images, and no fat saturation. Figure 2. The macroscopic appearance of the adrenal mass showed an cm tan-red adrenal mass with a smooth to focally irregular surface. Sectioning revealed a tan to red, multiloculated, solid, and cystic internal surface and focal areas of hemorrhage. A histopathological examination revealed a tumor with undifferentiated primitive-appearing round blue cells in a lobular pattern, forming sheets of Homer-Wright rosettes suggestive of a neuroblastoma. No ganglion cells were seen. A low mitosis karyorrhexis index (MKI) ( 100/5000 tumor cells) and unfavorable age-adjusted Shimada histology were characteristic findings consistent with an undifferentiated stroma-poor neuroblastoma (Fig. 3). On immunohistochemical stains, the tumor cells were positive for chromogranin and synaptophysin, and negative for melan A, S-100, and cytokeratin. The immunophenotype further supported the diagnosis of neuroblastoma. Fluorescence in situ hybridization for 1p36 deletion was negative and no N-myc amplification was detected, all of which suggested a more favorable prognosis. Based on imaging, surgical, and pathology findings, the Figure 3. The microscopic appearance of the specimen showed a tumor with undifferentiated, primitive-appearing, round blue cells in a lobular pattern, forming sheets of Homer- Wright rosettes. (Hematoxylin and eosin stain, magnification 125.) patient s International Neuroblastoma Staging System (INSS) stage is stage I. The staging workup included a positron emission tomography (PET) scan, repeat computed tomography (CT) scan of the chest, abdomen, and pelvis, bone scan, and bilateral bone marrow aspirates and biopsies, all of which revealed no evidence of metastatic disease. The patient was doing well on a follow-up 20 months after her surgery. Her 24-hour urine collection was remarkable for a VMA level of 6.4 mg (reference range, 8 mg), metanephrine level of 79 g (age-adjusted female range, g), normetanephrine level of 247 g (age-adjusted female range, g), and total metanephrine level of 326 g (age-adjusted female range, g). The plan was to observe the patient with CT scans every 6 months until 5 years after her adrenelectomy. Unfortunately, she was noncompliant with her imaging studies despite multiple notifications. She presented back 26 months after her surgery with right lower abdominal pain for which a CT scan of the abdomen and pelvis was performed. This demonstrated a mass appearing to arise from the right adrenal gland remnants measuring cm exerting a mass effect on the inferior vena cava anteriorly and right kidney medially, and displacing the kidney laterally. The findings are likely suggestive of recurrence of the neuroblastoma. A PET scan showed faint, heterogeneous radiotracer uptake with a more intense focus superiorly in the region of the adrenalectomy bed corresponding to a soft tissue mass seen on a recent CT. A chest CT showed no evi-
3 154 Adrenal Neuroblastoma in Pregnancy dence of metastatic disease to the chest. She underwent surgical resection of the tumor, which was an 8-cm right retroperitoneal stroma-poor undifferentiated neuroblastoma. The resected margins were negative for malignancy. The patient had a normal bone marrow biopsy and aspirate. CLINICAL PRESENTATION AND WORKUP Neuroblastoma refers to a malignancy derived from primitive neural crest cells of the adrenal medulla. Neuroblastomas are the fourth most common malignancy of childhood [1]. Up until September 2007, no more than 60 neuroblastomas in adults had been reported in the literature. The most common manifestations are to the result of a tumor mass, most likely an abdominal mass, or bone pain from metastases. A large percentage of neuroblastomas undergo spontaneous regression, and this could possibly account for the scarcity of its presence among the adult population [2]. Typically presenting at 22 months, they display no predilection for gender [3]. Clinical data suggest that 40% of neuroblastomas arise from within the adrenal gland. Symptoms associated with the diagnosis are usually unrelated to any catecholamine imbalance. However, on rare occasions, compression of the renal artery may lead to hypertension as a presenting manifestation [4]. The most common symptoms are a hard, asymptomatic mass in the abdomen, or bone pain resulting from metastatic spread. Neoplasms are extremely uncommon in pregnancy, although malignancies of the breast, cervix, and ovaries have been well documented throughout the obstetric literature. Hormonal changes associated with pregnancy, especially in the late phase of the third trimester, when estrogen levels reach a maximum, have been known to play a role in the amplification of tumor growth. It has been suggested that estrogen may play a role in the development of soft tissue sarcomas. Although a biopsy is considered the sine qua non of diagnosing a neuroblastoma, laboratory studies and imaging play essential roles as part of the evaluation. Twenty-fourhour urine catecholamine levels and their metabolites such as VMA are often elevated, and may lead to an initial diagnosis of pheochromocytoma. A plain abdominal radiograph, including the kidneys, ureters, and bladder, is also recommended in the primary assessment. After the identification of a mass on x-ray, a renal/bladder sonogram should be performed. This noninvasive imaging modality allows for a more thorough diagnostic evaluation. The laterality of the mass, its size, and the presence of calcifications are observed by abdominal CT. MRI may provide information regarding invasion into regional lymph nodes and vessels. Bone scintigraphy and/or a Table 1. The International Neuroblastoma Staging System Stage Criteria Stage 1 Localized tumor with a complete gross excision, with or without microscopic residual disease; ipsilateral lymph nodes negative for tumor microscopically (nodes attached to and removed with the primary tumor may be positive) Stage 2A Localized tumor with incomplete gross excision; ipsilateral nonadherent lymph nodes negative for tumor microscopically Stage 2B Localized tumor with or without complete gross excision, with ipsilateral nonadherent lymph nodes positive for tumor. Enlarged contralateral lymph nodes must be negative microscopically Stage 3 Unresectable unilateral tumor infiltrating across the midline (vertebral column) with or without regional lymph node involvement; or localized unilateral tumor with contralateral regional lymph node involvement; or midline tumor with bilateral extension by infiltration (unresectable) or by lymph node involvement Stage 4 Any primary tumor with dissemination to distant lymph nodes, bone, bone marrow, liver, skin, and/or other organs, except as defined for stage 4S Stage 4S Localized primary tumor as defined for stage 1, 2A, or 2B, with dissemination limited to skin, liver, and/or bone marrow (limited to infants 1 year of age). Marrow involvement should be minimal ( 10% of total nucleated cells identified as malignant by bone biopsy or by bone marrow aspirate). More extensive bone marrow involvement would be considered to be stage 4 disease. The results of a metaiodobenzylguanidine scan, if performed, should be negative for disease in the bone marrow skeletal survey are often helpful when bone metastasis is suspected [1]. The histopathological examination of neuroblastoma reveals a tumor with undifferentiated, primitive-appearing round blue cells with hyperchromatic nuclei and scant cytoplasm in a lobular pattern. Sheets of Homer-Wright pseudorosettes, consisting of neuroblasts surrounding eosinophilic neuropil, are a pathognomonic feature confirming the diagnosis of neuroblastoma [5 7]. Shimada et al. [8] developed a classification scheme for
4 Refaat, Idriss, Blaszkowsky 155 neuroblastomas. The system uses the degree of neuroblast differentiation, the Schwannian stromal quality, the MKI, the growth pattern, and the patient s age to classify the histology as either favorable or unfavorable. Patients belonging to one of the three following categories are considered within the favorable category: 1. Patients of any age with stroma-rich tumors without a nodular pattern. 2. Patients 18 months old with stroma-poor tumors, an MKI 200/5,000 (200 karyorrhectic cells per 5,000 cells scanned), and differentiated or undifferentiated neuroblasts. 3. Patients 60 months old with stroma-poor tumors, an MKI 100/5,000, and well-differentiated tumor cells. Staging, along with age at diagnosis and certain tests on tumor specimens, such as histology and N-myc amplification, play critical roles in the recommendations of specific treatment modalities [9]. The INSS is shown in Table 1. TREATMENT Although neuroblastoma is among the curable tumors in young children, it is associated with a worse prognosis in adults, with a 5-year median survival rate after diagnosis 40% [10 12]. Patients are classified into one of three risk groups: low, intermediate, and high risk. A combination of factors, consisting of the International Neuroblastoma Classification scheme along with tumor biology such as N- myc amplification, tumor stage including metastases and ploidy, and patient age, help define the three risk categories described above. Studies have demonstrated that, for low-risk patient groups (patients with low-stage neuroblastoma such as stage 1, 2A, or 2B) like our patient, total surgical excision is REFERENCES 1 Kushner BH, Cheung NK. Neuroblastoma from genetic profiles to clinical challenge. N Engl J Med 2005;353: Yamamoto K, Hanada R, Kikuchi A et al. Spontaneous regression of localized neuroblastoma detected by mass screening. J Clin Oncol 1998;16: Koontz SE. Common pediatric cancers. US Pharmacist 2004;10(onc suppl): Koch CA, Brouwers FM, Rosenblatt K et al. Adrenal ganglioneuromas in a patient presenting with severe hypertension and diarrhea. Endocr Relat Cancer 2003;10: Weinstein JL, Katzenstein HM, Cohn SL. Advances in the diagnosis and treatment of neuroblastoma. The Oncologist 2003;8: Triche TJ, Askin FB. Neuroblastoma and the differential diagnosis of small-, round-, blue-cell tumors. Hum Pathol 1983;14: Rubie H, Hartmann O, Michon J et al. N-myc gene amplification is a major prognostic factor in localized neuroblastoma: Results of the French NBL 90 curative 95% of the time. Several factors, such as tumor location, especially regarding its relationship to major nerves and blood vessels, the presence of metastases, patient age, and tumor mobility, determine the resectability of the tumor. For patients in whom resectability of the tumor may compromise vital organs, surgery should be postponed until after combination chemotherapy has been administered to reduce the size of the tumor. The success of such an approach has been demonstrated by several studies [13 15]. Chemotherapy is reserved for patients with favorably localized yet unresectable disease, or who present with lifethreatening symptoms such as spinal cord compression. A commonly used drug combination of low- or moderateintensity chemotherapy is often used, and includes active agents such as cyclophosphamide, doxorubicin, carboplatin, and etoposide [16 24]. Although the prognosis of this disease is poor in adults, our patient had a favorable low-risk assessment of her tumor [25]. She had stage 1 disease with a local recurrence completely excised, and her tumor lacked N-myc amplification. Urine studies (VMA, metanephrine, normetanephrine, dopamine) and a CT scan of the chest, abdomen, and pelvis will be repeated in 6 months. ACKNOWLEDGMENT Marwan Refaat and Shereene Idriss contributed equally to the article. AUTHOR CONTRIBUTIONS Conception/design: Marwan M. Refaat, Shereene Z. Idriss, Lawrence S. Blaszkowsky Data analysis and interpretation: Marwan M. Refaat, Shereene Z. Idriss, Lawrence S. Blaszkowsky Manuscript writing: Marwan M. Refaat, Shereene Z. Idriss, Lawrence S. Blaszkowsky Final approval of manuscript: Marwan M. Refaat, Lawrence S. Blaszkowsky study. Neuroblastoma Study Group of the Société Française d Oncologie Pédiatrique. J Clin Oncol 1997;15: Shimada H, Ambros IM, Dehner LP et al. The International Neuroblastoma Pathology Classification (the Shimada system). Cancer 1999;86: Brodeur GM, Pritchard J, Berthold F et al. Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 1993;11: Woods WG, Gao RN, Shuster JJ et al. Screening of infants and mortality due to neuroblastoma. N Engl J Med 2002;346: Franks LM, Bollen A, Seeger RC et al. Neuroblastoma in adults and adolescents: An indolent course with poor survival. Cancer 1997;79: Gaspar N, Hartmann O, Munzer C et al. Neuroblastoma in adolescents. Cancer 2003;98: Rubie H, Coze C, Plantaz D et al. Localised and unresectable neuroblastoma in infants: Excellent outcome with low-dose primary chemotherapy. Br J Cancer 2003;89:
5 156 Adrenal Neuroblastoma in Pregnancy 14 Rubie H, Plantaz D, Coze C et al. Localised and unresectable neuroblastoma in infants: Excellent outcome with primary chemotherapy. Neuroblastoma Study Group, Société Française d Oncologie Pédiatrique. Med Pediatr Oncol 2001;36: Leclair MD, Hartmann O, Heloury Y et al. Localized pelvic neuroblastoma: Excellent survival and low morbidity with tailored therapy the 10-year experience of the French Society of Pediatric Oncology. J Clin Oncol 2004; 22: Katzenstein HM, Bowman LC, Brodeur GM et al. Prognostic significance of age, MYCN oncogene amplification, tumor cell ploidy, and histology in 110 infants with stage D(S) neuroblastoma: The pediatric oncology group experience a Pediatric Oncology Group study J Clin Oncol 1998;16: Nickerson HJ, Matthay KK, Seeger RC et al. Favorable biology and outcome of stage IV-S neuroblastoma with supportive care or minimal therapy: A Children s Cancer Group study. J Clin Oncol 2000;18: Simon T, Spitz R, Faldum A et al. New definition of low-risk neuroblastoma using stage, age, and 1p and MYCN status. J Pediatr Hematol Oncol 2004;26: Brodeur GM, Maris JM. Neuroblastoma. In: Principles and Practice of Pediatric Oncology. Pizzo PA, Poplack DG, eds). Philadelphia: Lippincott Williams & Wilkins, 2002: Matthay KK, Villablanca JG, Seeger RC et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children s Cancer Group. N Engl J Med 1999;341: Laprie A, Michon J, Hartmann O et al. High-dose chemotherapy followed by locoregional irradiation improves the outcome of patients with international neuroblastoma staging system stage II and III neuroblastoma with MYCN amplification. Cancer 2004;101: Haas-Kogan DA, Swift PS, Selch M et al. Impact of radiotherapy for highrisk neuroblastoma: A Children s Cancer Group study. Int J Radiat Oncol Biol Phys 2003;56: Marcus KJ, Shamberger R, Litman H et al. Primary tumor control in patients with stage 3/4 unfavorable neuroblastoma treated with tandem double autologous stem cell transplants. J Pediatr Hematol Oncol 2003;25: Rowe PH, Oram JJ, Scott GW. Neuroblastoma in adults. Postgrad Med J 1979;55: Perez CA, Matthay KK, Atkinson JB et al. Biologic variables in the outcome of stages I and II neuroblastoma treated with surgery as primary therapy: A Children s Cancer Group study. J Clin Oncol 2000;18:18 26.
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