570361
research-article2015
IJSXXX10.1177/1066896915570361International Journal of Surgical PathologyWu et al
Case Reports
Ovarian Immature Teratoma With Gliomatosis Peritonei and Pleural Glial Implant: A Case Report
International Journal of Surgical Pathology 1–3 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896915570361 ijs.sagepub.com
Pao-Shu Wu, MD, PhD1, and Chiung-Ru Lai, MD1
Abstract Gliomatosis peritonei is a very rare phenomenon occurring almost exclusively in association with ovarian immature teratoma. It is characterized by numerous benign, mature glial nodules in the omentum and mesentery. The presence of glial tissue outside abdominal cavity is extremely rare in the setting of ovarian immature teratoma. We present a case of ovarian immature teratoma with both gliomatosis peritonei and pleural glial implant in a 4-year-old girl. Glial emboli were present in the pleural implant, suggesting lymphovascular dissemination might be the cause of extra-abdominal glial implantation. Keywords immature teratoma, gliomatosis peritonei, pleural glial implant, ovary
Introduction Gliomatosis peritonei, a very rare phenomenon, occurs almost exclusively in association with ovarian immature teratomas. It is characterized by the presence of multiple mature glial nodules in the peritoneum and omentum.1-3 However, glial implantation outside the abdominal cavity is extremely rare. Herein, we report a case of ovarian immature teratoma with both gliomatosis peritonei and pleural glial implant.
Case Report A 4-year-old girl presented with lower abdominal pain for one month. Physical examination showed a firm palpable mass in the left lower quadrant of abdomen. The serum α-fetoprotein level was mildly elevated (38 ng/mL). Computed tomography scan revealed a 15-cm, heterogeneous cystic mass in the left adnexa. In addition, a 2.3-cm, hypodense nodule on the right supradiaphragmatic pleura was found. The patient underwent exploratory laparotomy to resect the left adnexal tumor. Multiple white to yellowish nodules, measuring from 1 to 2.5 cm, were noted in the pelvic peritoneum and mesentery. These nodules were excised and intraoperative peritoneal washing cytology sample was collected. The pleural nodule was resected 3 months later via exploratory thoracotomy. The left adnexa tumor measured 12.5 × 12 × 6 cm and weighed 650 g. It was a multilocular cystic mass with solid components, including fat, cartilage, and bone. Microscopically, haphazard distribution of tissue from 3
germ cell layers, including abundant mature glial tissue, were noted (Figure 1A). The immature, embryonal neuroepithelial tissue (Figure 1B) occupied less than 1 lowpower field in each slide examined, consistent with a grade I immature teratoma.4 Nodules in peritoneum and mesentery showed aggregates of mature glial cells embedded among fibrous tissue and mesothelial cells (Figure 2A). The glial tissue was positive for glial fibrillary acidic protein (GFAP) immunohistochemical stain (Figure 2B). In addition, the peritoneal washing cytology revealed sheets of glial cells with oval to short spindle nuclei, indistinct cytoplasmic border, and delicate fibrillary processes, consistent with glial cell morphology. The pleural nodule also showed mature glial tissue with delicate neurofibrillary stroma interspersed with fibrous septa and capillaries. Several GFAP-positive glial emboli were found in the lymphovascular channels (Figure 3). There was no cytological atypia, mitotic activity or any immature embryonal-type tissue found in the peritoneal and pleural implants. The patient received adjuvant chemotherapy of bleomycin, cisplantin, and etoposide regime for 3 cycles and she has been free of tumor recurrence or metastasis for 18 months. 1
Taipei Veterans General Hospital, Taipei, Taiwan
Corresponding Author: Pao-Shu Wu, Department of Pathology and Laboratory Medicine, Taipei Veterans General Hospital, No. 201, Sector 2, Shipai Road, Taipei City 11217, Taiwan Email: [email protected]
Downloaded from ijs.sagepub.com at WESTERN OREGON UNIVERSITY on June 11, 2015
2
International Journal of Surgical Pathology
Figure 1. The ovarian immature teratoma. (A) Haphazard distribution of tissue from 3 germ layers (20×). (B) Primitive neuroectodermal epithelium (200×). Hematoxylin and eosin stain.
Figure 2. Gliomatosis peritonei. (A) Aggregates of mature glial tissue surrounded with mesothelial cells in the peritoneal implant (hematoxylin and eosin stain, 200×). (B) The glial nodule was immunoreactive for glial fibrillary acidic protein (200×).
Discussion Although gliomatosis peritonei has been reported in association with teratomas of endometrium,5 stomach,6 or even as a complication of ventriculoperitoneal shunt in the absence of teratoma,7 most cases of gliomatosis peritonei occur in the setting of ovarian immature teratoma. Intrathoracic glial implantation associated with ovarian immature teratoma is exceedingly rare. Only 1 case was reported previously in English literature. In that case, an ovarian immature teratoma with gliomatosis peritonei and a 2-cm pleural nodule was found in a 12-year-old girl. The pleural implant was composed of mature glial tissue, but no lymphovascular glial emboli were found.8 Two theories on histogenesis of gliomatosis peritonei have been proposed. The first one suggests the peritoneal glial implants arise from the primary teratoma, either by direct extrusion from ruptured tumor capsule or through angiolymphatic spreading.1,9 An alternative theory suggests the origin of peritoneal glial tissue is not from the primary teratoma but via the metaplasia of pluripotent Müllerian stem cells residing on the peritoneal surface or adjacent mesenchymal tissue.10 The metaplastic theory is
supported by molecular studies demonstrating the peritoneal glial implants are genetically distinct from the associated teratoma. Normal somatic tissue contains genetic alleles contributed from both maternal and paternal origins, whereas most ovarian teratomas contain duplicated maternal genetic materials.11 By genotyping the polymorphic microsatellite loci, Ferguson et al12 and Kwan et al13 revealed the glial implants exhibited heterozygosity at many microsatellite loci, whereas the associated teratoma showed homozygous patterns, indicating their nonclonal relationship. Although only 7 cases from both studies have been analyzed due to the rarity of gliomatosis peritonei, the results provide compelling evidence that most, if not all, gliomatosis peritonei are derived from nonteratomatous somatic cells rather than the result of direct spreading of mature glial tissue from the primary teratomas. The pathogenesis of intrathoracic glial implantation might be similar to gliomatosis peritonei via a metaplastic process. Alternatively, the pleural implants might be the consequence of direct angiolymphatic spreading from the existing gliomatosis peritonei. In the single case reported
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3
Wu et al References
Figure 3. Presence of glial emboli in the lymphovascular channels at the periphery of the pleural implant (hematoxylin and eosin stain, 40×).
previously, no lymphatic tissue was found in the intrathoracic nodule and the authors were in favor of the metaplastic theory.8 In our case, however, glial emboli in the pleural implant were clearly demonstrated, indicating the possibility of lymphovascular dissemination from either gliomatosis peritonei or the ovarian immature teratoma. Genotyping of microsatellite loci might shed light on the origin of the pleural glial implant. In summary, we describe an extremely rare case of ovarian immature teratoma associated with both gliomatosis peritonei and pleural glial implant. Albeit rare, pathologists should be aware of the possibility of extra-abdominal presence of glial implantation in the setting of ovarian immature teratomas. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
1. Robboy SJ, Scully RE. Ovarian teratoma with glial implants on the peritoneum: an analysis of 12 cases. Hum Pathol. 1970;1:643-653. 2. Fortt RW, Mathie IK. Gliomatosis peritonei caused by ovarian teratoma. J Clin Pathol. 1969;22:348-353. 3. Harms D, Jänig U, Göbel U. Gliomatosis peritonei in childhood and adolescence: clinicopathological study of 13 cases including immunohistochemical findings. Pathol Res Pract. 1989;184:422-430. 4. Kurman RJ, Carcangiu ML, Herrington CS, Young RH, eds. World Health Organization Classification of Tumours of Female Reproductive Organs. Lyon, France: IARC Press; 2014. 5. Ansah-Boateng Y, Wells M, Poole DR. Coexistent immature teratoma of the uterus and endometrial adenocarcinoma complicated by gliomatosis peritonei. Gynecol Oncol. 1985;21:106-110. 6. Coulson WF. Peritoneal gliomatosis from a gastric teratoma. Am J Clin Pathol. 1990;94:87-89. 7. Hill DA, Dehner LP, White FV, Langer JC. Gliomatosis peritonei as a complication of a ventriculoperitoneal shunt: case report and review of the literature. J Pediatr Surg. 2000;35:497-499. 8. Lipskar AM, Rothstein DH, Soffer AZ, Edelman M, Glick RD. Intrathoracic glial implants in a child with gliomatosis peritonei. J Pediatr Surg. 2009;44:1817-1820. 9. El Shafie M, Furay RW, Chablani LV. Ovarian teratoma with peritoneal and lymph node metastases of mature glial tissue. J Surg Oncol. 1984;27:18-21. 10. Dallenbach-Hellweg G. Critical commentary to Gliomatosis peritonei combined with mature ovarian teratoma. Pathol Res Pract. 1995;191:1037. 11. Surti U, Hoffner L, Chakravarti A, Ferrell RE. Genetics and biology of human ovarian teratomas. I. Cytogenetic analysis and mechanism of origin. Am J Hum Genet. 1990;47: 635-643. 12. Ferguson AW, Katabuchi H, Ronnett BM, Cho KR. Glial implants in gliomatosis peritonei arise from normal tissue, not from the associated teratoma. Am J Pathol. 2001;159: 51-55. 13. Kwan MY, Kalle W, Lau GT, Chan JK. Is gliomatosis peritonei derived from the associated ovarian teratoma? Hum Pathol. 2004;35:685-688.
Downloaded from ijs.sagepub.com at WESTERN OREGON UNIVERSITY on June 11, 2015
research-article2015
IJSXXX10.1177/1066896915570361International Journal of Surgical PathologyWu et al
Case Reports
Ovarian Immature Teratoma With Gliomatosis Peritonei and Pleural Glial Implant: A Case Report
International Journal of Surgical Pathology 1–3 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896915570361 ijs.sagepub.com
Pao-Shu Wu, MD, PhD1, and Chiung-Ru Lai, MD1
Abstract Gliomatosis peritonei is a very rare phenomenon occurring almost exclusively in association with ovarian immature teratoma. It is characterized by numerous benign, mature glial nodules in the omentum and mesentery. The presence of glial tissue outside abdominal cavity is extremely rare in the setting of ovarian immature teratoma. We present a case of ovarian immature teratoma with both gliomatosis peritonei and pleural glial implant in a 4-year-old girl. Glial emboli were present in the pleural implant, suggesting lymphovascular dissemination might be the cause of extra-abdominal glial implantation. Keywords immature teratoma, gliomatosis peritonei, pleural glial implant, ovary
Introduction Gliomatosis peritonei, a very rare phenomenon, occurs almost exclusively in association with ovarian immature teratomas. It is characterized by the presence of multiple mature glial nodules in the peritoneum and omentum.1-3 However, glial implantation outside the abdominal cavity is extremely rare. Herein, we report a case of ovarian immature teratoma with both gliomatosis peritonei and pleural glial implant.
Case Report A 4-year-old girl presented with lower abdominal pain for one month. Physical examination showed a firm palpable mass in the left lower quadrant of abdomen. The serum α-fetoprotein level was mildly elevated (38 ng/mL). Computed tomography scan revealed a 15-cm, heterogeneous cystic mass in the left adnexa. In addition, a 2.3-cm, hypodense nodule on the right supradiaphragmatic pleura was found. The patient underwent exploratory laparotomy to resect the left adnexal tumor. Multiple white to yellowish nodules, measuring from 1 to 2.5 cm, were noted in the pelvic peritoneum and mesentery. These nodules were excised and intraoperative peritoneal washing cytology sample was collected. The pleural nodule was resected 3 months later via exploratory thoracotomy. The left adnexa tumor measured 12.5 × 12 × 6 cm and weighed 650 g. It was a multilocular cystic mass with solid components, including fat, cartilage, and bone. Microscopically, haphazard distribution of tissue from 3
germ cell layers, including abundant mature glial tissue, were noted (Figure 1A). The immature, embryonal neuroepithelial tissue (Figure 1B) occupied less than 1 lowpower field in each slide examined, consistent with a grade I immature teratoma.4 Nodules in peritoneum and mesentery showed aggregates of mature glial cells embedded among fibrous tissue and mesothelial cells (Figure 2A). The glial tissue was positive for glial fibrillary acidic protein (GFAP) immunohistochemical stain (Figure 2B). In addition, the peritoneal washing cytology revealed sheets of glial cells with oval to short spindle nuclei, indistinct cytoplasmic border, and delicate fibrillary processes, consistent with glial cell morphology. The pleural nodule also showed mature glial tissue with delicate neurofibrillary stroma interspersed with fibrous septa and capillaries. Several GFAP-positive glial emboli were found in the lymphovascular channels (Figure 3). There was no cytological atypia, mitotic activity or any immature embryonal-type tissue found in the peritoneal and pleural implants. The patient received adjuvant chemotherapy of bleomycin, cisplantin, and etoposide regime for 3 cycles and she has been free of tumor recurrence or metastasis for 18 months. 1
Taipei Veterans General Hospital, Taipei, Taiwan
Corresponding Author: Pao-Shu Wu, Department of Pathology and Laboratory Medicine, Taipei Veterans General Hospital, No. 201, Sector 2, Shipai Road, Taipei City 11217, Taiwan Email: [email protected]
Downloaded from ijs.sagepub.com at WESTERN OREGON UNIVERSITY on June 11, 2015
2
International Journal of Surgical Pathology
Figure 1. The ovarian immature teratoma. (A) Haphazard distribution of tissue from 3 germ layers (20×). (B) Primitive neuroectodermal epithelium (200×). Hematoxylin and eosin stain.
Figure 2. Gliomatosis peritonei. (A) Aggregates of mature glial tissue surrounded with mesothelial cells in the peritoneal implant (hematoxylin and eosin stain, 200×). (B) The glial nodule was immunoreactive for glial fibrillary acidic protein (200×).
Discussion Although gliomatosis peritonei has been reported in association with teratomas of endometrium,5 stomach,6 or even as a complication of ventriculoperitoneal shunt in the absence of teratoma,7 most cases of gliomatosis peritonei occur in the setting of ovarian immature teratoma. Intrathoracic glial implantation associated with ovarian immature teratoma is exceedingly rare. Only 1 case was reported previously in English literature. In that case, an ovarian immature teratoma with gliomatosis peritonei and a 2-cm pleural nodule was found in a 12-year-old girl. The pleural implant was composed of mature glial tissue, but no lymphovascular glial emboli were found.8 Two theories on histogenesis of gliomatosis peritonei have been proposed. The first one suggests the peritoneal glial implants arise from the primary teratoma, either by direct extrusion from ruptured tumor capsule or through angiolymphatic spreading.1,9 An alternative theory suggests the origin of peritoneal glial tissue is not from the primary teratoma but via the metaplasia of pluripotent Müllerian stem cells residing on the peritoneal surface or adjacent mesenchymal tissue.10 The metaplastic theory is
supported by molecular studies demonstrating the peritoneal glial implants are genetically distinct from the associated teratoma. Normal somatic tissue contains genetic alleles contributed from both maternal and paternal origins, whereas most ovarian teratomas contain duplicated maternal genetic materials.11 By genotyping the polymorphic microsatellite loci, Ferguson et al12 and Kwan et al13 revealed the glial implants exhibited heterozygosity at many microsatellite loci, whereas the associated teratoma showed homozygous patterns, indicating their nonclonal relationship. Although only 7 cases from both studies have been analyzed due to the rarity of gliomatosis peritonei, the results provide compelling evidence that most, if not all, gliomatosis peritonei are derived from nonteratomatous somatic cells rather than the result of direct spreading of mature glial tissue from the primary teratomas. The pathogenesis of intrathoracic glial implantation might be similar to gliomatosis peritonei via a metaplastic process. Alternatively, the pleural implants might be the consequence of direct angiolymphatic spreading from the existing gliomatosis peritonei. In the single case reported
Downloaded from ijs.sagepub.com at WESTERN OREGON UNIVERSITY on June 11, 2015
3
Wu et al References
Figure 3. Presence of glial emboli in the lymphovascular channels at the periphery of the pleural implant (hematoxylin and eosin stain, 40×).
previously, no lymphatic tissue was found in the intrathoracic nodule and the authors were in favor of the metaplastic theory.8 In our case, however, glial emboli in the pleural implant were clearly demonstrated, indicating the possibility of lymphovascular dissemination from either gliomatosis peritonei or the ovarian immature teratoma. Genotyping of microsatellite loci might shed light on the origin of the pleural glial implant. In summary, we describe an extremely rare case of ovarian immature teratoma associated with both gliomatosis peritonei and pleural glial implant. Albeit rare, pathologists should be aware of the possibility of extra-abdominal presence of glial implantation in the setting of ovarian immature teratomas. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
1. Robboy SJ, Scully RE. Ovarian teratoma with glial implants on the peritoneum: an analysis of 12 cases. Hum Pathol. 1970;1:643-653. 2. Fortt RW, Mathie IK. Gliomatosis peritonei caused by ovarian teratoma. J Clin Pathol. 1969;22:348-353. 3. Harms D, Jänig U, Göbel U. Gliomatosis peritonei in childhood and adolescence: clinicopathological study of 13 cases including immunohistochemical findings. Pathol Res Pract. 1989;184:422-430. 4. Kurman RJ, Carcangiu ML, Herrington CS, Young RH, eds. World Health Organization Classification of Tumours of Female Reproductive Organs. Lyon, France: IARC Press; 2014. 5. Ansah-Boateng Y, Wells M, Poole DR. Coexistent immature teratoma of the uterus and endometrial adenocarcinoma complicated by gliomatosis peritonei. Gynecol Oncol. 1985;21:106-110. 6. Coulson WF. Peritoneal gliomatosis from a gastric teratoma. Am J Clin Pathol. 1990;94:87-89. 7. Hill DA, Dehner LP, White FV, Langer JC. Gliomatosis peritonei as a complication of a ventriculoperitoneal shunt: case report and review of the literature. J Pediatr Surg. 2000;35:497-499. 8. Lipskar AM, Rothstein DH, Soffer AZ, Edelman M, Glick RD. Intrathoracic glial implants in a child with gliomatosis peritonei. J Pediatr Surg. 2009;44:1817-1820. 9. El Shafie M, Furay RW, Chablani LV. Ovarian teratoma with peritoneal and lymph node metastases of mature glial tissue. J Surg Oncol. 1984;27:18-21. 10. Dallenbach-Hellweg G. Critical commentary to Gliomatosis peritonei combined with mature ovarian teratoma. Pathol Res Pract. 1995;191:1037. 11. Surti U, Hoffner L, Chakravarti A, Ferrell RE. Genetics and biology of human ovarian teratomas. I. Cytogenetic analysis and mechanism of origin. Am J Hum Genet. 1990;47: 635-643. 12. Ferguson AW, Katabuchi H, Ronnett BM, Cho KR. Glial implants in gliomatosis peritonei arise from normal tissue, not from the associated teratoma. Am J Pathol. 2001;159: 51-55. 13. Kwan MY, Kalle W, Lau GT, Chan JK. Is gliomatosis peritonei derived from the associated ovarian teratoma? Hum Pathol. 2004;35:685-688.
Downloaded from ijs.sagepub.com at WESTERN OREGON UNIVERSITY on June 11, 2015
