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Oligodendroglioma arising in the glial component of ovarian teratomas: a series of six cases and review of literature
  1. Nasir Ud Din1,
  2. Aisha Memon1,
  3. Kanwal Aftab2,
  4. Zubair Ahmad1,
  5. Rashida Ahmed1,
  6. Sheema Hassan1
  1. 1Department of Pathology and Microbiology, Aga Khan University Hospital, Karachi, Pakistan
  2. 2Department of Pathology King Abdul Aziz Specialist Hospital, Taif, Riyadh, Saudi Arabia
  1. Correspondence to Dr Nasir Ud Din, Department of Pathology and Microbiology, Aga Khan University Hospital, The Aga Khan University, P.O. Box 3500, Stadium Road, Karachi, Sind 54000, Pakistan; nasir.uddin{at}aku.edu

Abstract

Aims To report the exceedingly rare occurrence of oligodendroglioma in the glial component of ovarian teratomas.

Methods Six cases of oligodendrogliomas arising in the glial component of ovarian teratomas were studied and the literature was reviewed. Immunohistochemistry was performed by the Flex technique.

Results The ages of the patients ranged from 12 to 28 years (mean 21 years). Four tumours were located in the right and one in the left ovary. The size of the ovarian cysts ranged from 7 cm to 29 cm (mean 19.6 cm). Four cases arose in immature and two cases in mature teratomas. In all cases, oligodendroglioma was WHO grade II. On immunohistochemistry, glial fibrillary acidic protein stain was positive in all cases. The Mib 1 (Ki 67) proliferative index was low and the tumour cells were negative for synaptophysin. Follow-up was available in five patients and ranged from 1 to 42 months. Two patients died of disease after 1 and 36 months of diagnosis, respectively. In both these cases oligodendroglioma arose in an immature teratoma. The remaining three patients are alive with a follow-up of 4–42 months.

Conclusions Oligodendroglioma arising in the glial component of ovarian teratomas is exceedingly rare. Ovarian teratomas should be extensively sampled and carefully evaluated to rule out the possibility of a glial tumour. This is the single and largest series of oligodendrogliomas arising in ovarian teratomas. The prognosis is good for oligodendrogliomas arising in mature teratomas compared with those arising in immature teratomas, although long-term follow-up is needed to determine the exact behaviour.

  • Autopsy pathology
  • breast pathology
  • cancer
  • genitourinary pathology
  • glial component
  • gynaecological pathology
  • head and neck cancer
  • histopathology
  • immunohistochemistry
  • neuropathology
  • oligodendroglioma
  • ovarian teratoma
  • tumour markers

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The term teratoma (from the Greek teratos for monster) was first coined by Virshow1 for a sacroccocygeal growth. Teratoma is the most common germ cell tumour derived from two or more germ layers (ectoderm, mesoderm or endoderm). Several types of benign and malignant tumours developing in dermoid cysts have been reported. Malignant transformation in a mature cystic teratoma (MCT) is reported in 1–2% of all cases,2 mostly in postmenopausal women.3 Any component of the derivatives of three germ cell layers of a MCT can undergo malignant transformation, but this change occurs most commonly in the epithelial component and carcinomas predominate.3 Squamous cell carcinoma is the most common form (80%),4 followed by adenocarcinoma.5 The malignant transformation is accompanied by complex chromosomal aberrations.6

Neuroectodermal tumours arising in teratomas are very rare and fewer than 40 cases have been reported. The ages of the patients ranged from 6 to 69 years (mean 28 years). These tumours include primitive neuroectodermal tumour, medulloblastoma and glioblastoma multiforme.3 Oligodendroglioma arising in a teratoma is exceptionally rare and so far only four case reports7–10 in ovarian and two in extragonadal teratomas11 ,12 have been published in the literature. Here, we report six cases of oligodendrogliomas arising in ovarian teratomas.

Materials and methods

We retrieved six cases of oligodendrogliomas arising in ovarian teratomas from the surgical pathology files at Aga Khan University Hospital, Karachi, Pakistan. Since this was a retrospective study and did not involve actual patients, approval from the Hospital Ethics Committee was not sought. However, consent from the patients was obtained. For light microscopy, all specimens were fixed in 10% buffered formalin and processed routinely for paraffin wax embedding. Five-micron thick sections were stained with haematoxylin and eosin. The tumours were analysed with respect to mature or immature component, cellularity, nuclear atypia, mitosis, necrosis and vascular endothelial proliferation. Clinical data were noted from the surgical pathology reports and follow-up was obtained by telephone communication with the patients.

For immunohistochemistry sections were dewaxed, rehydrated, and moistened with running tap water. The sections were pretreated in a microwave oven at 450W for 20 min with target retrieval solution of high pH; they were then incubated with antibodies on an automated immunostaining system (Dako autostainer plus Produkionsvej 42 DK-2600 Glostrup Denmark) for 25 min at room temperature. Immunohistochemical studies were performed with the Flex technique using the following antibodies: glial fibrillary acidic protein (monoclonal; dilution 1:200; Dako Cytomation), synaptophysin (monoclonal; dilution 1:50; Dako Cytomation) and MIB 1 (monoclonal; dilution 1:200; Dako Cytomation).

Results

Clinical and gross features

Case 1

A 22-year-old woman presented with a 4-month history of pain in the abdomen and irregular menstruation. Ultrasound revealed a complex right ovarian cyst. She underwent cystectomy. The cyst grossly measured 12×10 cm containing hair tufts, bone and mucoid material.

Case 2

The salpingo-oophorectomy specimen of a 15-year-old female patient was received for histopathology. On opening, a 7×6.5-cm uniloculated cyst was seen filled with thick yellowish cheesy material with matted hair. A 5-cm solid area was seen composed of cartilaginous and fatty areas (figure 1).

Figure 1

Gross appearance of the ovarian cyst (case 2). The cyst contained yellow fat and hair shaft. This figure is produced in colour in the online journal; please visit the website to view the colour figure.

Case 3

A 25-year-old woman presented with gradual abdominal distension and pain for 12 months. Ultrasound abdomen revealed a huge left ovarian cyst. Cystectomy was done and the cyst measured 29×22 cm. Cut surface revealed a multiloculated cyst filled with clear serous fluid admixed with thick cheesy material and hair tufts. A 10×9 cm solid area with bony cut surface was also seen.

Case 4

A 28-year-old woman presented with a history of painless abdominal distention for 7 years. On examination, a large non-tender mass extending from the pubis to the epigastric region was noted. On exploration, a large right and small left ovarian masses were seen; there was moderate ascitis with peritoneal seedlings. The masses were resected and sent for histopathological examination. The right ovarian multinodular mass measured 24×15.5 cm. The cut surface was variegated. Nodular tan and firm to hard areas and hair shafts were also seen. The left ovary measured 7×5.5 cm with cut surface exhibiting thick cheesy material admixed with hair.

Case 5

A 12-year-old girl presented with a right ovarian mass. The received specimen showed a 13×11-cm solid cum cystic ovarian mass. The solid areas were hard to calcified. The cystic spaces were filled with serous to haemorrhagic fluid (figure 2).

Figure 2

Solid cum cystic cut surface with grey and haemorrhagic areas (case 5). This figure is produced in colour in the online journal; please visit the website to view the colour figure.

Case 6

A 24-year-old woman presented with a 6-month history of pain and swelling in the right lower side of the abdomen. The received ovarian cyst measured 23×17 cm. The cut surface revealed a uniloculated cyst filled with serous fluid. A 2.5×1.5-cm solid area was also seen.

Histological features

Histological examination of all cases showed teratomatous lesions composed of derivatives of all three germ cell layers, ie, cartilage, bone, bone marrow, epidermis and underlying adnexae, keratin flakes, adipose tissue, muscle, stratified squamous, respiratory and intestinal epithelium, salivary gland acini, choroid plexus epithelium and glial tissue. Cases 1, 2, 4 and 5 showed foci of neuroepithelium and immature cartilage in varying proportions. The glial component showed scattered foci composed of sheets of monomorphic cells delineated by fine vasculature. The cells demonstrated perinuclear halos imparting a ‘fried egg’ appearance (figures 3 and 4). No significant cytological atypia, vascular endothelial proliferation or necrosis was seen. The contralateral (left) ovary of case 4 also showed MCT.

Figure 3

(A) An area of proliferation of oligodendrocytes with calcifications adjacent to mature adipose and fibrocollagenous tissue and cartilage (case 2, H&E, scanning magnification). (B) High power examination shows oligodendrocytes with perinuclear clearing (case 2, H&E, 10× magnification). This figure is produced in colour in the online journal; please visit the website to view the colour figure.

Figure 4

(A) Oligodendroglioma adjacent to seroumucinous glands and ciliated columnar lining (case 4, H&E, 4× magnification). (B) High power shows sheets of oligodendrocytes and chicken-wire type vessels (case 4, H&E, 10× magnification). (C) Immunohistochemical stain glial fibrillary acidic protein positivity in oligodendroglioma (case 4, immunoperoxidase, 20×). This figure is produced in colour in the online journal; please visit the website to view the colour figure.

Immunohistochemical results

The tumour cells were positive with immunohistochemical stain, glial fibrillary acidic protein and negative with synaptophysin. The Ki 67 (MIB 1) index was 2–4%. Based on morphology and immunohistochemical profile, a diagnosis of oligodendroglioma, grade II arising in the glial component of an ovarian immature teratoma was made in four cases and mature teratoma in two cases. No molecular analysis was performed.

Follow-up was available in five cases and ranged from 1 to 42 months. Chemotherapy was given to a 22-year-old patient (case 1), 32 months after recurrence of disease, but the patient died of the disease after five cycles of chemotherapy. The other patient who died of disease was a 28-year-old woman (case 4) who had oligodendroglioma in association with immature teratoma and MCT of the contralateral ovary. This patient died of the disease 1 month after the diagnosis. No chemotherapy was given. The remaining three patients are alive and well with a follow-up of 4 to 42 months. These patients received no additional treatment. These cases are summarised in table 1.

Table 1

Summary of cases of oligodendrogliomas arising in ovarian teratomas (n=6)

Discussion

Malignancy arising in a MCT is a rare complication (1–2%),9 mostly reported in postmenopusal women (mean 51–62 years).3 Carcinomas are the most common malignancy3 and squamous cell carcinoma is the most common type.9

Neural tissue is found in at least four-fifths of all teratomas.13 ,14 Astrocytes, ependymal tissue, nerve ganglia, nerve bundles, Schwann cells and choroid plexus may be seen within MCT.13 Oligodendrocytes were also reported in the teratoma.15 The development of malignancy in the neural tissue is exceptionally rare. The majority of the reported cases were glioblastoma multiforme, followed by diffuse fibrillary astrocytoma16 and a single case of pilocytic astrocytoma17 and choroid plexus papilloma.18 The majority of these developed in MCT with only rare cases arising in immature teratomas.16 The occurrence of oligodendroglioma in a teratoma is even rarer and only four case reports in ovarian7–10 and two in extragonadal teratomas11 ,12 have been found in the literature. These tumours probably arose in oligodendrocytes.

We report the single largest series of oligodendrogliomas arising in ovarian teratomas. The previous case reports are summarised in table 2. The ages ranged from 12 to 28 years (mean 21 years; median 23 years) in our series compared with 13–29 years (mean 22 years; median 23.5 years) in the earlier case reports. While only a single case in a child has been reported previously,3 our series includes two cases in children. Four (66%) cases of oligodendrogliomas in our series arose in immature teratomas and two (33.3%) cases in mature teratomas, in contrast to three (75%) cases of oligodendrogliomas in mature teratomas and only one in immature teratomas seen in earlier studies (see table 2). All reported cases in our series as well as in previous case reports were WHO grade II. Molecular analysis was done in only one reported case, and showed loss of heterozygosity on the long arm of chromosomes 19 and 10.8

Table 2

Reported cases of oligodendrogliomas in ovarian teratomas (n=4)

The size of ovarian cysts in our series ranged from 7 to 29 cm (mean 19.6 cm) and in previous published (three cases) reports ranged from 6 to 24 cm (mean 11.3 cm). Four of our cases were located in the right ovary and one in the left ovary. In the reported cases, two were located in the right ovary and one in the left ovary. Laterality was not known in one of our cases and in one of the previously reported cases.

Surgery was the mainstay of treatment in the reported cases and no additional treatment was given. Whereas gross total resection is the treatment of choice in the central nervous system grade II oligodendroglioma, there is no agreement on the treatment of oligodendroglioma arising in an ovarian MCT, because very few cases have been reported in the literature.7 However, we feel that immature teratomas should be treated with chemotherapy in the routine manner as it proved fatal in two of our cases. In five of our patients, no additional treatment was given. In one case, chemotherapy was instituted after the recurrence of disease, but the patient died of disease. Like Jung et al.11 we also believe the cause of death in this case was the immature teratoma component and not oligodendroglioma. Follow-up was available in five of our cases and ranged from 1 to 42 months (mean 17.6 months). Two patients died of disease at 1 and 36 months after diagnosis, respectively. In both, oligodendrogliomas arose in immature teratomas. MCT of the contralateral ovary was also present in case 4. The follow-up of the earlier reported cases ranged from 9 to 48 months (mean 22.7 months). All patients were alive during the reported follow-up.

Conclusion

In summary, oligodendrogliomas arising in the glial component of ovarian teratomas are exceedingly rare and only four case reports are available in the literature. The glial component should be carefully evaluated and more sections from the glial component should be submitted to rule out the possibility of a glial tumour arising in the glial component. We report the single largest series of oligodendrogliomas arising in ovarian teratomas. The prognosis is good with oligodendrogliomas arising in mature teratomas compared with immature teratomas, although long-term follow-up is needed to determine the exact behaviour.

Take-home messages

  • Epithelial malignancies arising in ovarian teratomas are common compared with glial tumours.

  • Glial tumours tend to develop in younger patients in contrast to epithelial tumours, which mostly occur in postmenopausal patients.

  • The prognosis is worse for oligodendrogliomas developing in immature teratomas compared with mature teratomas.

References

Footnotes

  • Competing interests None.

  • Patient consent Obtained.

  • Provenance and peer review Not commissioned; externally peer reviewed.