CASE REPORT

Pregnancy After Laparoscopic Bilateral Partial Ovarian Decortication for Stage IC Borderline Ovarian Tumour Ali Hassan Hamed, MD,1,2 Robert Emerson, MD,3 Leo Bonaventura, MD,4 Srdjan Saso, BSc, MRCS,5 Giuseppe Del Priore, MD, MPH1 Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Indiana University School of Medicine, Indianapolis IN

1

Department of Obstetrics and Gynecology, Assiut University, Egypt

2

Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis IN

3

Reproductive Medicine, American Health Network, Indianapolis IN

4

Institute of Reproductive and Developmental Biology, Imperial College, London, UK

5

Abstract Background: Fertility preservation techniques are a growing area of research as more women in the reproductive age group develop gynaecologic cancers. We report here a novel technique of fertility preservation used in the treatment of a patient with borderline ovarian tumour. Case: A 29-year-old woman with stage I borderline ovarian tumour was referred to our tertiary level hospital. She had a history of infertility and requested fertility preservation be considered in treatment decisions. We performed bilateral laparoscopic partial decortication of the ovaries, and the patient successfully conceived spontaneously following the procedure. Conclusion: Fertility-preserving surgery should be an option for young women with borderline ovarian tumours who wish to retain fertility. Removing abnormal ovarian tissue may restore fertility. The laparoscopic approach is safe and feasible for these patients.

Résumé Contexte : Les techniques de préservation de la fertilité constituent un champ de recherche en évolution, de plus en plus de femmes en âge de procréer étant atteintes de cancers gynécologiques. Nous nous penchons sur une technique novatrice de préservation de la fertilité utilisée dans le cadre de la prise en charge d’une patiente présentant une tumeur ovarienne à la limite de la malignité. Cas : Une femme de 29 ans présentant une tumeur ovarienne à la limite de la malignité de stade I a été orientée vers notre hôpital de niveau tertiaire. Elle présentait des antécédents d’infertilité et souhaitait que la préservation de la fertilité soit prise en Key Words: Pregnancy, borderline ovarian tumours, laparoscopy Competing Interests: None declared. Received on January 3, 2014 Accepted on March 13, 2014

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considération dans le cadre du processus de prise de décision quant au traitement. Nous avons pratiqué une décortication laparoscopique bilatérale partielle des ovaires et la patiente a été en mesure de connaître une grossesse spontanée à la suite de l’intervention. Conclusion : La chirurgie visant à préserver la fertilité devrait constituer une solution possible pour les jeunes femmes présentant une tumeur ovarienne à la limite de la malignité qui souhaitent demeurer fertiles. L’excision de tissus ovariens anormaux pourrait permettre de rétablir la fertilité. L’approche laparoscopique est sûre et praticable dans le cas de ces patientes. J Obstet Gynaecol Can 2014;36(9):826–829

INTRODUCTION

L

ow malignant potential or borderline ovarian tumours are epithelial ovarian tumours with slower rates of growth and lower rates of invasion and metastasis than malignant epithelial ovarian tumours. The World Health Organization defines them as “ovarian tumours exhibiting an atypical epithelial proliferation greater than that seen in the benign counterpart but without destructive stromal invasion.”1 We present here the case of a woman with secondary infertility and a low malignant potential tumour who conceived spontaneously after partial bilateral ovarian decortication. THE CASE

A 29-year-old woman with a history of two first trimester miscarriages presented with three years of secondary infertility. She was heterozygous for factor V Leiden

Pregnancy After Laparoscopic Bilateral Partial Ovarian Decortication for Stage IC Borderline Ovarian Tumour

Figure 1.

Figure 2.

mutation. She had smoked for 13 years and had previously used oral contraception for eight years. During evaluation for infertility, transvaginal ultrasound assessment showed the right ovary measuring 3.1 × 2.2 cm and the left ovary measuring 4.0 × 3.6 cm with four small cysts (mean diameters 1.8, 1.3, 1.2, and 1.9 cm).

The patient was discharged on the first postoperative day. Histopathology confirmed the diagnosis of borderline serous adenofibromatous ovarian tumour. The FIGO staging of the tumour was IC, as it involved both ovaries with surface excrescences.

The patient was subsequently prescribed oral contraceptives. Because the left ovarian cysts were still present at a follow-up ultrasound three months later, laparoscopy was performed, and bilateral ovarian masses were identified (Figure 1). The masses were biopsied and sent for histopathologic evaluation, which showed borderline serous adenofibromatous ovarian tumour. The patient was referred to a gynaecologic oncologist. She requested fertility preservation be considered in treatment decisions. Preoperative investigations showed a serum CA 19-9 of 37 U/L and serum CA-125 of 66 U/L. The patient underwent bilateral partial ovarian decortication by laparoscopy to remove all grossly visible tumours and to perform partial omentectomy and pelvic and para-aortic lymph node dissection (Figure 2). To perform ovarian decortication, the plane between the stroma of the ovary and the 2 to 3 mm thick cortex (the potential space between an ovarian cyst and the overlying capsule) was identified. This potential space was identified by slowly incising the cortex with scissors, and the tension in the cortex caused it to lift away from the underlying stroma. After an incision of a few millimetres was made, the plane was enlarged by placing one blade of the scissors into the potential space, and dissection of the cortex was facilitated. All visibly abnormal cortical tissue was removed, leaving approximately 30% of each ovary. Bleeding was minimal.

The patient conceived spontaneously following her first episode of menstrual bleeding approximately six weeks after surgery. Her pregnancy was uneventful until she developed preterm labour at 30 weeks’ gestation. The cervix dilated to 3 cm, but with bed rest labour did not progress. She presented in labour at 36+4 weeks and delivered vaginally. The male infant weighed 3030 g, with Apgar scores of 9 at one minute and 10 at five minutes. For three years the patient has remained symptom-free, and MRI, serum tumour markers, and physical examination indicate she has remained disease-free. DISCUSSION

Borderline ovarian tumours represent approximately 10% to 15% of all ovarian tumours.2 There is variability in the reported incidence of borderline ovarian tumours, mostly because of referral bias. Most reports come from tertiary centres managing higher numbers of cases than primary or secondary centres. The prognosis for patients with borderline ovarian tumour is reported to be favourable, with five-year overall survival rates for early-stage disease of approximately 98% and rates from 86% to 92% for more advanced disease.3 The etiology of borderline ovarian tumours has not yet been clearly established, but they appear to originate from the müllerian duct and surface epithelium of the ovary.4 SEPTEMBER JOGC SEPTEMBRE 2014 l 827

Case Report

With regard to risk factors for borderline ovarian tumours, Riman et al. found in a case–control study of 193 patients that nulliparous women had a greater risk of developing borderline tumours than parous women. The authors also found lactation to be protective.5 However, unlike invasive ovarian cancer, oral contraceptive use did not provide protection against the development of borderline tumours.5 Depending on histological characteristics, borderline ovarian tumours are classified as serous (50%), mucinous (46%), and mixed, endometrioid, clear cell, or Brenner tumours (3.9%).6 Serous borderline ovarian tumours are bilateral in 30% of cases and can be associated with extraovarian implants in 25% to 30% of cases.6 These implants can be benign (40%), non-invasive (35%), or invasive (25%), and these characteristics will in turn influence therapeutic options.6 Mucinous borderline ovarian tumours are classified as intestinal (85%) or endocervical/müllerian type (15%), depending on the nature of the epithelial lining.7 They can be associated with pseudomyxoma peritonei (10%), necessitating a thorough investigation of the gastrointestinal tract, with special attention to the appendix because this can be the primary tumour origin.7 In the case of lesions with broad densely fibrous papillae, as in this case, borderline ovarian tumours are also known as serous cystadenofibromatous tumours of low malignant potential. Microscopically, the internal surface of the cyst, and the fibrous stromal papillae are covered by columnar serous epithelium which is usually ciliated. Laminated calcifications (psammoma bodies) are frequently apparent.8 In addition, borderline ovarian tumours lack extensive cribriform or solid (confluent) growth or stromal invasion; the presence of either of these features is diagnostic of serous carcinoma.8 Surgical removal is the primary treatment for borderline ovarian tumours. As these tumours are more likely to affect younger women, who probably wish to conserve their fertility, and are usually diagnosed at an early stage,9 the option of fertility-preserving surgery must be discussed with these patients. The role of complete surgical staging of borderline ovarian tumours is still under debate. Some authors reported upstaging of apparent stage I borderline ovarian tumours in 12% to 47% of patients who underwent complete surgical staging.3,10 On the other hand, some surgeons do not perform comprehensive staging because survival rates remain very good even with advanced stage tumours.11,12 For stage I disease, conservative surgery consisting of unilateral salpingo-oophorectomy or cystectomy is an alternative in young women who want to preserve their 828 l SEPTEMBER JOGC SEPTEMBRE 2014

fertility. Women with advanced-stage disease or who have finished childbearing are best managed with radical surgery comprising peritoneal washings, total abdominal hysterectomy, bilateral salpingo-oophorectomy, complete peritoneal resection of macroscopic lesions, and, in cases of mucinous borderline ovarian tumours, appendectomy. Laparoscopy has proved feasible for performing surgery for borderline ovarian tumours, including radical and conservative surgery. In experienced hands, it has been found to be safe and effective for diagnostic and therapeutic purposes for early borderline ovarian tumours.13 Many studies have compared the safety of conservative and radical surgery in early stage borderline ovarian tumours.13–16 Recurrence rates have been slightly higher in patients undergoing fertility-sparing surgery than in those undergoing radical surgery, but fertility-sparing surgery does not reduce survival rates because most recurrent lesions are also borderline tumours, which can be cured with complete surgical resection. Thus, fertility-sparing surgery can be considered as a well-tolerated and feasible option in women with early-stage borderline ovarian tumours.17 In our case, we used a technique described by other authors for cryopreservation of ovarian cortical tissue in women with cancer.18 We have used this technique for the same purpose. Since this patient did not have a typical cystic borderline ovarian tumour, we performed partial decortication to remove the tumour completely. It is unclear how decortication could have been associated with restoration of her fertility. However, a similar effect has been reported in women with polycystic ovary syndrome who undergo ovarian drilling.19 Decortication is a simple technique that can be used to preserve fertility in treating women with borderline ovarian tumours. It should be considered as an option in carefully selected cases. Oncologists should be aware that cancer treatment and fertility preservation are not mutually exclusive.20 ACKNOWLEDGEMENTS

The woman whose story is told in this case report has provided written consent for its publication. REFERENCES 1. Tavassoli FA, Devilee P, eds. World Health Organization classification of tumours. Pathology and genetics. Tumours of the breast and female genital organs. Lyon: IARC Press; 2003. Available at: http://www.iarc.fr/en/publications/pdfs-online/pat-gen/bb4/ bb4-cover.pdf. Accessed July 7, 2014.

Pregnancy After Laparoscopic Bilateral Partial Ovarian Decortication for Stage IC Borderline Ovarian Tumour

2. Bell DA. Ovarian surface epithelial-stromal tumors. Hum Pathol 1991;22:750–62. 3. Gershenson DM. Clinical management potential tumours of low malignancy. Best Pract Res Clin Obstet Gynaecol 2002;16(4):513. 4. Harris R, Whittemore A, Itnyre J, Collaborative Ovarian Cancer Group. Characteristics relating to ovarian risk: a collaborative analysis of 12 US case-control studies. III Epithelial tumors of low malignant potential in white women. Collaborative Ovarian Cancer Group. Am J Epidemiol 1992;136:1204–11. 5. Riman T, Dickman PW, Nilsson S, Correia N, Nordlinder H, Magnusson CM, et al. Risk factors for epithelial borderline ovarian tumors: results of a Swedish case-control study. Gynecol Oncol 2001;83:575–85. 6. Winter WE 3rd, Kucera PR, Rodgers W, McBroom JW, Olsen C, Maxwell GL. Surgical staging in patients with ovarian tumors of low malignant potential. Obstet Gynecol 2002;100(4):671–6. 7. Cadron I, Leunen K, Van Gorp T, Amant F, Neven P, Vergote I. Management of borderline ovarian neoplasms. J Clin Oncol 2007;25(20):2928–37. 8. McCluggage WG. The pathology of and controversial aspects of ovarian borderline tumours. Curr Opin Oncol 2010 Sep;22(5):462–72. 9. Tinelli R, Tinelli A, Tinelli FG, Cicinelli E, Malvasi A. Conservative surgery for borderline ovarian tumors: a review. Gynecol Oncol 2006;100:185–91. 10. Fauvet R, Boccara J, Dufournet C, David-Montefiore E, Poncelet C, Daraï E. Restaging surgery for women with borderline ovarian tumors: results of a French multicenter study. Cancer 2004;100(6):1145. 11. Camatte S, Morice P, Thoury A, Fourchotte V, Pautier P, Lhomme C, et al. Impact of surgical staging in patients with macroscopic “stage I” ovarian borderline tumours: analysis of a continuous series of 101 cases. Eur J Cancer 2004;40(12):1842.

12. Rao GG, Skinner E, Gehrig PA, Duska LR, Coleman RL, Schorge JO. Surgical staging of ovarian low malignant potential tumors. Obstet Gynecol 2004;104(2):261. 13. Seracchioli R, Venturoli S, Colombo FM, Govoni F, Missiroli S, Bagnoli A. Fertility and tumor recurrence rate after conservative laparoscopic management of young women with early-stage borderline ovarian tumors. Fertil Steril 2001;76:999–1004. 14. Zanetta G, Rota S, Chiari S, Bonazzi C, Bratina G, Mangioni C. Behavior of borderline tumors with particular interest to persistence, recurrence, and progression to invasive carcinoma: a prospective study. J Clin Oncol 2001;19:2658–64. 15. Morice P, Camatte S, El Hassan J, Pautier P, Duvillard P, Castaigne D. Clinical outcomes and fertility after conservative treatment of ovarian borderline tumors. Fertil Steril 2001;75:92–6. 16. Ji H, Yliskoski M, Anttila M, Syrjänen K, Saarikoski S. Management of stage-I borderline ovarian tumors. Int J Gynaecol Obstet 1996;54:37–44. 17. Park JY, Kim DY, Kim JH, Kim YM, Kim YT, Nam JH. Surgical management of borderline ovarian tumors: the role of fertility-sparing surgery. Gynecol Oncol 2009; 113:75–82. 18. Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 2004; 364(9443):1405–10. 19. Hamed HO, Hasan AF, Ahmed OG, Ahmed MA. Metformin versus laparoscopic ovarian drilling in clomiphene- and insulin-resistant women with polycystic ovary syndrome. Int J Gynaecol Obstet 2010;108(2):143–7. 20. Chalian R, Licciardi F, Rebarber A, Del Priore G. Successful infertility treatment in a cancer patient with a significant personal and family history of cancer. J Womens Health (Larchmt) 2004;13(2):235–7.

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Pregnancy after laparoscopic bilateral partial ovarian decortication for stage IC borderline ovarian tumour.

Contexte : Les techniques de préservation de la fertilité constituent un champ de recherche en évolution, de plus en plus de femmes en âge de procréer...
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