Low-Grade Serous Ovarian Tumors Debra A. Bell, MD Mayo Clinic and Mayo Medical School Rochester, MN

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1 1 Low-Grade Serous Ovarian Tumors Debra A. Bell, MD Mayo Clinic and Mayo Medical School Rochester, MN It is very appropriate to discuss low-grade ovarian serous neoplasms in a symposium in honor of Dr. Robert Scully, because he was in part responsible for placing the borderline category in the 1973 World Health Organization (WHO) Histological Classification of Ovarian Tumors, 1 and strongly believed in this category throughout his career. After the WHO Classification, Dr. Scully returned to consideration of low-grade serous tumors in the mid-1980s. Although he did not publish a large number of articles in this area, he and his coworkers published a number of important articles describing 1) the classification of peritoneal implants associated with serous borderline tumors as invasive and noninvasive and demonstrating their prognostic significance 2, 2) stromal microinvasion in serous borderline tumors 3, 3) primary peritoneal serous borderline tumors and low-grade carcinomas 4,5, 4) significant paper on lowgrade noninvasive serous tumors with a micropapillary pattern 6, and finally 5) an important contribution providing criteria for well differentiated low-grade serous carcinoma with extensive psammoma body formation termed serous psammocarcinoma 7. This discussion will focus on two of these areas, the classification of peritoneal implants associated with low-grade noninvasive serous neoplasms and the current data on low-grade serous tumors with a micropapillary/cribriform pattern. Mimics of both entities and diagnostically challenging issues will be addressed as well. Although it is now somewhat difficult to believe, in the 1970s and early 1980s, many pathologists, including those at the large cancer institutes, refused to make a diagnosis of an ovarian borderline tumor, classifying all such neoplasms as low-grade carcinomas. It was not uncommon for a woman with a borderline tumor to be treated with a total hysterectomy and subsequent chemotherapy, particularly if she had associated peritoneal implants. This was caused in part because at that time, it did not appear that any histological features of these tumors could predict who would fall into the minority of patients with an adverse outcome.

2 2 Peritoneal Implants of Noninvasive Low-Grade Serous Tumors In the 1980s, several groups examined the impact of the appearance of peritoneal lesions associated with serous borderline tumors on prognosis 2,8,9. Bell and Scully 2 demonstrated a statistically different prognosis between patients with noninvasive implants and those with invasive implants. The conclusion that the appearance of peritoneal implants is a major prognostic factor in low-grade non-invasive serous tumors is now widely accepted, although not all studies demonstrate these differences and there are some differences in the criteria used to diagnose implants 10. Although much emphasis and discussion of implants now focuses on poor prognosis implants and their terminology and diagnostic criteria, one of the major achievements of these early articles was the recognition that the majority of women with serous borderline tumors and peritoneal implants had a good prognosis and can be treated conservatively. Histologic features: Noninvasive implants (implants) show two histologic patterns. The first, which have been termed epithelial-type are composed of glands with intraglandular tufting, atypia and detached clusters of atypical epithelial cells that resemble typical serous borderline tumor, usually present within smoothly contoured mesothelial invaginations. The second pattern, termed desmoplastic-type noninvasive implants, consists of glands with intraglandular papillae, papillary tufts of epithelial cells and nests of cells interspersed within and often compressed by a predominating loose fibroblastic stroma that often is admixed with inflammatory cells. The stromal response typically predominates over the epithelial component and shows a well demarcated interface with underlying tissues. The epithelium in these two histologic patterns shows mild to moderate cytologic atypia and few mitotic figures. The epithelial cells are usually columnar-serous type epithelial cells that may be ciliated, or polygonal cells with a moderate amount of eosinophilic cytoplasm. The eosinophilic cells are present more frequently in desmoplastic implants. Single cells with eosinophilic cytoplasm may be seen in implants with predominating stroma, but do not indicate invasion. There is general agreement that patients with such implants have an excellent prognosis 2,10,11. Invasive implants (histologically identical to primary peritoneal low-grade serous carcinoma) show infiltration of tissue most frequently by elongate, branching micropapillae and solid nests of cells. Occasionally glands with a cribriform architecture are present. In contrast to noninvasive implants, the epithelium generally predominates over the associated stroma. The epithelium is usually cuboidal or polygonal with a high nuclear to cytoplasm ratio, although

3 3 nuclei are relatively uniform and small, visible nucleoli are common. Columnar epithelial cells are rare. Areas of disagreement: Although there is widespread agreement that evidence of invasion of underlying normal tissue in peritoneal lesions associated with serous borderline tumors is an adverse prognostic feature, the significance of proliferative epithelial features including micropapillae and solid nests of epithelial cells in lesions that do not show obvious tissue invasion remains somewhat unclear and these criteria are variably utilized 10. That the latter features were associated with an adverse prognosis was first proposed by K.A. Bell and colleagues 11 in Although several subsequent studies found these features to co-vary with tissue invasion, but not to have independent prognostic significance 12,13, these criteria have become generally incorporated into the definition of invasive poor prognosis implants by many groups. Such implants are variably classified as invasive implants, low-grade serous carcinoma or noninvasive micropapillary implants. It has been stated that all invasive or poor prognosis implants have the cytologic appearance of low-grade serous carcinoma, but on occasion, difficult cases do not show the typical micropapillarity or solid nests of cells of serous carcinoma, and appear to extend into underlying tissue. The prognosis of these rare lesions is unknown. Problems in differential diagnosis: 1. Noninvasive vs. invasive implants: Implants with tissue invasion show irregular infiltration of underlying tissue and usually have the appearance of low-grade serous carcinoma showing infiltrating micropapillae, solid nests of cells or nests with a cribriform pattern. Implants are often especially difficult to classify when they involve the omentum. Noninvasive implants follow the fibrovascular septae, are not expansile and do not infiltrate into surrounding fat. Invasive implants are irregular, expansile and extend into surrounding fat. Micropapillary features/solid nesting pattern assist in the diagnosis. 2. Papillary tufts or nests of epithelial cells surrounded by clefts in noninvasive implants must be distinguished from the solid nests of micropapillary implants. The papillary tufts often have scalloped borders, are composed of cells with columnar or eosinophilic cytoplasm, and appear compressed by the stroma. Solid nests of low-grade serous carcinoma usually have smooth contours with the surrounding tissue, are composed of

4 4 cuboidal cells with a higher nuclear to cytoplasmic ratio, and appear robust and uncompressed. 3. Elongate, irregular branching of eosinophilic epithelium in fibroblastic tissue vs. micropapillae. Occasionally, the epithelium in noninvasive implants may become quite complex, but this complexity is generally within glands and is composed of cells with eosinophilic cytoplasm. The glands, despite their complexity, are still a minor component of the proliferation and often appear compressed. Such complex glands are often at or near the peritoneal surface of the implant. 4. Lesions without classic micropapillary/solid nest appearance that appear infiltrative. The epithelium in these lesions is often columnar, both in the infiltrating glands that contain detached clusters of epithelial cells, and in the infiltrating papillary tufts. These are occasionally seen and pose difficult problems in classification. Their prognosis is unknown. Micropapillary/Cribriform Noninvasive Low-Grade Serous Neoplasms Of The Ovary A minority of low-grade, noninvasive serous tumors have a distinctive micropapillary appearance and are classified variably as serous borderline tumors/atypical proliferative tumors, micropapillary variant, micropapillary serous carcinoma, or noninvasive low-grade serous carcinoma. The clinicopathologic features of these tumors differ from the more common, typical serous borderline tumors. Micropapillary tumors occur in the same age range as typical serous borderline tumors, but are more frequently bilateral and associated with surface and peritoneal involvement, and may be and may be more commonly associated with invasive implants or peritoneal low-grade serous carcinoma. They are also frequently associated with stromal invasion, either in the ovarian tumor or in peritoneal lesions on extensive sectioning 6, The histologic features of these tumors compared to typical serous borderline tumors are outlined in Table 1.

5 5 Table 1. Histologic Features Typical Serous Borderline Tumor compared to Micropapillary Variant Feature Typical Micropapillary Architecture Papillae with irregular contours Hierarchical branching to tufts of atypical cells Smoothly contoured papillae Elongate micropapillae (5x longer than wide) emanating directing from cyst walls/papillae, scant stroma Cytology Moderate N:C ratio Columnar, cuboidal or polygonal cells Variable nuclei High N:C ratio Polygonal cells Small, uniform nuclei Amount of epithelium 10% of epithelial volume in At least one focus of required for diagnosis otherwise benign-appearing serous cystadenoma confluent micrpapillarity > 5mm in dimension in a typical serous borderline tumor Controversial issues: 1. Follow-up data: There is general agreement that ovarian tumors of this type without stromal invasion and confined to the ovary have an excellent prognosis 6,14,16,20,21. The overall survival of patients with these tumors and peritoneal spread varies by study, with some studies showing a statistically significant higher mortality with micropapillary serous tumors that with typical serous borderline tumors 22 and others showing no statistically significant difference in survival 6,12,13,17,23,24. This may be due to relatively short follow-up durations in many of the studies. Some groups have reported an increased frequency of tumor recurrences 17,21,22, but other studies have not documented this finding 6,12,16,23,24. Many authorities believe that these recurrences frequently have the appearance of low-grade serous carcinoma, and several 17,21,22,24, but not all 6,12,13. 20, studies have corroborated this observations.

6 6 2. Nomenclature: Many diagnose these tumors as serous borderline tumors/apt, micropapillary variant, and other classify them as noninvasive low-grade serous carcinoma. Part of this controversy is due to differences in prognosis in different studies discussed above and part is due to fear that classification of these tumors as carcinoma, particularly when they are stage I, may lead to overtreatment. 3. The most important point in this debate is to transmit the information in an understandable format to the clinician. Differential diagnosis: 1. High-grade serous carcinoma with a micropapillary architecture may mimic a micropapillary borderline tumor. On high power, however, such neoplasms pleomorphic, high-grade nuclei. 2. Extensive tufting in a typical serous borderline tumor. On occasion, a typical serous borderline tumor will show extensive formation of detached clusters of cuboidal, columnar, and polygonal atypical cells in small clusters; however, elongate micropapillae are not seen. 3. Micropapillary-like tufting in typical serous borderline tumors. Typical serous borderline tumors, especially those with extensive tubal or eosinophilic metaplasia may form slender papillary tufts that are much longer than they are wide. These do not have the cytologic features of micropapillary tumors as the tufts are composed of columnar or polygonal cells with a moderate amount of cytoplasm in contrast to the scant cytoplasm seen in micropapillary tumors. Low-Grade Serous Carcinoma All authorities would classify a typical or micropapillary borderline tumor as invasive low-grade serous carcinoma if areas of stromal invasion measuring greater than 5 mm in greatest dimension are identified. Low-grade serous carcinomas confined to the ovaries are rare and their prognosis is good, although few studies have focused on this issue. The prognosis of higher stage low-grade serous carcinomas has been found to be worse than non-invasive micropapillary tumors 14, and the survival of patients with invasive or micropapillary peritoneal disease has been shown by many authors to be longer than that of patients with high-grade serous carcinomas but other groups have documented a higher death rate 28.

7 7 Stromal invasion is usually easily identified as solid nests and micropapillae obviously infiltrating the stroma in a haphazard fashion. Several more subtle forms of stromal invasion are rare and may be difficult to recognize including 29,30 : 1. Macropapillary pattern. Large papillae with plump fibrovascular cores lined by bland columnar cells are present in the stroma, often surrounded by a tissue cleft. They may be recognized by the inverted appearance of the epithelial cells, in which the apex of the cells is adjacent to the stroma. 2. Subtle infiltrating glands. On rare occasions, glands lined by only mildly atypical cuboidal to columnar epithelial cells are present somewhat haphazardly in an often sclerotic stroma and may be more difficult to identify as invasive. Conclusions A great deal of progress has been made regarding the pathogenesis, classification, and prognosis of low-grade serous neoplasms of the ovary since the beginning of Dr. Robert Scully s career. We now know that the majority of patients with ovarian serous borderline tumors have a good prognosis, even when extensive peritoneal implants are present and most patients only need surgical removal of the tumor. We know that invasive, low-grade serous carcinomas develop via different pathways than high-grade serous carcinomas and that low and high-grade serous carcinoma are essentially different diseases. Low-grade serous carcinomas arise from serous borderline tumors with frequent mutations in KRAS and BRAF with few chromosomal abnormalities and high-grade serous carcinomas are characterized by TP53 mutations and BRCA inactivation and high levels of chromosomal instability 31,32. It is likely that this important knowledge would not have been as easily obtained without the standardization of the category of borderline tumors by Dr. Scully and his co-authors in the 1973 WHO Histological Classification of Ovarian Tumors and his thoughtful observations on their biology.

8 8 References 1. Serov SF, Scully RE, Sobin LH. Histological typing of ovarian tumours. International Histological Classification of Tumours, No. 9. Geneva: World Health Organization; Bell DA, Weinstock MA, Scully RE. Peritoneal implants of ovarian serous borderline tumors. Histologic features and prognosis. Cancer. Nov ;62(10): Bell DA, Scully RE. Ovarian serous borderline tumors with stromal microinvasion: a report of 21 cases. Hum Pathol. Apr 1990;21(4): Bell DA, Scully RE. Serous borderline tumors of the peritoneum. Am J Surg Pathol. Mar 1990;14(3): Weir MM, Bell DA, Young RH. Grade 1 peritoneal serous carcinomas: a report of 14 cases and comparison with 7 peritoneal serous psammocarcinomas and 19 peritoneal serous borderline tumors. Am J Surg Pathol. Jul 1998;22(7): Eichhorn JH, Bell DA, Young RH, Scully RE. Ovarian serous borderline tumors with micropapillary and cribriform patterns: a study of 40 cases and comparison with 44 cases without these patterns. Am J Surg Pathol. Apr 1999;23(4): Gilks CB, Bell DA, Scully RE. Serous psammocarcinoma of the ovary and peritoneum. Int J Gynecol Pathol. 1990;9(2): McCaughey WT, Kirk ME, Lester W, Dardick I. Peritoneal epithelial lesions associated with proliferative serous tumours of ovary. Histopathology. Mar 1984;8(2): Michael H, Roth LM. Invasive and noninvasive implants in ovarian serous tumors of low malignant potential. Cancer. Mar ;57(6): Bell DA, Longacre TA, Prat J, et al. Serous borderline (low malignant potential, atypical proliferative) ovarian tumors: workshop perspectives. Hum Pathol. Aug 2004;35(8): Bell KA, Smith Sehdev AE, Kurman RJ. Refined diagnostic criteria for implants associated with ovarian atypical proliferative serous tumors (borderline) and micropapillary serous carcinomas. Am J Surg Pathol. Apr 2001;25(4):

9 9 12. Prat J, De Nictolis M. Serous borderline tumors of the ovary: a long-term follow-up study of 137 cases, including 18 with a micropapillary pattern and 20 with microinvasion. Am J Surg Pathol. Sep 2002;26(9): Longacre TA, McKenney JK, Tazelaar HD, Kempson RL, Hendrickson MR. Ovarian serous tumors of low malignant potential (borderline tumors): outcome-based study of 276 patients with long-term (> or =5-year) follow-up. Am J Surg Pathol. Jun 2005;29(6): Smith Sehdev AE, Sehdev PS, Kurman RJ. Noninvasive and invasive micropapillary (low-grade) serous carcinoma of the ovary: a clinicopathologic analysis of 135 cases. Am J Surg Pathol. Jun 2003;27(6): Burks RT, Sherman ME, Kurman RJ. Micropapillary serous carcinoma of the ovary. A distinctive low-grade carcinoma related to serous borderline tumors. Am J Surg Pathol. Nov 1996;20(11): Park J-Y, Kim D-Y, Kim J-H, et al. Micropapillary pattern in serous borderline ovarian tumors: does it matter? Gynecol Oncol. Dec 2011;123(3): Deavers MT, Gershenson DM, Tortolero-Luna G, Malpica A, Lu KH, Silva EG. Micropapillary and cribriform patterns in ovarian serous tumors of low malignant potential: a study of 99 advanced stage cases. Am J Surg Pathol. Sep 2002;26(9): Fauvet R, Demblocque E, Morice P, Querleu D, Darai E. Behavior of serous borderline ovarian tumors with and without micropapillary patterns: results of a French multicenter study. Ann Surg Oncol. Mar 2012;19(3): Prat J. Serous tumors of the ovary (borderline tumors and carcinomas) with and without micropapillary features. Int J Gynecol Pathol. Jan 2003;22(1): Longacre TA, Kempson RL, Hendrickson MR. Serous tumours of low malignant potential (serous borderline tumours): moving toward detente. Histopathology. Sep 2005;47(3): Chang S-J, Ryu H-S, Chang K-H, Yoo S-C, Yoon J-H. Prognostic significance of the micropapillary pattern in patients with serous borderline ovarian tumors. Acta Obstet Gynecol Scand. 2008;87(4):

10 Seidman JD, Kurman RJ. Subclassification of serous borderline tumors of the ovary into benign and malignant types. A clinicopathologic study of 65 advanced stage cases. Am J Surg Pathol. Nov 1996;20(11): Gilks CB, Alkushi A, Yue JJW, Lanvin D, Ehlen TG, Miller DM. Advanced-stage serous borderline tumors of the ovary: a clinicopathological study of 49 cases. Int J Gynecol Pathol. Jan 2003;22(1): Uzan C, Kane A, Rey A, et al. Prognosis and prognostic factors of the micropapillary pattern in patients treated for stage II and III serous borderline tumors of the ovary. Oncologist. 2011;16(2): Malpica A, Deavers MT, Lu K, et al. Grading ovarian serous carcinoma using a two-tier system. Am J Surg Pathol. Apr 2004;28(4): Bodurka DC, Deavers MT, Tian C, et al. Reclassification of serous ovarian carcinoma by a 2-tier system: a Gynecologic Oncology Group Study. Cancer. Jun ;118(12): Gershenson DM, Sun CC, Lu KH, et al. Clinical behavior of stage II-IV low-grade serous carcinoma of the ovary. Obstet Gynecol. Aug 2006;108(2): Fader AN, Java J, Ueda S, et al. Survival in women with grade 1 serous ovarian carcinoma. Obstet Gynecol. Aug 2013;122(2 Pt 1): McKenney JK, Balzer BL, Longacre TA. Patterns of stromal invasion in ovarian serous tumors of low malignant potential (borderline tumors): a reevaluation of the concept of stromal microinvasion. Am J Surg Pathol. Oct 2006;30(10): Silva EG, Deavers MT, Malpica A. Patterns of low-grade serous carcinoma with emphasis on the nonepithelial-lined spaces pattern of invasion and the disorganized orphan papillae. Int J Gynecol Pathol. Nov 2010;29(6): Vang R, Shih I-M, Kurman RJ. Ovarian low-grade and high-grade serous carcinoma: pathogenesis, clinicopathologic and molecular biologic features, and diagnostic problems. Adv Anat Pathol. Sep 2009;16(5): Prat J. Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchows Arch. Mar 2012;460(3):

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