International Ovarian Tumour Analysis (IOTA) Phase 5 (IOTA-5)

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Submit a question and our knowledgeable staff will respond. Department of Obstetrics and Gynecology, Apolinaska 18, 120 00 Prague, Czech Republic. Disclosures: The authors indicated no financial relationships. Compare the epidemiologic and reproductive risk factors in BOTs with those in ovarian cancers and describe the molecular background of development of BOTs. Use the pathological terminology with either original grouping of borderline category or new subclassification of BOTs and assess the major predictor of recurrence and survival.

Determine an appropriate diagnostic algorithm for patients with symptoms suggesting malignant ovarian tumors that will identify borderline ovarian tumors when present. This article is available for continuing medical education credit at CME. Abstract Borderline ovarian tumors represent a heterogeneous group of noninvasive tumors of uncertain malignant potential with characteristic histology. They occur in younger women, are present at an early stage, and have a favorable prognosis, but symptomatic recurrence and death may be found as long as 20 years after therapy in some patients. Three terms are currently used to refer to these tumors: borderline tumor, tumor of low malignant potential, and atypical proliferative tumor .

8 per 100,000 women per year . BOTs differ significantly from ovarian carcinomas with regard to percentile distribution of tumor histotypes, lower FIGO stage, excellent overall prognosis, younger age distribution, higher infertility rate, and a lower frequency of BRCA mutations. The increased incidence of BOTs within ovarian malignant tumors has been observed in recent decades worldwide together with slightly decreasing incidence of ovarian cancer . In Sweden, the incidence of BOTs increased from 1. In a review of 15 studies, which included a total of 948 patients, 69. Even though the prognosis for most patients with BOTs is excellent, a minority will have a more aggressive form and eventually die from their disease.


If survival is specified to major histological types, Sherman et al. A third of patients diagnosed with BOTs are younger than 40 years of age and frequently are candidates for fertility-sparing surgery . Borderline tumors are rarely seen in women with BRCA mutations . Other epidemiologic characteristics do not differ significantly between BOT and ovarian carcinomas, and epidemiological studies have also confirmed similar reproductive risk factors in BOTs as in ovarian cancers, except for higher frequency of infertility . Rather than a single hypothesis, an overlap in mechanisms involved in each hypothesis may more likely explain the reproductive risk factors in full. Epithelial ovarian tumors, including borderline tumors, represent a rather heterogeneous group with common origins in tubal or ovarian surface epithelium or epithelial inclusion cysts. Tumors of the same morphology can be found in all structures developmentally derived from Müllerian ducts.

Many authors presume that these tumors originate from common stem or progenitor cells as a result of genetic and epigenetic changes. Tissue-specific stem cells: The replicative potential of these cells is comparable to the lifetime of the organism. They serve as a basic source for recovery of tissue of all the types of specialized cells and represent a minority population of the cells. Progenitor cells: These cells are the closest daughter cells of stem cells. They have limited but rapid replicative potential, and they can migrate and differentiate to specialized cells. They have distinctively limited replicative potential and their lifetime is only a small part of the organism’s lifetime.

They execute all specific tissue functions. The key features of tumor cells are unlimited replication, dedifferentiation, and loss of contact inhibition. During such an accumulation, the tumor population of first benign, then borderline and finally malignant characteristics could be stepwise generated. Thanks to recent molecular genetic studies, two major types of epithelial ovarian tumors can be distinguished. These types differ in molecular changes during carcinogenesis and in biological behavior. This classification describes different molecular pathways of carcinogenesis rather than relationship to any histotype.

Genomic changes of the tumor, rather than pure tumor morphology, seem to be a better tool for BOT biological behavior recognition. Projects addressing this field of research, however, are relatively rare. The prevalence of KRAS and BRAF mutations is higher in benign cystadenomas with minor portions of BOT than in pure benign cystadenomas. For mucinous tumors, mutations in KRAS, but not in BRAF, are typical.

A limited number of studies focused on molecular changes in peritoneal implants of BOT. Studies based on X chromosome inactivation patterns described distinct origins of ovarian tumor and implants, whereas others found the same molecular changes in ovarian tumor and implants. Analyses published so far have identified genomic areas and mechanisms involved in BOT carcinogenesis. However, results are still fragmentary and not suitable to be led into clinical practice. 5,807 patients provided by du Bois et al. Recent studies show that serous BOTs represent a wide spectrum of tumors with different biological potential . These implants are either invasive or noninvasive, depending on their microscopic appearance.

If the advanced stage is detected, careful examination of the appendix and intestine is warranted to exclude an occult extraovarian primary tumor simulating the primary ovarian mucinous borderline tumor with intraepithelial carcinoma. For that reason, the term seromucinous seems to be more accurate than endocervical-type of mucinous borderline tumor . Some metastatic mucinous carcinomas can manifest histological features suggestive of their primary ovarian origin. Endometrioid borderline tumors composed of atypical or histologically malignant endometrioid type glands or cysts are often set in a dense fibrous stroma with an absence of stroma invasion. They arise either from the surface ovarian epithelium or from endometriosis and have the potential to progress to low-grade endometrioid carcinoma.

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Clear-cell borderline tumors are characterized by atypical or histologically malignant glands or cysts lined by clear or hobnail cells set in a dense fibrous stroma with an absence of stromal invasion. The rarity of clear-cell borderline tumors could reflect the fact that the precursors of clear-cell carcinoma most often have the morphology of endometriosis with atypia rather than a clear-cell neoplasm. Borderline Brenner tumors have atypical or malignant features of the epithelium but lack stromal invasion. Mixed epithelial borderline tumors are composed of an admixture of two or more of the five major cell types: serous, mucinous, endometrioid, clear cell, and transitional cell. To date, there is no agreement on the definition of prognostic factors in terms of recurrence as invasive disease.

The pathological stage of disease and subclassification of extraovarian disease into invasive and noninvasive implants, together with the presence of postoperative macroscopic residual disease, currently appears to be the major predictor not only for recurrence and but also for survival . Some studies have not revealed the presence of invasive implants in contrast to noninvasive implants as a negative prognostic factor . It has been shown that stromal microinvasion, if unassociated with extraovarian invasive implants, has no effect on the rate of recurrence or the rate of progression to invasive disease, as confirmed in large meta-analysis . One promising prognostic factor seems to be the evaluation of DNA content. Borderline tumors with aneuploid DNA content have a worse prognosis for recurrence and survival. In large flow cytometric analysis on 370 BOTs reported by Kaern et al.

Lymph node involvement could not convincingly be confirmed to be an independent risk factor , and various investigators concluded from these results that systematic lymphadenectomy can be omitted. Primary ovarian borderline tumors usually affect patients at the reproductive age, when the preservation of childbearing potential plays a very important role. Concerning the indication of conservative treatment in higher stages of the disease, there is data on conservative management in serous BOT with peritoneal implants showing that the strongest prognostic factor in patients with an advanced-stage borderline tumor is again the use of conservative surgery, with a relative risk for recurrence of 5. Several retrospective studies reported on the outcome of BOTs after laparoscopy and compared these findings with the outcome after laparotomy. In a review conducted by du Bois et al. It seems that the higher risk of relapse is probably not associated with the reduction in overall survival . Therefore, current guidelines do not recommend adjuvant treatment, even for patients with advanced BOTs.

Most BOTs are detected by ultrasound. Ultrasound is broadly accepted as a highly accurate preoperative method in discriminating between benign and malignant adnexal masses if performed by experienced ultrasound examiner . Multilocular-solid tumor with papillae, rather smooth inner cyst wall, and regular septa and anechoic intracystic fluid. Multilocular-solid tumor with larger number of endophytic and exophytic tumor papillae, high intrapapillary flow density, and intracystic fluid with low-level echogenicity. Mucinous intestinal-type BOTs have different sonographic features from other common borderline tumors. Some BOTs are barely distinguishable from benign or invasive ovarian tumors.

The mean age for BOT diagnosis is 10 years younger than that of epithelial ovarian cancer . The more detailed and noninvasive evaluation of angiogenesis can by made by the use of intravascular contrast agents, which improve the detection of low-volume blood flow by increasing the signal-to-noise ratio. Even though the findings of contrast-enhanced ultrasound examination differed between benign and malignant tumors in the studies addressing this topic, there was a substantial overlap in contrast findings between benign and borderline tumors . 3D image can help to evaluate the internal cyst wall of the mass and to look for irregularities or solid papillary projections.

There are known limitations to making specific diagnoses of BOTs, even in the hands of an ultrasound expert. Hyperechogenic implants surround the contralateral ovary without involvement of ovarian stroma. Because the other modern imaging technigues are also based on the assessment of tumor morphological and vessel patterns, their results are also limited by the overlap of macroscopic features between benign and malignant ovarian tumors. For that reason, there is no additional benefit to using conventional computed tomography, magnetic resonance imaging, or even positron emission tomography in the diagnosis of BOTs. These approaches lead to extra costs and patient discomfort. Indeed, there is a high risk of false-positive CA125 results due to a variety of clinical variables, such as menstruation, ovulation, endometriosis, liver disease, inflammatory disease, and functional cysts, which may potentially lead to a large number of unnecessary ultrasound examinations and interventions. 1990 , did not perform well for patients with BOTs.

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The RMI is a scoring system derived from a logistic regression formula that combines menopausal status with the serum CA125 level and ultrasound variables. For such masses, it is therefore necessary to use methods other than subjective assessment. The majority of patients with BOTs are frequently diagnosed during their reproductive age. For these patients, therapeutic decisions regarding fertility-sparing surgery, treatment of infertility or premature hormonal deprivation, intra- and postoperative morbidity, and adjuvant chemotherapeutic treatments are particularly pertinent . Currently, no prospective randomized trials are available for clinical management. The exception to this rule is very young patients for whom the preservation of the maximum amount of ovarian tissue is attempted and the possible recurrence can be detected in a timely manner by close follow-up performed optimally by transvaginal scan. A random wedge biopsy of the contralateral ovary to exclude an occult concurrent lesion is also not advised because of the risk of postoperative periovarian adhesions leading to the mechanical factor of sterility and low diagnostic rate related to a blind section of macroscopic normal ovary .

If a relapse in the remaining ovary occurs, further conservative management may be offered to patients who plan further pregnancies. However, if at the time of clinical relapse an invasive disease is found, complete debulking is recommended without sparing fertility. Intraoperative Diagnosis and Staging To establish a complete FIGO staging, a combination of intraoperative exploration of the entire abdominal cavity should be conducted, with peritoneal washings, omentectomy, multiple peritoneal biopsies, and complete resection of all macroscopic suspected lesions. For resection of the primary tumor, bilateral salpingo-oophorectomy in combination with hysterectomy is recommended.

Optimal staging allows a correct pathological diagnosis to be obtained based on the entire tumor tissue and to define a group with a higher risk of recurrency. The staging surgery could be performed at the time of surgical treatment of the ovarian tumor when fresh frozen section analysis has confirmed the diagnosis of borderline tumor or during a restaging surgery when the borderline tumor was diagnosed by permanent histological analysis after the first surgery. Although there is widespread agreement on the histologic appearances of BOTs, it must be recognized that extensive specimen sampling is required to firmly establish the diagnosis, especially in mucinous tumors. This sampling is not always possible during intraoperative diagnosis, which needs to be recognized by both the pathologist and the operating surgeon to minimize inappropriate initial surgical therapy. There is a great deal of debate regarding the prognostic benefit of complete staging if macroscopic exploration is normal—in particular, whether omentectomy, hysterectomy, and appendectomy should be performed in such a situation.

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The omentum is the most likely site for invasive implants . Some authors have questioned the role of hysterectomy in cases where no peritoneal implants on the surface of the uterine serosa are present . BOTs who underwent hysterectomy in addition to bilateral adnexectomy . Laparoscopy is more frequently used for conservatively treated patients. Laparoscopic management of borderline ovarian tumors is associated with a higher rate of cyst rupture and incomplete staging . To date, there is no clear evidence that chemotherapy can decrease relapse rates or improve survival in any subset of patients with diagnosed BOTs .

However, infertility is frequently observed in patients with BOTs. In cases with extensive tumor involvement of both ovaries or the remaining ovary with or without uterine serosa infiltration, fertility-sparing surgery may not be possible. However, the preservation of germ cells and other fertility techniques considering the patient’s desire must be taken in account. A conceptual framework for managing concerns about fertility at the time of malignant tumor diagnosis is presented in a review conducted by Jeruss and Woodruff . HRT should be offered to these patients . If the preservation of fertility is not desired, bilateral salpingoophorectomy with or without hysterectomy is performed. When extraovarian recurrence in the form of borderline tumor or invasive disease occurs, extensive cytoreductive surgery, in line with the surgical management of primary ovarian cancer, is the treatment option of choice.

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Regular and intensive follow-up of the patients is essential for the early detection of recurrence in the form of borderline or invasive disease. This must be conducted for a longer period of time than for patients with ovarian cancer. In the case of very late recurrences, it may be difficult to distinguish between recurrence of the initial borderline tumor and a new primary tumor. However, this distinction does not seem to change further management and late recurrences are considered as a recurrence from the initial tumor. The importance of close follow-up is stressed in the literature. Studies specifically addressing the optimal follow-up modalities and more individualized surveillance strategies related to the higher risk group for recurrency are still missing. Transvaginal and transabdominal ultrasound are currently the optimal techniques for the surveillance of patients treated for BOTs because of their high ability to detect discrete intraovarian abnormalities as well as extraovarian implants when performed by an experienced examiner .

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Specifically in conservatively treated patients, recurrent tumors predominantly manifest in the ovaries, where the transvaginal scan plays an invaluable role, as was demonstrated by IOTA. The IOTA study also showed that CA125 and symptoms are of limited value in follow-up. There are also serious limitations of gynecologic examination after conservative treatment. The clinical examination may not allow discrimination of benign masses from malignant ones, especially if the malignant ones manifest as encapsulated lesions with a smooth surface . In many centers, the preoperative diagnosis of BOTs is insufficient and the role of ultrasound in this setting is underused.

MAPK pathways and allelic dysbalances on chromosome I. BOTs tending to aggressive biological behavior. Whether the micropapillary pattern alone implies an unfavorable prognosis is not confirmed by all investigators, but all studies revealed that micropapillary tumors, if associated with invasive implants, behaved more aggressively. The preoperative imaging method of choice is ultrasound. Serous borderline tumors and mucinous endocervical-like borderline tumors are more likely to evidence bilaterality than their benign counterparts, similar to that of early stage low-grade cancer. On the contrary, mucinous intestinal-type BOTs are usually unilateral, whereas bilaterality supports the suspicion of secondary ovarian involvement from the gastrointestinal tract. BOTs are difficult masses to correctly classify preoperatively because their macroscopic features may overlap with invasive and benign ovarian tumors.

A correct preoperative diagnosis is made only for one- to two-thirds of patients. Borderline ovarian tumors frequently affect women in their reproductive ages, and a more conservative surgery to preserve subsequent fertility is preferred. A conservative approach should be proposed to a select group of patients who wish to preserve fertility, with early-stage mucinous BOTs or completely resected serous BOTs with noninvasive implants, compliance to long-term follow-up, and awareness that there is a higher incidence of relapse compared with radical treatment. In such cases, the restaging procedure could be omitted in the absence of micropapillary pattern and if careful intraoperative exploration of the pelvis and abdomen and resection of all macroscopic lesions were performed initially.

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Laparoscopy could be employed in the management of BOTs, but only in the hands of experienced oncologic surgeons to reduce the risk of intraoperative tumor rupture, inadequate staging, and residual tumor disease left in situ, associated with higher recurrency rate. In cases of advanced or recurrent disease, adequate surgery with optimal primary or secondary debulking is needed. Follow-up should be based on ultrasound examination, which has proven to be the most effective current imaging method able to explore the pelvis as well as abdomen without any additional risk to patients. Special attention should be paid to the remaining ovary in conservatively treated patients. Borderline ovarian tumors represent a wide spectrum of tumors with different biological potential and uncertain malignant potential.