Conservative Approach in Gynecologic Malignancies

Abstract

Objective: This review was undertaken with the purpose of highlighting the options of a conservative approach in the management of gynecologic cancers so that clinicians exhibit some restraint before deciding on extensive surgeries as the management option. Background: Ovarian function and fertility are the main concerns while treating young women with gynecologic cancers. A conservative approach in management addresses these issues and aims at preserving the uterus and/or ovarian tissue. Early cervical and endometrial cancers, germ cell ovarian tumors, borderline ovarian tumors, and even early epithelial ovarian tumors are the gynecologic cancers where there is scope for a conservative approach. It may be in the form of radical trachelectomy for cervical cancer, medical (hormonal) treatment for endometrial carcinoma, or uterus/ovary-preserving surgeries for ovarian malignancies. On other end of the spectrum, there are advanced malignancies that may require extensive surgeries, which may further add to the morbidity. A less radical approach is in vogue in advanced ovarian malignancies where neoadjuvant chemotherapy followed by interval surgery is practiced instead of extensive primary debulking surgery. Similarly, the concept of sentinel lymph node sampling avoids unnecessary extensive lymphadenectomy in cervical cancers. Methods: A detailed literature search was made entering the terms conservative, fertility sparing, germ cell, borderline, epithelial, ovarian, trachelectomy, cervical, endometrial, neoadjuvant, and chemotherapy. Conclusions: Each relevant identified article was reviewed and a detailed overview of conservative options while managing gynecological malignancies is made. (J GYNECOL SURG 26:151)

Introduction

Genital tract malignancies in a female pose a great challenge to the treating fraternity. In general, cancer management is synonymous with radicalism, where the affected tissues are removed or destroyed surgically or by chemotherapy or radiotherapy. Obviously, this approach denies a younger woman of her fertility capacity. The ovarian destruction deprives her of estrogen, resulting in menopause-associated problems.

The success of chemotherapy in curing gestational trophoblastic neoplasia (GTN) revolutionized cancer therapy. Ovarian germ cell tumors are a group of malignancies that have a similar origin as GTN and a proven cure after conservative fertility-sparing surgical approach. A conservative approach aims at preserving the ovary(ies) and/or uterus for the purpose of future pregnancy or at least ovarian function. The surgery in these cases is confined to the removal of diseased tissues/ovary with preservation of the normal ovarian tissue and the uterus. Borderline ovarian tumors also have a fairly established scope for conservative management. Of late, such a conservative approach has been extended even to early invasive epithelial ovarian cancers as well as cervical cancers. Radical trachelectomy is the new addition to the management of early cancer cervix in young women who desire fertility preservation. Medical management has been effectively tried in women with receptor-positive endometrial carcinomas.

Another facet of this approach is conservatism in order to prevent management-related morbidity. The concept of “sentinel node sampling” in the management of carcinoma cervix or vulva has helped in minimizing extensive pelvic lymphadenectomy in early cervical cancers. “Neoadjuvant chemotherapy” has made optimal debulking possible in advanced ovarian malignancies where otherwise the primary debulking surgery would have been suboptimal or would have compromised the quality of life.

Surgical Conservatism in Gynecologic Malignancies

Carcinoma of the cervix

Radical trachelectomy

For a long time, radical hysterectomy with bilateral pelvic lymphadenectomy or pelvic radiation has been the standard treatment option available for invasive cancer of the cervix.

The past 20 years have seen significant changes in the attitude of the clinicians treating carcinoma of the cervix. Fertility-sparing surgery in the form of radical trachelectomy has been an addition to the treatment modalities available for early invasive carcinoma cervix. The approach provides an opportunity to conserve the uterus minus the cervix in those who strongly desire fertility after cancer treatment. The extent of the disease and the woman's preference are the major determinants to choose this as the treatment option. The ideal candidate is one with a small volume (<2 cm) International Federation of Gynecology and Obstetrics (FIGO) stage ≤IBI cervical cancer, with the disease confined to the cervix, with no evidence of spread to the uterine corpus or parametrium¹ (Table 1).

Table 1.

The Selection Criteria for Radical Trachelectomy ¹

• Desire to preserve fertility

• FIGO stage IA1 with presence of vascular space invasion or IA2 and IB1

• Lesion size less than 2-cm diameter confined to the cervix

• No involvement of the upper endocervical canal as determined by examination under anesthesia, colposcopy, and MRI

• No evidence of pelvic node metastasis

• Squamous cell carcinoma or adenocarcinoma histological subtypes

FIGO, International Federation of Gynecology and Obstetrics; MRI, magnetic resonance imaging.

The technique of radical trachelectomy² involves laparoscopic lymphadenectomy followed by vaginal resection of the cervix, parametrium, and upper one third of the vagina. The uterine corpus with the upper isthmus is left intact and the cervix below that is transected. Hence, it is important that the proximal end of the tumor is at least 1 cm away from the internal cervical os. A preoperative magnetic resonance imaging (MRI) scan is helpful in accurately identifying the internal os and the endocervical extent of the tumor.³

The pregnancies following this procedure have a significantly high risk of preterm labor and preterm premature rupture of membranes.⁴ Due to this reason, a permanent prophylactic circlage is placed at the end of trachelectomy.

As the isthmus is partially removed during trachelectomy, there is hardly any lower segment, hence the need to deliver the babies by classical cesarean section in the post-trachelectomy pregnancies.

Sentinel node biopsy

Sentinel node biopsy is a concept originally related to carcinoma of penis and later applied to other malignancies including carcinoma of vulva, breast, and cervix. The sentinel lymph node (SLN) is the first lymph node to which cancer is likely to spread from the primary tumor. A negative SLN biopsy result suggests that cancer has not spread to the lymph nodes, whereas a positive result indicates that cancer is present in the SLN and may be present in other lymph nodes in the same area. Thus, the procedure helps in planning lymphadenectomy.

The procedure uses either radioactive dye injected before surgery or intraoperative injection of isosulfan blue dye or both.^5,6,7 In preoperative lymphoscintigraphy, 99m-Tc-labeled phytate is injected into the uterine cervix, at the 3, 6, 9, and 12 o'clock positions, at a dose of 55–74 MBq in a volume of 0.8 mL and during surgery, lymphatic mapping is done with a handheld gamma probe.⁸

Intraoperative lymphatic mapping with blue dye is another alternative or is done in combination with lymphoscintigraphy.

In cancer of the cervix, sentinel nodes are found commonly in the interiliac, external iliac, or obturator groups. These may be one or two nodes on one or both sides of the pelvis.

The sentinel nodes, thus identified, are removed and subjected to frozen section. Further lymphadenectomy is planned based on the biopsy report. Lymphadenectomy is not done for women who are sentinel node negative, thus avoiding unnecessary extensive dissections.

Ovarian malignancy

Conservation of the uterus and the contralateral normal ovary has been the established treatment for germ cell tumors and borderline epithelial tumors of the ovary. Recently this approach has shown to be apt even for selected cases of early invasive epithelial ovarian tumors in the women desirous of fertility.⁹

Ovarian germ cell tumors (OGCT)

Germ cell tumors of the ovary are 40 times less common compared to the epithelial tumors but curable at all presenting stages of the disease. More commonly, these are seen in younger women and present at earlier stages where the disease is still restricted to one or both ovaries.

The surgical approach in malignant germ cell tumors includes optimal staging with unilateral salpingo-ovariectomy on the involved side, and preserving the uterus and the contralateral ovary.^10,11 Optimal staging translates to include: ascitic fluid/peritoneal washings for cytology, extensive search for pelvic/ abdominal deposits, pelvic and abdominal peritoneal biopsies, omentectomy, and pelvic lymph node biopsies. Biopsy of the contralateral normal-looking ovary is not recommended, for it is thought that the postsurgical adhesions caused by this step may negate the very purpose of the fertility-sparing approach.¹² However, it has been shown that biopsy does not result in adhesion-related fertility problems.¹³ When both ovaries are involved, ovariectomy on the side maximally involved and cystectomy on the side least involved, followed by chemotherapy may be the option. In a situation where both the ovaries appear to be involved without any chance of preserving normal ovarian tissue, preserving the uterus and offering in vitro fertilization with donor oocyte is still an option.¹⁴

For all OGCT except those with well-documented stage IA pure dysgerminoma, postoperative chemotherapy is recommended¹⁵ (Fig. 1). However, some studies have shown that optimal surgery and a close- surveillance program is safe practice for both stage I dysgerminomas and teratomas, with a 5-year survival rate of 95%.¹⁶

FIG. 1.

Conservative approach in malignant germ cell tumors. *If ovarian tissue could not be conserved, uterus preservation and assisted reproduction with donor oocyte may be the option.

Chemotherapy, which has the advantage of preserving fertility in the majority of cases, has replaced radiotherapy in the treatment of metastatic dysgerminoma. Low et al.¹⁷ reported 98.2% and 94.4% 5-year survival for stage I and II and for stage III and IV, respectively, in women who had conservative surgery with or without chemotherapy. They reported 14 healthy live births in the chemotherapy group.

Surgery alone is the acceptable treatment for sex cord stromal tumors of the ovary. However, those who have metastatic disease or Sertoli-Leydig tumors with poor differentiation or heterologous elements should receive chemotherapy.^10,11,18

Carcinoma of low malignant potential [borderline ovarian tumors (BOT)]

Borderline ovarian tumors account for 10%–15% of the epithelial tumors. Serous borderline tumors are the most common of these whereas mucinous, endometrioid, clear cell, and Brenner tumors are less common varieties. Approximately 50% of the serous borderline tumors and 80%–90% of the mucinous borderline tumors are confined to one ovary at diagnosis.¹⁹ However, nearly a third of the BOT are associated with peritoneal implants, and these implants are either noninvasive (80%) or invasive (20%).²⁰

The diagnosis is based on histopathological features wherein the tumor shows the malignant features in the form of nuclear atypia, epithelial stratification, and formation of micropapillary projections and benign features by the absence of stromal invasion.

There is another pathological finding that has gained significance. It is observed that the micropapillary pattern (characterized by highly complex exophytic papillary growth pattern without apparent stromal invasion) in the primary tumor is associated with higher frequency of exophytic ovarian growth, bilaterality, advanced stage, and invasive implants. Seidman et al.²¹ even named this entity “micropapillary serous carcinoma (MPSC)” and suggested this be treated as invasive carcinoma. However, other studies argue against this and opine that the micropapillary pattern is a part of borderline tumors with obviously a better prognosis compared to invasive serous carcinomas.²²

The survival rate for stage I serous borderline tumors is nearly 100%. Patients with advanced-stage serous BOT with noninvasive implants also have an excellent prognosis with near 100% survival.²⁰ However, serous BOT with invasive implants have a 30%–40% mortality rate and should be managed as carcinomas.

Similarly, mucinous borderline tumors (MBT), when confined to the ovary, have an excellent prognosis and in advanced stages are associated with poor survival possibility. Advanced-stage MBTs are commonly (80%) associated with pseudomyxoma peritonei, show aggressive behavior, and are now known to be of appendiceal origin.²⁰ They are bilateral, and have a mean diameter of less than 10 cm in contrast to the true ovarian MBTs, which are larger and unilateral.

Conservative approach

Frozen section is usually asked for during laparotomy for suspicious ovarian tumors, especially in younger women. When a diagnosis of serous borderline tumor is made at frozen section, careful exploration and staging with adequate tissue sampling (omentectomy/omental biopsy, pelvic and abdominal peritoneal biopsies, pelvic lymph node sampling) is indicated. When the disease is advanced, an attempt should be made to remove all the peritoneal implants to determine whether they are invasive. The primary tumor in the ovary should be dealt with by cystectomy or salpingo-ovariectomy in any combination, with a purpose of preserving the normal ovarian tissue at least on one side. Patients should be told that with ovarian cystectomy, there is a 10% chance of recurrence in the ipsilateral or contralateral ovary, which may require additional surgery.²³ When both of the ovaries are extensively involved, at least the uterus should be retained so that the patient still has the option of childbearing with the aid of assisted reproduction.

All stage I serous borderline tumors and the advanced-stage serous borderline tumors, in the absence of invasive implants or micropapillary serous carcinomas, require no further therapy. However, periodic follow-up is necessary. Postoperative platinum-based chemotherapy is recommended for advanced borderline serous tumors with invasive implants or those with noninvasive implants with gross residual disease.¹⁹ However, it is yet to be established whether postoperative chemotherapy is really beneficial in this group.

Molecular and genetic factors are the latest addition to the research in borderline ovarian tumors. Aneuploidies and overexpression of tumor-suppression gene p53 are associated with increased risk of progression/recurrence and death.

In case of mucinous borderline tumors, advanced disease and the presence of pseudomyxoma peritonei almost invariably indicates nonovarian origin of the disease. Advanced disease directly dictates an aggressive approach with detailed exploration and staging. Here, it is mandatory to remove the appendix and also to explore the gastrointestinal tract, pancreas, and biliary tract. A conservative approach may be the choice in case of borderline mucinous tumors confined to one ovary, without any pseudomyxoma peritonei.

Removal of the preserved ovary and uterus after completing pregnancies is not required for those who are compliant with follow-up²⁴ (Fig. 2).

FIG. 2.

Conservative management of borderline ovarian tumors.

Early Invasive Ovarian Cancer

About 15% of invasive epithelial ovarian cancer may occur in young women, who may desire preservation of fertility potential.

In the literature, several reports are found that have addressed the issue of fertility-sparing surgery in early invasive epithelial ovarian carcinoma.^25,26,27 Conservative surgery with preservation of the uterus and the contralateral normal ovary is recommended only for young women desirous of fertility, and having FIGO stage IA G1 disease.

While deciding on this recommendation, three major issues were considered: (1) possibility of occult involvement in the contralateral normal looking ovary, (2) possibility of relapse in the spared ovary, and (3) Does retaining the ovary and uterus act as an independent risk factor for disease progression and death? Benjamin et al. showed only 2.5% occult involvement in the normal-looking ovary in women who had stage I disease.²⁸ The incidence of recurrence in the remaining ovary was 7% on average.²⁷ Besides, it was shown that progression and death was independent of the approach. Even with aggressive surgery and adjuvant chemotherapy, some patients with early-stage cancer eventually relapse and die of tumor.²⁷

Optimal cancer treatment should get the foremost importance in cases of invasive epithelial ovarian tumors at any stage. Hence, fertility-sparing management should be offered only after thoroughly assessing the patient's real desire to retain fertility.

At surgery, complete surgical staging should be carried out. All the patients, except those with stage IA G1 disease, should receive postoperative chemotherapy. Whether conservative surgery has the role in other stage I invasive carcinoma (IB and IC or with higher grades) without compromising the prognosis is yet to be established. Some argue that the preserved ovary and the uterus be removed after the completion of pregnancy(ies) in order to reduce the risk of recurrence,²⁴ whereas others recommend close surveillance and expectant management in these young women for the preservation of the endocrine function²⁷ (Table 2).

Table 2.

Conservative Approach in Ovarian Malignancies in Young

Staging laparotomy with fertility-preserving surgery	Chemotherapy after surgery
Germ cell tumors	Required in all except pure dysgerminoma stage I
Borderline ovarian tumors
Stage IA serous	Not required
Advanced serous tumors with noninvasive implants	Required if gross residual disease after surgery
Advanced serous tumors with invasive implants	Required
Early stage mucinous tumors and without pseudomyxoma peritoneii	Required if gross residual disease after surgery
Early invasive epithelial ovarian tumors (stage IAG1)	Not required

In the context of ovarian malignancies, the conservative approach has another role. It is in the management of advanced epithelial ovarian malignancies that require extensive primary debulking surgery even at the cost of increased surgical morbidity. The ultraradical procedure for advanced cancer, in the attempt to achieve the least possible residual disease, may require bowel resections, diversions, diaphragmatic resections, or partial hepatectomy. This will significantly increase the surgical and postoperative morbidity and despite all the aggressiveness, optimal cytoreduction is possible only in 40% of the stage III or IV ovarian cancers.²⁹ Based on these views, the new modality of treatment called neoadjuvant chemotherapy was conceptualized and is becoming popular.³⁰ In this modality, based on the histopathology of the tumor biopsy, three to four courses of chemotherapy are given, after which the interval debulking surgery is done. The remaining courses of chemotherapy are given after the surgery. With this approach, optimal cytoreduction is possible in 70%–80% of the cases with a less invasive surgery and reduced morbidity.^29,31 The disease-free and survival rates were equivalent to that with conventional management.²⁹

Carcinoma of endometrium

Carcinoma of endometrium is one of the malignancies that presents at an early stage of the disease. The disease, though uncommon in the young, is prevalent in 8%–14% of women less than 45 years.

Fertility-sparing management of endometrial cancer includes mainly hormonal treatment. As hysterectomy is avoided during surgery, a uterine specimen is not available for evaluation and pathological staging. Therefore, staging is mainly by clinical evaluation with the aid of multidiagnostic modalities. Ultrasonography, MRI, endometrial sampling (hysteroscopy guided) and histopathological typing and grading and lymph node sampling are the few modalities that have a role in staging and management of the disease. CA 125 and the receptor status of the tumor may aid in prognosticating the disease.

The selection criteria³² for conservative hormonal therapy in endometrial cancer in the young include the following:

Adenocarcinoma grade 1

No myometrial and cervical invasion as documented by MRI (contrast-enhanced MRI demonstrated the highest diagnostic accuracy for determining myometrial invasion³³; it can also accurately assess cervical, adnexal, and nodal involvement³⁴)

No lymph node involvement after laparoscopic lymphadenectomy

Medroxyprogesterone acetate 200—800 mg daily is the most frequently used regimen for this purpose. During treatment, women should undergo endometrial evaluation every 1–3 months. With progesterone therapy for early carcinoma of endometrium, the resolution rate of 50%–80%³⁵ was reported. However, 30%–40% had recurrence; hence, it is suggested to do the definitive surgery after delivery. Ramirez et al.³⁶ noted that a median time of 12 weeks was required for the response after hormonal treatment and that the disease had a median time of 19 months to recur.

Chemotherapy, Radiotherapy, and Fertility

There is a general notion that the ovarian function wanes off after chemotherapy and radiotherapy. It is true with radiotherapy used for gynecological malignancies such as carcinoma of cervix and endometrium where the dose is much above the ovarian tolerance limit. It is noted that the tolerance limit varies with age and in women aged less than 40 years, this dose tolerance limit is 20–24 Gy with standard fractionation of 1.8–2.0 Gy/day.³⁷

Similarly, chemotherapy may cause premature menopause or in less severe form, temporary amenorrhea for a variable period. This effect depends on the dose and delivery schedule of the drugs, the additive/synergistic influence of the drug combinations, and the category of drug itself. Alkylating drugs such as cyclophosphamide, melphalan, and thio-tepa are known to cause premature ovarian failure. The most highly indicated agent in gynecologic malignancies, cisplatin, can also cause premature ovarian failure. However, it was shown that a total dose of <400 mg/m² is unlikely to cause ovarian failure.³⁸

The age of the patient also seems to have a significant influence on the effect of chemotherapy on ovarian function.³⁹ Higher ovarian reserve in a younger woman gives her the edge on her older counterpart when preservation of ovarian function after chemotherapy is a concern. About 75%–95% pregnancies are reported after treatment for malignant germ cell ovarian tumors^13,17 and an overall 60% cumulative pregnancy rate in all ovarian cancers.⁴⁰ There was no significant teratogenic effect of chemotherapy on pregnancy.¹³

Assisted Reproduction: Options for Fertility Preservation⁴¹

Ovarian transposition (oophoropexy) is the procedure in which ovaries may be positioned in the paracolic gutters or above the level of pelvic brim so that they remain outside the field during radiotherapy. Besides this embryo/oocyte cryopreservation or cryopreservation of ovarian cortical tissue are the other available options in younger women before starting the treatment for malignancy.

Conclusions

Gynecologists should be well aware of the conservative line of management while treating young women with gynecologic cancers. Surgical radicalism may deprive the woman of her ovarian and/or childbearing function, which could otherwise have been preserved by a conservative approach. Early cervical and endometrial cancers, germ cell ovarian tumors, borderline ovarian tumors, and even early epithelial ovarian tumors are the gynecologic cancers where there is scope for a conservative approach.

Footnotes

Disclosure Statement

No competing financial interests exist in association with this review article.

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Conservative Approach in Gynecologic Malignancies

Abstract

Abstract

Introduction

Surgical Conservatism in Gynecologic Malignancies

Carcinoma of the cervix

Radical trachelectomy

Sentinel node biopsy

Ovarian malignancy

Ovarian germ cell tumors (OGCT)

Carcinoma of low malignant potential [borderline ovarian tumors (BOT)]

Conservative approach

Early Invasive Ovarian Cancer

Carcinoma of endometrium

Chemotherapy, Radiotherapy, and Fertility

Assisted Reproduction: Options for Fertility Preservation 41

Conclusions

Footnotes

Disclosure Statement

References

Assisted Reproduction: Options for Fertility Preservation⁴¹